Dendritic Growth in Somatosensory Region of Brain Cortex in Pigs Residing in a Simple or a Complex Environment

Temple Grandin
Dept. of Animal Science
Colorado State University
Fort Collins, Colorado 80523 USA

Dissertation, University of Illinois, 1989

Literature Review

A. Effects of Environmental Restriction and Complexity

Behavioral effects of environmental restriction

This will be a review of the scientific literature on the effect of either isolation or sensory restriction on animals after weaning. In all cases, prior to weaning, the animals were reared by their natural mothers. Therefore, any effect of sensory restriction was not confounded with the effects of maternal deprivation, which profoundly alters later behavior (Harlow and Zimmerman, 1959; Mason, 1960).

Isolated postweaning rearing conditions will increase the reactivity and excitability of rodents (Korn and Moyer, 1968; Valzelli, 1973; Riittenen et al., 1986). In the Korn and Moyer (1968) experiments on adult rats, four weeks of isolation in standard laboratory cages was less detrimental in these respects than fourteen weeks. Isolation heightened emotionality; isolated rats reacted violently when they were picked up.

Hyperexcitability has been documented in dogs kept in a sensory-restricted environment. Pairs of puppies residing in barren kennels become unusually aroused and excited when exposed to something new (Melzack, 1954), These puppies could hear and smell dogs in adjacent kennels, and the kennels were illuminated continuously so the puppies in a pair could see and interact with each other. Almost a year after being returned to a residential environment with a human family, the subjects were still hyperexcitable (Melzack, 1954) and electroencephalographic patterns from their brains indicated extreme arousal (Helzack and Burns, 1965).

Animals living in a barren or restricted environment will seek stimulation. During a four-hour experiment, rhesus monkeys in an opaque cage worked hard to discriminate between blue and yellow cards to operantly open a window for a brief glimpse into the rest of the laboratory (Butler, 1953). Rats residing in a barren environment will bar press more than those in an enriched environment (Ehrlich, 1959). The restricted environment consisted of five rats in a 60 x 30 x 23-cm wire cage. Enriched environment rats were raised in groups of ten in a two-tiered environment consisting of a 120 x 76 x 60-cm cage filled with playthings such as corks, tunnels, ramps, and platforms. During testing, each rat was placed individually in a Skinner box. Reinforcement for bar pressing consisted of either clicks or turning on a light.

Pigs residing in crates which were just wide enough to allow turning around at a flared end, turned around 11 to 12 times per day (McFarlane et al., 1988). Even animals which did not have to turn around to gain access to feed or water nevertheless did turn around about the same number times as did those which had to do so. This is presumptive evidence of the pig's need for a certain level of physical activity.

Pigs in intensive housing systems spend long periods sleeping, punctuated by brief periods of intense excited activity, as when a door slams or a person walks into the room. This behavior is similar to that of Melzack's puppies; in the restricted environment, they became very excited when minor changes were made in their cages (Melzack, 1954). Stallions kept in stalls without exercise were harder to handle than those given daily exercise (Dinger and Noiles, 1986).

Pigs reared in indoor pens with minimal contact with people were more excitable and difficult to load into a trailer than those reared outside with frequent contact with people (Warriss et al., 1983). Stolba and Wood-Gush (1980) found that pigs in barren pens with concrete floors reacted more strongly to and played longer with a tire than did those in straw-bedded pens.

Wood-Gush and Beilharz (1983) found that pigs in cages spent less time lying when their environment was enriched with a trough filled with dirt. Maybe pigs in more barren pens sleep longer to reduce the arousal level of an overly aroused nervous system. Zentall and Zentall (1983) suggested that autistic children withdraw from stimulation to prevent further arousal of an already overly aroused nervous system.

Central nervous system effects of environmental restriction

Environmental restriction has long-term effects on an animal's central nervous system (Helzack, 1969). Six months after being released from a sensory-restricted environment, young dogs still had electroencephalographic patterns which indicated an abnormally high level of arousal (Helzack and Burns, 1965).

The experiments reviewed in this paper support the hypothesis put forth by Walsh and Cummins (1975) that animals living in an enriched environment usually are less excitable than animals in barren surroundings. Restricting sensory input makes the nervous system of both humans and animals more sensitive and more reactive to external stimulation. Schultz (1965) stated: "When stimulus variation is restricted, central regulation of threshold sensitivities will function to lower sensory thresholds. Thus, the organism becomes increasingly sensitized to stimulation in an attempt to restore balance." Walsh and Cummins (1975) concluded that animals in an enriched environment are subject to greater arousal during rearing and therefore are less likely to exhibit over arousal in a novel or highly stimulating environment.

Sensitization to external stimuli occurs within the central nervous system. Placing a small cup on a person's forearm to block tactile stimulation for one week increased tactile sensitivity on the opposite (unshielded) forearm (Aftanas and Zubek, 1964). This effect was quite persistent, as increased sensitivity was still present three days after the cup had been removed.

The sensitizing effect of restricted sensory input also can occur across sensory modalities. The brain needs sensory input to maintain normal reactivity levels. Zubek et al. (1964a) found that a person who is blindfolded or wears translucent goggles for one week has increased tactile, pain, and heat sensitivities, respectively. Even partial deprivation of visual input will sensitize the skin (Zubek et al., 1964b). Trimming the whiskers of baby rats causes the areas of the brain that receive sensory input from the whiskers to become more excitable (Simons and Land, 1987), and this effect persisted. Receptive fields were still enlarged three months after the whiskers had regrown.

Other indicators of increased central nervous system arousal are the effects of depressant and convulsive drugs, respectively, on animals residing in different environments. Rats living singly in small cages were compared to those in groups, and the isolated rats had higher thresholds for anesthetics. Juraska et al. (1983) administered both depressant and convulsive drugs to rats isolated in small laboratory cages (isolated condition, IC) or living in a group of 12 in an enriched environment (enriched condition, EC) which consisted of a large enclosure with many different toys. The IC rats injected with sodium pentobarbital took longer to lose the righting reflex. In a second experiment, when rats reared in IC and EC, respectively, were given the convulsant drug, pentylenetetrazol, the IC rats went into light flash-induced convulsions at lower doses.

Bombarding an animal with excessive stimulation can cause detrimental signs similar to those caused by restricted stimulation. In the IC/overstimulated condition, mice were subjected involuntarily to intense sound, light, and vibration, whereas those in the EC were allowed to initiate and control their interaction with toys. Both IC and IC/overstimulated mice were more irritable than were EC mice, and both forced under stimulation and forced overstimulation increased irritability.

Concept of optimal stimulation

Zentall and Zentall (1983) believe that organisms modulate incoming sensory stimulation to maintain the nervous system at an optimal level of arousal. In some cases, for example, stereotyped behavior may be an attempt by a disturbed biological system to restore homeostasis (Damasio and Maurer, 1978). Environments offering low levels of stimulation tend to cause behavior in animals which is stimulus-seeking. Conversely, animals living in an overstimulating environment sometimes attempt to reduce their central nervous system arousal by engaging in repetitive activity (Zentall and Zentall, 1983).

Dantzer and Mormede (1983) and Dantzer (1986) suggested that repetitive stereotypic behavior can serve a de-arousal function. For example, food-deprived pigs will engage in repeated chain-pulling in between food deliveries which occurred every four minutes, and pigs which had access to the chain had lower plasma corticosteroid levels. Stereotypes also occur in pigs living in barren environments which provide low levels of sensory stimulation (Ewbank, 1978; Markowitz, 1982). Therefore, stereotypes may occur in both under stimulating and overstimulating environments. In under stimulating environments, of course, they probably serve to increase sensory input (Ewbank, 1978; Harkowitz, 1982). Young children deprived of normal hugging will engage in excessive masturbation, which stopped when nonreproductive tactile contact with parents was increased (McGray, 1978).

Even though animals living in a barren environment may attempt to reduce central nervous system arousal level, the central nervous system nevertheless may remain in an abnormally aroused state. Perhaps some of the environments that have been imposed experimentally deprived the animals beyond their physiological ability to cope. For example, extremely barren environments would never be encountered in nature.

Nervous systems are endowed with a certain amount of plasticity so the animals can deal with changing environmental demands. The ability to adjust the relative sensitivity of sensory systems to different environments would be useful to an animal for survival in the wild. Simons and Land (1987) concluded that sensory input affects the development of the brain's somatosensory cortex.

Structural changes in the brain

Stimulation and opportunities for activity provided by an enriched environment cause changes in dendritic branching in the brain. Groups of weanling rats residing for four weeks in a large enclosure with toys and objects to climb (enriched condition, EC) had greater dendritic branching in the visual cortex than did those living singly In standard laboratory cages (isolated condition, IC) (Greenough and Juraska, 1979; Volkmar and Greenough 1972).

More recent research results indicate that new synapses may be formed by neural activity induced by the enriched environment (Greenough et al., 1985). Researchers also have compared IC and EC with (social condition, SC), the latter consisting of two animals living together in a 22 x 25 x 30-cm laboratory cage. Floeter and Greenough (1979) found no differences in dendritic branching in the cerebellums of SC and IC monkeys (Macaca fascicularis). The EC monkeys had the most dendritic branching.

In rats, SC animals had intermediate levels of dendritic branching in the visual cortex (Volkmar and Greenough, 1972). The IC rats had the least branching, the EC rats the most. Weanling rats in EC also had heavier brains than did those in IC (Bennett et al., 1964; Diamond et al., 1964). Rats in EC also had a thicker cortex and additional glial cells (Bennett et al., 1964; Diamond et al., 1964; Diamond, et al., 1966). In these experiments, the control rats were housed in trios in 32 x 32 x 20-cm laboratory cages, and all rats were in their respective environments for at least 29 days.

Very short (four-day) periods of differential housing affected cortical depth in the dorsal-medial part of the brain's occipital cortex (Diamond et al., 1976). Cortical depth differences in weanling rats were induced mainly by environmental impoverishment, whereas in adults they were induced mainly by enrichment.

Neural hypertrophy does not necessarily mean that an animal is in an environment that is higher quality overall. Research indicates that neural hyptertrophy can sometimes be detrimental. Rats exposed to continuous lighting had greater spine density in the visual cortex (Parnavelas et al., 1973), but their retinas were damaged (Bennett et al., 1972, 0'Steen, 1970). Stimulation of the hippocampus with an implanted electrode induced axonal growth and reorganization of synapses, but these new connections increased excitability and seizures developed (Sutala et al., 1988)

Farm animals

Enriching pigs' environments may help prevent changes in the central nervous system which lead to hyperexcitability and stereotyped behavior. Casual observations of pigs residing in indoor pens indicates that they often exhibit an excessive startle reaction to door slamming or other disturbances. Farmers have learned that playing a radio with a variety of music and talk reduces pigs' reactivity to extraneous sounds. Observations at slaughter plants indicate that some pigs are more excitable and difficult to handle than others (Grandin, 1986).

Pigs living in indoor pens with minimal contact with people were more excitable and difficult to load than those residing outside with frequent contact with people (Warris et al., 1983). Pigs from 1.2 x 1.2-m relatively barren pens also were slower to approach a novel object or human strangers compared to pigs that had had access to toys and frequent contact with people (Grandin et al., 1983).

Pigs which are either balky or excitable are more difficult to transport and handle at the slaughter plant. Those that at reluctant or refuse to move are more likely to be subjected to excessive electric-prodding. Electric prod-induced excitement is detrimental to pork quality (Barton-Gade, 1985; Grandin 1986). Repeated electric-prodding also will increase bloodsplashing (hemorrhage) in the pork carcass (Calkins et al., 1980). Further, it is detrimental to the pig's welfare; heart rate increases progressively with successive prods, and if it is continued, the pig's heart rate will reach dangerously high levels and death can result (van Putten and Elshof, 1978; Mayes and Jesse, 1980). A pig will stop and lie down when its heart rate is near the lethal point (Hayes and Jesse, 1980).

B. Environmental Enrichment Methods

Choice of environmental enrichment

Stolba (1981) observed pigs in a semi-natural environment help determine suitable environmental enrichment devices. The studies were an important first step in determining choices pigs make from among a variety of natural objects. It is important that the play objects provided pigs be things that they appreciate, and the objects must support sustained interest. Research can be used to determine the type of objects pigs prefer.

Choice tests have been used to determine animals' preferences for type of flooring, social groupmates, and mate (Hughes and Black, 1973; Hughes, 1976; Dawkins; 1982; Farmer and Christison, 1982; McGlone and Morrow, 1987); to test sheep's preferences for type of handling facilities (Hitchcock and Hutson, 1979; Hutson, 1981) and restraint methods (Grandin et al., 1986; Rushen, 1986); and to determine pigs' preferred angle and flooring surface for ramps (Phillips et al., 1988).

When choice tests are used, it is essential that they be controlled adequately to prevent previous experiences from influencing the choices. For example, previous experience with different pastures can alter pasture preference in sheep (Arnold and Maller, 1917), and the environment in which they were reared can affect caged hens' subsequent flooring and social preferences (Hughes, 1976).

Another potential problem with preference tests is that something that is preferred on a short-term basis may have detrimental long-term effects on the animal's well-being (Hughes and Black, 1973; Duncan, 1978; van Rooijen, 1982) For example, animals may prefer one type of flooring during a two-hour preference test, but the preferred flooring may injure the animals' feet after several months.

Piglets usually prefer plastic-coated expanded-metal floor over concrete (Farmer and Christison, 1982). In practice, plastic-coated expanded-metal flooring is excellent for farrowing crates and nursery pens but causes problems when used for a finishing floor. Casual observations indicated that pigs finished on either flattened or plastic-coated expanded metal had excessive hoof growth, and they balked and were difficult to drive into a high-speed slaughter line (Grandin, 1988).

Preference tests are one useful method for determining practical objects that producers could use to enrich a pig's environment. Unlike flooring, feed, or housing, object choices are unlikely to have adverse long-term effects on the pigs' health or performance. There is a need for information on the pig's short- and long-term preferences for means of environmental enrichment so that recommendations can be made to producers.

Play in Farm Animals

Farmers have offered pigs various objects in attempts to enrich their environment and reduce vices. van Putten (1969) recommended placing chains or rubber hoses in pens to occupy the pigs' attention and reduce tail-biting. Weanling pigs will play with many kinds of objects, and they vigorously chewed, tugged, and shook suspended strips of cotton cloth (Grandin et al., 1983). They also rooted and rolled balls, wooden boards, plastic boxes and other objects when these items were first placed in their pen. When these objects became soiled with excreta, however, the pigs lost interest in them. Suspended strips of cloth seemed to hold the pigs' interest longer than did suspended chains, clean objects more than did soiled.

Fagen (1984) described play as follows: "Play means behavioral performance that emphasizes skills for interacting with the physical and social environments and that occur under circumstances under which the function of the exercised skills can not possibly be achieved." Play occurs in many farm animals, including cattle, sheep, pigs and horses (Brownlee, 1954, 1984; Tyler, 1972; Schoen et al., 1978; Sachs and Harris, 1978; van Putten, 1978; Dobao et al., 1984-85; Crowell-Davis et al., 1987), as well as a relative of the domestic pig, the collared peccary (Byers and Beckoff, 1981; Byers, 1984). It is interesting that in the collared peccary both juveniles and adults play, because ordinarily in ungulates only juveniles and subadult males play (Byers, 1984).

Object play, including "tug-of-war", has been observed in dogs, cats, horses, and jackals (van Lawick and Goodall, 1971; West, 1977; Fagen, 1981; Martin, 1984). Captive bushdogs and foxes play with sticks (Biben, 1982). A captive rhinoceros will root a ball and other objects (Inhelder, 1978; Hediger, 1968). Piglets also engage in object play (Gundlach, 1988; Fraedrich, 1974). Weanling pigs tugged on cloth strips in a manner similar to that of dogs playing "tug-of-war" (Grandin et al., 1983). Foals will pick up sticks and carry them around and toss them in the air (Crowell-Davis et al., 1987).

Activity patterns in livestock

There are few data available on the daily activity patterns of play in pigs. Domestic livestock do have daily patterns of activity for grazing and other behavior (Hughes and Reid, 1951; Squires, 1974; Arnold and Dudzindki, 1978). Pigs residing indoors are more active during the day (Morrison et al., 1968). In rich environments there are two peaks of activity -- around 0900 and 1700 hrs in pigs (Dantzer and Mailha, 1972; Dantzer, 1973; Bure, 1981). When pigs had an opportunity to control the temperature in their pen, a cooler environment was preferred at night (Curtis and Morris, 1982).

Aggression and environmental enrichment

Pigs are a relatively feisty species. When strange pigs are mixed they will fight one another vigorously, at least in part to establish a new social order (McBride et al. , 1964). Fighting among pigs causes injuries (Symoens and van der Brand, 1969; Jones, 1969) and will reduce weight gains if the pigs are overcrowded or have limited access to food (Graves et al., 1978; Sherritt at al., 1974).

Fighting among newly weaned piglets generally has little adverse effect on the pigs' long-term performance, but it can be detrimental to welfare. McGlone and Curtis (1985) found that fighting and injuries could be reduced by providing newly weaned pigs small hides where they could place their head and shoulders. Anecdotal reports suggest that providing pigs toys during times of social mixing also will reduce fighting.

Straw bedding did not reduce fighting in growing pigs fed ad libitum, but it had a tendency to reduce fighting in fasted pigs (Kelley et al., 1980) Another factor which will influence aggression is type of housing. Pigs in indoor pens were more aggressive than those residing outdoors (Meese and Ewbank, 1973). Crowding tends to increase pig aggression (Bryant and Ewbank, 1972; Kelley et al., 1980; Randolph et al., 1981), but it does not increase all kinds of aggression in a uniform manner. Reducing floor space reduces aggression which occurs away from the feeder, but it has no clear effect on aggression at the feeder (Ewbank and Bryant, 1972). Restricting lying space increased aggressive encounters when animals were standing but had little effect on aggression in other areas (Ewbank and Bryant, 1972). More information is needed about the effects of environmental richness on aggression in pigs.

C. Thesis Research Outline

Dendritic growth in the pig's cerebral cortex

In the first experiment to be reported in this thesis, the effect of environmental enrichment on dendritic growth in the pig's brain was studied. Heretofore, many such studies have been conducted with rodents (see review by Greenough and Chang, 1985), and three with primates (Struble and Riesen, 1978; Floeter and Greenough, 1979; Stell and Riesen, 1987). The study to be reported here was the first conducted with a domestic farm animal. Valuable knowledge about environmental effects on brain development may be able to be gained by studying animals that have a larger, more complex brain than does the rat.

Excitability and handling of the pig

The second series of experiments were designed to determine effects of environmental enrichment on the excitability and handling of pigs living in intensive systems. The aim was to determine effects of various kinds and extents of environmental enrichment on the excitability of pigs in space-restrictive, relatively barren pens.

0bject play by the pig

In the third series of experiments, choice tests were conducted to determine the types of play objects that are preferred by pigs, both short- and long-term. Daily activity patterns of toy play also were determined. In the last experiment, effects of access to play objects prior to or during social mixing of newly weaned piglets were determined to learn whether toys would reduce agonistic behavior.

The environmental enrichment methods used in all of these experiments were simple, practical procedures that swine producers could use. Results of these experiments may help answer questions as to whether relatively simple environmental enrichment procedures will improve the productivity and welfare of pigs residing in intensive production systems.

Dendritic Growth in Somatosensory Region of Brain Cortex in Pigs Residing in a Simple or a Complex Environment

A. Introduction

An animal's experiences affect the anatomical development of its brain. Volkmar and Greenough (1972) studied weanling rats that had resided for 29 or 30 days in three different environments: enriched condition (EC), social condition (SC), and isolated condition (IC). In the EC, 12 animals resided most of the time in a 45 x 60 x 70-cm cage furnished with many different objects that were changed daily, and they also were placed in a large object-filled box for 30 minutes of activity every day. The objects were pieces of wood, children's toys, ladders and laboratory utensils. In the IC, single rats resided in 22 x 25 x 30-cm cages with solid metal sides and a wire mesh top and front. In the SC, the rats resided in pairs in the same type of cage as in the IC. Rats in the EC group had the most dendritic branching, those in the IC the least. Differential rearing environment had the greatest effect on the higher-order dendrites (i.e., those located farther from the cell body).

Similar but smaller and more localized increases in dendritic branching have been found to occur following training in mazes and motor tasks (Black et al., 1987; Chang and Greenough, 1982; Greenough at al., 1985).

Most studies on the effects of environmental richness on dendritic branching and synapse growth have been conducted on rodents (Greenough and Chang, 1985). The EC/SC/IC paradigm described above was used in a monkey study, too (Floeter and Greenough, 1979). Macaca fascicularis raised in the EC (with toys and climbing structures) had more dendritic branching in cerebellar Purkinje cells than did paired or isolated monkeys. The EC monkeys also had larger Purkinje somas.

In another experiment, old World monkeys (Macaca arctoides) placed in isolation had significantly less dendritic branching than colony-reared monkeys (Struble and Riesen, 1978). Further studies by Stall and Riesen (1987) indicated that monkeys reared in isolation with objects, ladders and swings had greater dendritic branching in the motor 1 cortex compared to monkeys reared by their mothers in the colony or reared in isolation without gymnastic equipment.

In cats, Spinelli at al. (1980) found that training a kitten to avoid a shock by lifting its foreleg resulted in greater dendritic density in the cortical area which receives sensory input from the forearm. Beaulier and Colonnier (1987) also found that IC cats had more FS synapses and fewer RA synapses per neuron compared to EC cats. FS and RA synapses are the two main morphological types of synapses in the cerebral cortex. FS synapses have flat vesicles and RA synapses have round vesicles.

The preceding experiments have all involved conditions specifically designed for comparison of environmental enrichment or training with its absence. The purpose of the present experiment was to determine whether the quality of different rearing environments which might be used in production agriculture can affect the morphology of cerebral cortical neurons in pigs. To assess this, pigs reared in a simple, production-like condition were compared with pigs reared in a large group with straw, a variety of different objects, and additional contact with people.

B. Experimental Procedure

Animals and treatments

Twenty-four littermate pairs of 18- to 25-day-old Hampshire-sired crossbred pigs were studied in two trials. Mean weight of trial 1 pigs was 7.97 kg (SD=0.87) and trial 2 pigs was 10.78 kg (SD=1.60). In each trial, 12 pigs resided in a complex environment (CE) (similar to the EC in the experiments described earlier), and 12 in a simple environment (SE) (similar to the SC described earlier). Trial 1 lasted 68 days, and Trial 2, 65 days. Half of the animals in each trial ware used for anatomical study.

The SE consisted of rearing two pigs in each of six 1.22 x 1.22-m pens with plastic-coated expanded-metal floors in a windowless, environmentally controlled house where air temperature was 22 to 28 C. Pen partitions were constructed of vertical glass fiber-reinforced plastic rods. Pigs in different pens could see each other, but could have no physical contact, because there was an empty pen between every two that were occupied. The room was illuminated continuously by fluorescent tubes (200 lux) in Trial 1. In Trial 2, the luminairas were timer-controlled so illumination started at the approximate time of sunrise (0600) and stopped at the approximate time of sunset (2030) each day; this provided the SE pigs with approximately the same light/dark cycle as the CE pigs. The SE pigs ate from a self-feeder and drank from a nipple waterer. The room was entered only for feeder servicing for 10 min every day or pen washing for 60 to 90 min every third day.

The 12 CE pigs resided together in a house with a concrete slab floor bedded with straw (new straw added daily) with an adjoining outdoor pen with a concrete slab floor. In both trials, the CE pigs ware handled by the experimenter for 15 to 30 min every day. The experimenter petted the animals, scratched their abdomens, and allowed them to chew on boots and coveralls.

In Trial 1 the CE pigs were provided a variety of objects to manipulate. These objects were changed daily and included a plastic milk crate, various cloth strips tied to the fence, ropes, chains, plastic ball, dirt, corrugated cardboard, newspapers, telephone directories, soda cans, stones, garbage can, and pieces of wood. The CE pigs in Trial 2 were provided only three 7.5 x 50-cm white cotton cloth strips suspended from a rope across the pen; the strips were changed weekly. Feed was provided in a self-feeder with lids, and water was provided in a float-controlled automatic waterer.

Brain preparation

At the end of each trial, six pigs from each treatment group were sacrificed and their brains were perfused, fixed, Golgi-Cox impregnated, sectioned, and mounted by procedures described in Chapter III (Grandin at al., 1988), a modification of the methods of Olasar and Van Der Loos (1981) and Greenough (1984). Figure 4 shows the locations of the tissue blocks that were removed from the visual and somatosensory regions of the cerebral cortex. Somatosensory cortical tissue blocks were from the area determined by Adrian (1943), who used evoked responses to tactile stimuli from the brain of anesthetized pigs. Adrian (1943) and Woolsey and Fairman (1946) are in excellent agreement in this regard. The work of Kruska (1971, 1972) was used to determine the location of the visual cortex in the pig brain. Results of Campbell (1905) are in accord with Kruska's findings.

Dendritic growth determination

An Olympus BH-2 binocular microscope (Tokyo, Japan) with an Olympus BH2-DA camera lucida attachment was used to make pencil tracings of layer II pyramidal cells in both the somatosensory and visual regions of the cerebral cortex. All slides were coded so the drawings could be made with the drawer blind to treatment. Microscope magnification was 450X.

To determine the level of cortical lamination, 12 visual cortex sections of each brain were counterstained with methylene blue following the Glaser and Van Der Loos (1981) protocol (counterstained sections were not used for data collection). The processing procedure was the same as described in Chapter III, but additional steps were added after sectioning:

  1. 70% ethanol for 10 sec
  2. 50% ethanol for 10 sec
  3. Two immersions in deionized water in separate pans for 30 sec each
  4. Ammonia water (19% NH4OH) for 20 min
  5. p-Phenylene di-amine (.5 g in 1000 ml water) for 5 min
  6. Two immersions in deionized water in separate pans for 2 min each
  7. 1% Kodak Dektol Fixer for 2 min
  8. Kodak Rapid Fixer for 7 min
  9. Three immersions in deionized water in separate pans for 5 min each
  10. 1:1 tamponee:water for 5 min (formula for tamponee: sodium acetate 13.6 g, glacial acetic acid 23.45 ml, water to make 1 L)
  11. 1:1 and 2% methylene blue in deionized water for 8.5 min.
  12. Tamponee for 30 sec
  13. 1:1 tamponee and deionized water for 20 min.
  14. 50% ethanol in deionized water for 15 sec
  15. 70% ethanol in deionized water for 15 sec
  16. 95% ethanol in deionized water for 60 sec
  17. Two immersions in 100% ethanol in separate pans for 20 sec each.

For each pig, a minimum of 14 drawings of basilar dendrites of layer II pyramidal neurons in the visual and somatosensory regions of the cerebral cortez, respectively, were made at 450X magnification. Apical dendrites were not evaluated because many of them had been transected by the microtome. Pig cortical neurons are extremely large relative to those of rodents, and therefore more difficult to align.

A stratified sampling method was developed to specify the location of the pyramidal cells to be drawn. The outline of each section was traced with a projection microscope (Bausch and Lomb 42-63-59, Rochester, New vork) at low power (22X). Lines were drawn connecting landmarks on the projected drawing (as shown in Figures 5 and 6) to determine three locations in the somatosensory cortex and four in the visual cortex. More than one location was used because usually there were an insufficient number of well-impregnated or untransected cells in any one location. In the somatosensory cortex, four drawings were made from each location, and in the visual cortex, three. Four sections per animal were used, The remaining two drawings of the 14 were made from two locations picked at random (if remaining undrawn neurons in the respective areas were well-impregnated) or from the undrawn well-impregnated neurons which remained in the locations.

Dendritic complexity was quantified by concentric ring analysis (Sholl, 1956; Greenough, 1975). A clear plastic overlay with concentric circles at 20 m equivalent intervals was centered visually over the neuron's soma, and the basilar dendritic branches that crossed each ring were counted. Total ring intersections (TRI) were then determined by summing the counts for all rings.

Soma width was determined by measuring the width of the cell body at its widest point, 90 degrees perpendicular to the main apical process. Measurements were made on the camera lucida drawings with a ruler marked at millimeter intervals.

Pig behavior

At the end of Trial 1, behavior of pigs from both environments was tested to determine the pig's time to approach a strange man and a novel object, respectively. Each animal was tested individually in an octagonal arena with 1.22-m high white-painted plywood walls (Figure 7). The arena floor was covered with brown plastic carpet. The vestibule floor was broom finish concrete. The room was illuminated at 200 lux. Tests of time to approach the strange man and time to approach the novel object were conducted separately. The strange man was a person unknown to the pigs. He stood still during the test The novel object was a new red metal feeder, standing on its end.

Testing was alternated between CE and SE pigs. Strange man approach tests and strange object approach tests were conducted successively, in random order. During testing, each pig was placed in the vestibule for a 3 min adjustment period. After this, the entrance gate to the arena was opened, The timer was started when the pig's nose passed the entrance gate and stopped when the pig walked up and touched the man or the object. The test was terminated if the pig failed to touch the man or the object within 3 min.

At the end of Trial 2, behavior of pigs from both environments was tested in a narrow chute. The layout of the apparatus is shown in Figure 8. The narrow chute was constructed from plywood painted white. It was 1.22-m high, 27-cm wide at the bottom and 38-cm wide at the top. The wooden chute floor was painted gray and the vestibule floor was covered with brown plastic carpet.

To tend to discourage the pig's movement through the chute, the floor contained three obstacles perpendicular across the path: a 5-cm-wide light beam, a 7.5-cm-wide perforated metal strip, and a 2 x 3.7-cm-wide wood board. To encourage movement through the chute, a decoy pig (not from the experiment) was placed in a welded-wire mesh pen at the end of the chute.

The testing procedure was similar to that in Trial 1 except there was no adjustment period in the vestibule. The timer was started when the pig was placed in the vestibule. The test was terminated if the pig failed to walk all the way through the chute to the decoy pig within 5 min. Each pig was tested twice.

In Trial 2, behavior of pigs in both environments was observed for 24 h during week 7 of the trial. It was videorecorded (NV8030 time-lapse recorder, Panasonic Co., Secaucus, NJ) The videorecording system was operated at 0.9 frames/s. In the SE, one camera viewed three of the six pens. In the CE, one camera viewed the inside of the straw-bedded shed and a second the concrete slab. Data were registered while records were reviewed at a speed 18 times faster than the recording speed. High speed reviewing made subtle nosing and rooting movements appear as readily discernible vibrations of the snout. Nosing of other pigs and rooting or chewing objects was quantified by one-zero sampling (Lehner, 1979) every 5 min. The entire videorecord was viewed. A five-min interval, in which one pig was active in the way of interest, was given a score of 1; if two different animals were observed to be active within the same interval, a score of 2 was given, and so on.

Statistical analysis

The individual pig was the experimental unit. The dependent variables were total ring intersections (TRI), soma width, and the product index, (TRI x soma width). The latter variable was calculated to serve as an index of neuron development.

Data were analyzed by the SAS General Linear Model (analysis of variance) procedure (SAS, 1982) In an attempt to enhance the power of the statistical tests, individual data (x) were transformed as follows: x2, log x, arcsine(x1/2), (x1/2), and (x -1). The (x1/2)-transformed data improved the significance level, and data resulting from this transformation will be presented and interpreted together with the raw data.

While camera lucida drawings were being made, it became apparent that many pyramidal cells had a distorted shape. Apical dendrites were twisted, and some basilar trees were grossly asymmetrical. In some cases, the asymmetry was not due to transection by the section plane. Instead, it was the natural shape of the cell. To determine if distortion of the cells was affecting our ability to detect differences in dendritic growth due to environment, a sorting procedure suggested by Janice M. Juraska (personal communication, 1987) was developed to arbitrarily eliminate distorted cells. In the end, pyramidal cells had to comply with the following criteria to be retained in the sorted category:

  1. Basilar tree more than 170 m in diameter measured perpendicularly relative to the apical process (9 mm measured on the camera lucida drawing was equal to 20 m on the cell).
  2. Soma more than 18 m wide at the widest part perpendicular to the apical process.
  3. Symmetrical basilar tree. (If more than 75% of the basilar dendrites were on one side of a line extending 180 degrees from the apical process, the cell was rejected.)
  4. Main apical branch more than 140 m long. (If the main apical process was transected, but more than 4 m wide at the point of transection, the cell was retained. This criterion was based on experience studying pyramidal cells, Cells with apical processes 4.5 m or thicker near the soma had apical processes and dendrites longer than 140 m.)

These criteria were arbitrary, but they were based on experience and intended to remove the misshapen cells and cells that did not conform to the symmetrical pyramidal cells with long apical processes described in several reports (Sholl, 1956; Greenough, 1975; Greenough and Juraska, 1979). Figures 9 and 10 illustrate somatosensory layer II pyramidal neurons which satisfy the above criteria, whereas Figures 11 and 12 illustrate neurons that do not satisfy these criteria. The basilar tree is less than 170 m wide in Figure 11, and in Figure 12 the basilar tree is asymmetrical. Basilar trees with a major branch transection near the cell body were also rejected. In Trial 1, 9.91 (SD=4.50) somatosensory cortical drawings per pig were retained in the sorted data set; In Trial 2, 7.50 (SD=1:45). In Trial 1, 5.27 (SD=1.11) visual cortical drawings per pig were retained; In Trial 2 6.66 (SD=2.39). Data for both sorted and unsorted cell sets were analyzed.

Visual cortical data for one CE barrow in Trial 1 was, unavailable for analysis due to incomplete Golgi-Cox impregnation.

C. Results

Pigs reared in the SE had more extensive basilar dendrites in the somatosensory cortex than did those in the CE. Total ring intersections for both trials combined (unsorted) were 55.70 ± 2.38 (mean ± SE) in SE pigs and 48.62 ± 2.38 in CE pigs (P<.06; Table 1). After sorting, the significance level changed to P<.03 (Table 1). For the raw data, the significance level was P<.06, and on the square root-transformed data, P<.05.

Graphing the raw data revealed that the greatest differences between the SE and CE pigs were in rings 3 and 4 (Figures 13 and 14). Rings 1 and 2 (closer to the soma) showed less difference.

Pigs from the SE also had larger somas in the somatosensory cortex than did those from the CE: 7.72 ± 0.17 versus 7.27 ± 0.17 (Table 1) (P<.08, raw data; P<.08 square root-transformed data). Sorted soma widths did not differ significantly. Both sorted and unsorted somatosensory cortex index scores differed significantly between environments (Table 1) (P<.05 and P<.04, respectively); the SE pigs had higher scores.

When the data were categorized according to trial, there were no effects of rearing environment in Trial 1. Environmental effects on TRI and index scores approached significance in Trial 2 (Table 2) (P<.08 and P<.09); there was a tendency for the SE pigs to have more dendritic branching.

When data from both trials for the visual cortex were pooled, environment had no effect on TRI, soma size, or the product Index, (TRI x soma size) (Tables 3 and 4). Graphs of the raw data for visual cortex in Trials 1 and 2 pooled illustrate the lack of difference between treatments (Figures 15 and 16). When Trials 1 and 2 were analyzed separately there were no treatment differences (Table 4).

There was a strong effect of gender on somatosensory cortical traits when data from both trials were pooled. Gilts had larger somas (7.78 ± 0.17 versus 7.22 ± 0.17, P<.03) (Table 5). However, there was no gender effect for visual cortex where data from both trials were pooled (Table 6). Analysis employing a gender X trial interaction model revealed an effect of trial on TRI in both the somatosensory and visual regions of the cerebral cortex (P<.03 for somatosensory unsorted; P<.006 for visual sorted) (Tables 7 and 8); barrows had higher TRI in Trial 1, gilts in Trial 2. Sorting changed significance levels of the somatosensory TRI and soma size, but had little effect on those for the visual cortex.

In Trial 1 there was a tendency for the CE pigs to touch both the strange man and the novel object sooner. Mean times to approach the strange man were: CE--59.5 ± 13 sec (mean SE), SE--100.3 ± 18 sec (NS). Approach times toward the strange object were CE--49.8 ± 13 sec and SE--83.5 ± 18 sec (NS). Even though the mean times were not significantly different, there was a significant difference between rearing environments for the number of pigs which touched the man in less than 60 sec. Nine out of 12 CE pigs touched the man in less than 60 sec, whereas only 4 out of 12 SE pigs did go (X2, 4.19, P<.05), In the approach on object test, 9 out of 12 CE pigs touched within 60 sec, whereas only 5 out of 12 SE pigs did go (X22.74, P<.10). When data for both the man and object approach tests were combined, 18 out of 24 CE pigs touched within 60 sec, whereas only 9 out of 24 SE pigs did go (X2, 6.85, P<.01).

In Trial 2, CE pigs were more willing to walk through the chute. Mean times to walk through in the first test were: CE--2.27 ± .53 min and SE--4.54 ± .37 min (P<.001). Mean times for the second test were: CE--1.47 ± .53 mm and SE--4.13 ± .48 min (P<.001). Times were shorter for the second trial compared to the first.

On the first chute test, 10 of 12 CE pigs walked through within 5 min, whereas only 2 of 12 SE pigs did (X2=10.66, P<.01). In the second test, 10 of 12 CE pigs walked through, but only 4 of 12 SE pigs (X26.18, P<.02). When both tests were combined, the results were: 20 of 24 CE pigs walked through within 5 min, but only 6 of 24 SE pigs did go (X2=16.540, P<.001).

Pigs in the SE engaged in significantly more nosing of each other than pigs in the CE. The CE pigs had only 14 5-in periods where nosing each other was observed whereas the SE pigs had 119 5-min intervals nosing each other (X2=194, P<.001). The CE pigs also had greater overall rooting activity directed toward a variety of objects (295 versus 215 5-min intervals, (X2=9,54, P<.001).

The CE pigs directed over 90% of their rooting activity toward objects, whereas the SE pigs spent up to 60% of their rooting time, rooting each other.

Casual observations of the pigs during pen cleaning (SE pigs) and petting (CE pigs) indicated that there may have been a difference in the intensity of rooting and nosing. The CE pigs nibbled gently on the straw, whereas the SE pigs rubbed their noses intensely against the floor. Rubbing and massaging another pig may be more stimulating to the somatosensory cortex than rooting straw. The recipient of the massaging appeared to react positively, often rolling over and presenting its belly to the instigating pig. There also was a tendency for the SE pigs that engaged in higher levels of nosing to have greater dendritic growth.

The TRI scores for the three videotaped SE pigs were, 56.63, 45.05 and 50.90. The animal with the highest TRI score also had the highest number of 5-min intervals which contained rooting of the other pig. The number of 5-min intervals which contained rooting were, 41, 37 and 38, respectively. The animal that had the lowest TRI score had the highest number of 5-min intervals which contained rooting of objects in the pen. Number of 5-min intervals which contained rooting of objects was 15, 20, and 16, respectively,

The SE pigs were more excitable than CE pigs, They also appeared to be actively seeking additional stimulation. During pen washing, these pigs became highly excited and tried to bite the hose and play in the water stream. Every time the experimenter moved the water stream away from the pigs, they jumped so as to be in it again. When the SE pigs were in an excited state during pen cleaning, they often rubbed their noses against the floor, perhaps in redirected behavior.

Furthermore, during feeder cleaning, the SE pigs would rush forward and bite the experimenter's hand, and when they were pushed away they returned instantly and bit the hand again. In the CE, the pigs were calmer and the experimenter could easily push the pigs aside (and they stayed away for a while) while cleaning the feeder.

Moreover, in the SE pigs, there were signs the animals were active while people were absent. For example, unscrewed bolts frequently were found on the floor.

D. Discussion

The experimental environments employed -- simple (SE) and complex (CE) --corresponded approximately to the SC and EC, respectively, used in earlier rat and monkey experiments. Pigs were not placed in an IC, for two reasons. First, Floeter and Greenough (1979) found no differences in cerebellar dendritic branching between IC and SC monkeys. Second, isolation of highly social animals such as monkeys and pigs may create stress and abnormal behavior (Harlow and Zimmerman, 1959; Melzack, 1954, 1969). In the interest of the pigs' welfare, we felt we did not have sufficient justification to subject the animals to the stress of long-term isolation (IC).

Rats residing in the EC had greater dendritic branching in the visual and temporal, but not the frontal, lateral cortex (Greenough, 1984). Similar findings also have been found in the neocortex of adult and middle-aged rats (Uylings et al., 1978; Green et al., 1983; Volkmar and Greenough, 1972). Rats residing in an enriched environment had a neocortex that was heavier in several regions compared to those in standard 32 x 20 x 20-cm cages (Bennett et al., 1964; Diamond et al., 1964; Katz and Davis, 1984). The enriched environment consisted of groups of 10 to 12 rats residing in a large cage equipped with ladders, platforms, exercise wheel, and other objects. For 30 min each day, the rats living in the EC also were placed in a maze in which positions of barriers were changed daily (Bennett et al., 1964). The control rats were housed in trios in small (32 x 32 x 20-cm) cages.

Other brain studies revealed that rats from the EC also had a thicker cortex (Bennett et al., 1964; Diamond et al., 1964). Moreover, rats which had a thickened cortex also had additional gia cells in the cortex (Diamond et al., 1966). The EC also caused increases in a wide variety of interrelated brain measures such as synaptic density (Turner and Greenough, 1985; Bhide and Bedi1 1984) and ratio of oligodendrocytes to neurons in the occipital cortex (Katz and Davis, 1984).

In the present experiment, the SE pigs had greater dendritic branching in the somatosensory cortex than did the CE pigs. The SE pigs also had pyramidal cells with larger somas. There was no significant effect of environment on dendritic branching or soma size in the visual cortex. These results are contrary to our hypothesis that the CE pigs (corresponding approximately to EC rats) would have increased dendritic growth Results of previous research on rats indicated that the EC enhanced dendritic development in both neocortical and noncortical areas of the brain (Floeter and Greenough, 1979; Volkmar and Greenough, 1972; Juraska et al., 1985).

The most likely explanation for the apparent anomalous results in this experiment is direct stimulation of the somatosensory cortex. Previous investigators have found that exercise or sensory stimulation will augment neuroanatomy. Exercise will increase dendritic branching in rat cerebellum (Pysh and Weiss, 1979). Training a kitten to avoid a shock by lifting its foreleg resulted in greater dendritic density in the cortical area which receives sensory input from the forearm (Spinelli et al., 1980). Tactile, vestibular, and other sensory stimulation applied to young dogs increased the size of vestibular neurons, while there were inconsistent differences in frontal and auditory regions of the cerebral cortex (e.g. three of eight stimulated puppies had larger pyramidal cells) (Fox, 1971). Shapiro and Vukovich (1970) also found that the application of visual, auditory, and vestibular stimulation and mild electric shocks to infant Sprague-Dawley rats increased spine density in the visual and auditory regions of the cerebral cortex.

Rubbing and massaging another pig may be more stimulating the somatosensory cortex than is rooting straw. Casual observations indicated that SE pigs may have pressed harder with their snouts than CE pigs. The recipient of the massaging appeared to react positively, often rolling over and presenting its belly to the instigating pig.

Placing an animal in a relatively barren environment will increase excitability, irritability, and self-stimulatory behavior. Pigs residing in a barren environment engage in more activities involving the snout. van Putten (1980) found that pigs housed on partially slatted floors without straw massaged other pigs with their snouts twice as much compared to pigs with access to straw. Stolba (1981) also reported that as the environment was made increasingly barren, behaviors directed toward other pigs increased. Less nibbling and massaging of other pigs occurs in straw-bedded pens. providing enrichment in addition to straw further reduces activities directed toward other pigs (Stolba, 1981).

From a sensory standpoint, the SE pigs may have been more deprived than SC rats. The SE pigs had no bedding to root or nibble. They were fed a diet in the form of a finely ground meal, which required little time to consume. SC rats had bedding material and hard food pellets to chew. In the relatively barren SC condition, the rats still had access to materials which enabled them to perform natural chewing behaviors for long periods. Even though the rats could not burrow in the bedding, they could still manipulate it. The pigs had no substrate to manipulate. Small amounts of straw will reduce stereotypes in tethered sows (Fraser, 1975). Possibly, SE pigs engaged in greater amounts of abnormal behavior than SC rats. This could have resulted in abnormally high amounts of input to the somatosensory cortex.

Animals that engage in stereotypes often seek abnormally intense amounts of stimulation. They even will sometimes injure themselves in an effort to obtain stimulation (Cross and Harlow, 1965). Among other things, stereotyped behavior rewards the animal by releasing brain oploids. Self-destructive behavior in retarded children and crib-biting in horses are both stopped by administration of opioid blocking drugs (e.g., Naloxone, Naltrexone) (Sandman et al., 1983; Dodman et al., 1987).

Adrian (1943) reported that a major portion of the pig's somatosensory cortex receives input from the snout, which is one of the most sensitive parts of the pig's anatomy. Therefore, when the SE pigs pressed their snouts against something, presumably intense input was relayed to the somatosensory cortex.

The greater intensity of activity of the SE pigs at pen washing time and the observed intense activities involving their snouts may explain the increased dendritic branching in their somatosensory cortex. Pigs in barren pens with concrete floors reacted more strongly and played longer with a tire than did pigs reared in straw-bedded pens (Stolba and Wood-Gush, 1980). Pigs reared on concrete floors gazed and rooted with greater intensity compared to pasture-reared pigs (Friend and Taylor, 1986). The animals were observed on a pasture which was novel to all animals.

The behavioral tests conducted at the end of the two trials in the present study indicated that CE pigs behaved differently than SE pigs. The SE pigs exhibited greater avoidance responses when they were isolated in the novel arena or chute apparatus. Ten of 12 SE pigs refused to walk through the chute, whereas only two CE pigs refused. The SE pigs' behavior was similar to that of unhandled rats. Rats that are handled during infancy explore larger areas of an open field (Levine et al. 1967). Helzack and Thompson (1956) found that dogs reared in a restricted environment had greater avoidance responses when a person approached.

The SE pigs sought stimulation, but it was an approach-avoidance situation. The first few times the pens were washed, the SE pigs panicked and fled to the rear of the pen. But when they became habituated to pen washing, they approached and excitedly bit at the water stream and hose. Within a few days pen washing had changed from an activity that triggered a strong avoidance response to one that elicited strong approach response. The SE pigs often defecated in the feeder. After the experimenter cleaned it, they sometimes defecated in the feeder again almost immediately. This suggests that they might have been seeking stimulation from the presence of the experimenter, however short the visit may have been. In a totally novel situation, the SE pigs avoided novel stimulation; but in their familiar pens, they actively sought stimulation by belly nosing, biting the experimenter, and biting the water stream and hose.

The SE pigs were more excitable than the CE pigs. Similar observations have been made by other investigators in other species. Animals in the IC were more excitable than were EC animals (Korn and Moyer, 1968; Walsh and Cummins, 1975). Isolation of mice increased reactivity, muscle tone, and aggressive behavior (Valzelli, 1973). Pairs of puppies confined to a barren cage with no visual contact with other dogs responded to a new environment with increased activity (Melzack, 1965). Puppy pairs became hyperexcitable even though they could smell and hear other dogs. After being returned to a normal environment a year later, the dogs still were more excitable (Melzack, 1954). Walsh and Cummins (1975) found that rats became hyperactive when their toys were changed. Interestingly, the EC in the laboratory probably is relatively simple compared to life outside the laboratory. A garbage dump or a rural environment has greater complexity than a laboratory cage filled with objects and otherwise enriched.

Quality of the environment affects behavior. Riittinen et al. (1986) compared the effects of different environments on behavior. Weanling mice were subjected to three different environmental treatments: standard IC, IC with overstimulation, and EC with objects. In the IC/overstimulated condition, the mice were subjected involuntarily to intense sound, light, and vibration. In the EC condition, they were allowed to initiate and control their interaction with the objects. Both IC and IC/overstimulated mice were more irritable than the EC mice. Thus, both forced understimulation and forced overstimulation increased irritability, as measured while the mouse was being "attacked" by a bottle brush moving toward it. The most frequent response to the bottle brush by EC mice was escape, whereas IC and IC/overstimulated mice had a higher frequency of beating their forepaws against the side of the cage.

Increased dendritic branching or spine density does not necessarily mean that the animal has been in a higher quality environment. In monkeys, colony-reared animals had less dendritic branching in the motor I and frontal regions of the cerebral cortex compared to animals reared in an isolated condition with ladders, objects, and swings.(Stell and Riesen, 1987). Rats exposed to continuous lighting had greater spine density in the visual cortex (Parnavelas et al., 1973), but their retinas were damaged (Bennett et al., 1972; O'Steen, 1970). Stimulation of the hippocampus with an implanted electrode induced axonal growth and reorganization of synapses, but these new connections increased excitability and seizures developed (Sutala et al., 1988).

In a developing nervous system, there is an overproduction of neurons. As the brain matures, excess synapses are eliminated. This seems to be a kind of biological sculpturing process. Fifty to 70 percent of developing neurons are eliminated in some parts of the developing embryonic nervous system (Oppenheim, 1985). In Rhesus monkeys (Macaca mulatto) excess synapses are still being eliminated before full behavioral competence (Rakic et al., 1980). Rakic et al. (1980) suggested that complete maturation may be related to the elimination of synapses.

Maybe increased dendritic branching in the somotosensory cortex of the SE pigs was caused by a decrease in synapse elimination. Intense sensory input from the pig's snout may have provided stimulation which prevented elimination of synapses. During the course of the experiment, the pigs' brains were undergoing rapid development. Brain weight increases rapidly from birth to 20 to 22 weeks of age (Dickerson and Dobbing, 1966). Cholesterol levels also increase greatly during this time (Dickerson and Dobbing, 1966). This is an indicator of myelinization.

Different parts of the brain may respond differentially to increased sensory input. In our experiment with pigs, and in that of Stell and Riesen (1987) with monkeys, rearing environment had no effect on the anatomy of the visual cortex, but it affected other parts of the brain. In rats, EC-induced changes in cortical depth were more variable in the somatosensory cortex than in the visual cortex (Diamond et al. 1964). Motor I cortex was augmented by increased physical activity provided in an isolated EC condition (Stell and Riesen, 1987). In the frontal cortex, there was a tendency for the colony-reared monkeys to have the lowest levels of dendritic branching compared to the IC and isolated EC monkeys. In motor I cortex, monkeys in the two IC and the colony had similar levels of dendritic branching (Stell and Riesen, 1987).

Increased dendritic growth in the somatosensory cortex of SE pigs may have occurred in an abnormal manner due to extreme sensory restriction relative to the snout. There is evidence that direct stimulation from a sense organ is not the primary mechanism of environmental enrichment effects on neural hypertrophy. In cortical weight experiments, the greatest changes occur in rat visual cortex. Cortical weight is greater in EC animals kept in total darkness and in blind EC rats (Krech et al., 1963; Rosenzweig and Bennett, 1969). Diamond et al. (1972) stated that this indicates that vision is not the primary cause of the EC effect in the visual cortex of rodents.

In the visual cortex of the rat, effects of environment and gender interact in complicated ways. Within the visual cortex, different cell populations respond differentially to environmental enrichment in male rats as opposed to females (Juraska, 1984). Apical oblique and basilar branches of layer III pyramidal neurons had a smaller response to the EC in females than in males. Layer V pyramidal neurons in both genders showed equal amounts of dendritic growth.

Even within a single neuron, different types of synapses react in different ways to environmental enrichment. Beaulier and Colonnier (1987) found that an enriched environment caused FS synapses to decrease, and each residual synapse widens. Although RA synapse numbers do not change, the total contact area in this case is 16% greater than in FS synapses. These experiments provide support for the idea that an entire system of the brain may respond differently to environmental enrichment compared to another system.

Recent research by Black et al. (1987) revealed that the paramedian lobule of the cerebellar cortex in rats trained in a constantly changing complex acrobatic task had a thicker molecular layer than rats subjected to large amounts of routine exercise. Exercise on a treadmill or exercise wheel provided far more physical activity than the acrobatic training (Greenough and Bailey, 1988). Maybe some parts of the brain have increased dendritic branching due to quantity of input whereas other areas will respond only to increased quality of information-carrying capacity of the input. Another possibility is that the animals that performed the acrobatic task had to continually maintain their balance while traversing narrow balance beams and teeter-totters. The treadmill and exercise wheel would not force the rats to actively maintain balance. Actively maintaining balance on an unstable apparatus may have provided additional stimulation to the cerebellum. Even though the balance center is located outside the paramedian lobule, balance may affect it. In humans, defects in both midline and lateral cerebellar zones will cause gait difficulties (Gilman et al., 1981)

Depending upon the circumstances, there may be three possible mechanisms which control neural responses to environment: 1) neural hypertrophy increases in the EC due to increased sensory input, 2) increased sensory input prevents normal synapse elimination, or 3) more complex sensory input due to active exploration and learning causes greater development of dendrites and synapses.

The most likely explanation for these anomalous results is that the SE pigs simply had greater nervous input to the somatosensory cortex. Direct observations indicated that rooting was more intense in SE pigs. Further research would be necessary to verify these observations and permit conclusions to be drawn.

The behavior of the IC pigs resembled the animals' excitable behavior described in sensory restriction research by Melzack (1954). Animals raised in an enriched environment were less excitable than those in barren surroundings (Walsh and Cummins 1975). The excessive belly nosing exhibited by the IC pigs may have been a futile attempt to reduce nervous system arousal. Repetitive stereotypic behavior can serve a de-arousal function (Dantzer and Hormede, 1983). The environment that the IC pigs lived in was much more barren than would ever be would ever be encountered in nature. In conclusion, the extent of neuronal development in the pig's somatosensory cortex cannot be used as a measure of environmental quality.

Another unexpected result was that the barrows had greater dendritic branching in both the visual and the somatosensory regions of the cerebral cortex in Trial 1 (Tables 8 and 9), whereas in Trial 2 the gilts had more. Juraska (1984) found in rats that gender had different effects in different cortical layers. For example, there was little gender effect on visual cortex in layer IV, but a definite effect in layer III. Within the same gender, cortical layer has an effect on dendritic branching in rats: "Granule cells with somata in the superficial third of the granule cell layer had substantially more dendritic material than those with somata in the deep portions of the cell layer" (Green and Juraska, 1985).

Both apical and basilar processes were drawn for all Trial 1 pigs, but the high frequency of apical process transection rendered these structures useless for data analysis. In Trial 2, no attempt was made to find cells with relatively intact apical processes This facilitated the finding of more drawable cells close to the surface of the cortex. Therefore, It is possible that in Trial 1 pigs many cells were in deeper layers than was the case in Trial 2 pigs Further research would be required to verify differential gender effects in different cortical layers of the pig.


Adrian, E.D. 1943. Afferent areas in the brain of ungulates. Brain 66:7-103.

Aftanas, M. and J.P. Zubek. 1964. Interlimb transfer of changes in tactual acuity following occlusion of a circumscribed area of the skin. Percept. Motor Skills 18:437-442.

Arnold, G.W. and M.L. Dudzinski. 1978. Ethology of Free-Ranging Domestic Animals. Elsevier Scient. Publ. Co., Amsterdam, Netherlands.

Arnold, G.W. and R.A. Miller. 1977. Effects of nutritional experience in early and adult life on the performance and dietary habits of sheep. Appl. Anim. Ethol. 3:5-26.

Barton-Gade, P. 1985. Developments in the pre-slaughter handling of slaughter animals. Proc. European Meeting of Meat Res. Workers. Paper 1:1, pp 1-6.

Beaulier, C. and M. Colonnier. 1987. Effect of richness of the environment on the cat visual cortex. J. Comp. Neurol. 266:478-494.

Bennett, E.L., M.C. Diamond, D. Krech, and M.R. Rosenzweig. 1964. Chemical and anatomical plasticity of the brain. Science 146:610-619.

Bennett, M.H., R.F. Dyer, and J.D. Dunn. 1972. Light induced retinal degeneration: effect upon light-dark discrimination. Exper. Neurol. 34:434-445.

Bhide, P.B. and K.S. Bedi. 1984. The effects of a lengthy period of environmental diversity on well-fed and previously undernourished rats. II. Synapse-to-neuron ratios. J. Comp. Neurol. 227:305-310.

Biben, H. 1982. Object play and social treatment of prey in bush dogs and crab-eating foxes. Behaviour 79:201-211.

Black, J.E., A.L. Jones, B.J. Anderson, K.R. Isaacs, A.A. Alcantara, and W.T. Greenough. 1987. Cerebellar plasticity: Preliminary evidence that learning rather than repetitive motor exercise, alters cerebellar cortex thickness in middle aged rats. Proc. Soc. Neurosci. 13:1596.

Brownlee, A. 1984. Animal play. Appl. Anim. Behav. Sci. 12:307-312.

Brownlee, A. 1954. Play in domestic cattle in Britain: analysis of its nature. Brit. Vet. J. 110:48-68.

Bryant, M.J. and R. Ewbank. 1972. Some effects of stocking rate and group size upon agonistic behaviour in.groups of growing finishing pigs. Brit. Vet. J. 128:64.

Bure, R.G. 1981. Animal well-being and housing systems for piglets. In: W. Sybesma (Ed.), The Welfare of Pigs, pp. 198-206. Martinus Nijhoff Publishers, Boston, MA.

Butler, R.A. 1953. Discrimination learning by rhesus monkeys to visual-exploration motivation. J. Comp. Physiol. Psych. 46:95.

Byers, J.A. 1984. Play in ungulates. In: P.K. Smith (Ed.), Play in Animals and Humans, pp. 43-65. Basil Blackwell, New York, NY.

Byers, J.A. and M. Bekoff. 1981. Social spacing and cooperative analysis of the collared peccary, Tayassu Tajacu. J. Mammal. 62:767-785.

Calkins, C.R., G.W. Davis, N.A. Cole, and D.A. Hutsell. 1980. Incidence of bloodsplashed hams from hogs subjected to certain antemortem handling methods. J. Anim. Sci. 50 (Suppl. 1):15 (Abstr.).

Campbell, A.W. 1905. Histological Studies on the Localisation of Cerebral function. Cambridge: Cambridge University Press.

Canadian Meat Council. 1980. Guide to PSE Pork. Canadian Meat Council, Islington, Ontario.

Chang, F.L.F. and W.T. Greenough. 1982. Lateralized effects of monocular training on dendritic branching in adult split-brain rats. Brain Res. 232:283-292.

Cross, H.A. and H.F. Harlow. 1965. Prolonged and progressive effects of partial isolation on the behavior of Macaque monkeys. J. Exp. Res. in Personality, Vol. 1, pp. 39-49.

Crowell-Davis, S.L., K.A. Houpt, and L. Kane. 1987. Play development in Welsh pony (Equus caballus) foals. Appl. Anim. Behaviour Sci. 18:119-131.

Curtis, S.E. and G. L. Morris. 1982. Operant supplemental heat in swine nurseries. Proc. Second Int. Livestock Environment Symp. pp. 295-297. Am. Soc, Agr. Eng., St, Joseph, MI.

Damasio, A. and R. Maurer. 1978. A neurological model for childhood autism. Arch. Neurol. 35:777-786.

Dantzer, R. 1986. Behavioral, physiological, and functional aspects of stereotyped behavior: A review and reinterpretation. J. Anim. Sci. 62:1776-1786.

Dantzer, R. 1973. Etude de la stabilisation des rhythmes d'activite locomotrice de porcelets introduits dans in nouvel environment. J. Physiol. (Paris) 66:495.

Dantzer, R. and G. Mailha. 1972. Mise en evidence d'un rhythme dans le comportement d'activite motrice du porcelet. C. R So. Biol. 166:456.

Dantzer, R. and P. Mormede. 1983. De-arousal properties of stereotyped behaviour: evidence from pituitary-adrenal correlates in pigs. 1983. Appl. Anim. Ethol. 10:233-244.

Dawkins, M.S. 1982. Elusive concept of preferred group size in domestic hens. Appl. Anim. Ethol. 8:365.

Diamond, M.C., C.A. Ingram, R.E. Johnson, E.L. Bennett, and M.R. Rosenzweig. 1976. Effects of environment on morphology of rat cerebral cortex and hippocampus. J. Neurobiol. 7:75-85.

Diamond, M.C., D. Krech, and M.R. Rosenzweig. 1964. The effects of an enriched environment on the histology of the rat cerebral cortex. J. Comp. Neurol. 123:111-120.

Diamond, M.C., F. Law, H. Rhodes, B. Lindner, H.R. Rosenzweig, D. Krech, and E.L. Bennett. 1966. Increases in cortical depth and glia numbers in rats subjected to an enriched environment. J. Comp. Neurol. 128:117-126

Diamond, M.C., M.R. Rosenzweig, E.L. Bennett, B. Lindner, and L. Lyon. 1972. Effects of environmental enrichment and impoverishment on rat cerebral cortex. J. Neurobio. 3:47-64.

Dickerson, J.W.T. and J. Dobbing. 1966. Prenatal and postnatal growth and development of the central nervous system of the pig. Proc. Royal Soc. (London) Bio. Sci. 166:384-406.

Dinger, J.E. and E.E. Moiles. 1986. Eftect of controlled exercise on libido 2-yr-old stallions. J. Anim. Sci. 62:1220-1223.

Dobao, M.T., J. Rodriganez, and L. Silio. 1984-1985. Choice of companions in social play in piglets. Appl. Anim. Ethol. 13:259-266.

Dodman, N.H., L. Shuster, M.H. Court, and R. Dixon. 1987. Investigation into the use of narcotic antagonists in the treatment of stereotypic behavior pattern. Crib biting in the horse. Am. J. Vet. Res. 48:311-319.

Duncan, I.J.H. 1978. The interpretation of preference tests in animal behaviour. Appl. Anim. Ethol. 4:197-200.

Ehrlich, A. 1959. The effects of past experience on the rat's response to novelty. Can. J. Psychol. 15:15-19,

Eibl-Eibesfeldt, I. 1978. On the ontogeny of behavior of a male badger (Meles meles L.) with particular reference to play behavior. In: D. Mueller-Schwarze (Ed.), Evolution of Play Behavior. Benchmark Papers in Animal Behavior, Vol. 10. Dowden Hutchins Ross, Stroudsburg, PA.

Ewbank, R. 1978. Stereotypies in clinical practice. Proc. 1st World Con. Ethol. Applied to Zootechnics. pp. 499-502. Madrid, Spain.

Ewbank, R. and M.J. Bryant. 1972. Aggressive behaviour amongst groups of domesticated pigs kept at various stocking rates. Anim. Behav. 20:21-28.

Fagen R. 1981. Animal Play Behavior. Oxford University Press, New York, NY.

Fagen, R. 1984. Play and behavioural flexibility. In. P. K. Smith (Ed.), Play in Animals and Humans, pp. 159-173. Basil Blackwell, New York, NY.

Farmer, C. and G.I. Christison. 1982. Selection of perforated floors by newborn and weanling pigs. Can. J. Anim. Sci. 62:1229-1236.

Floeter, M.K. and W.T. Greenough. 1979. Cerebellar plasticity: modification of Purkinje cell structure by differential rearing in monkeys. Science. 206:227-229.

Fox, M.W. 1984. Farm Animals, Husbandry Behavior and Veterinary Practice. University Park Press, Baltimore, MD.

Fox, M.W. 1971. Integrative Development of Brain and Behavior in the Dog. Chicago: University of Chicago Press.

Fraedrich, H. 1974. A comparison of behaviour in the Suidae. Proc. Int. Symp. on Behavior of Ungulates and Its Relation to Management, Vol. I, pp. 133-143. Univ. of Calgary, Calgary, Alberta.

Fraser, D. 1975. The effect of straw on the behavior of sows in tether stalls. Anim. Prod. 21:59-68.

Friend, T. and L. Taylor. 1986. Open field test behavior of growing swine maintained on a concrete floor and pasture. Appl. Anim. Sci. 16:143-148.

Gill, J.L. 1986. Repeated measurement: sensitive tests for experiments with few animals. J. Anim. Sci. 63:943-954.

Gilman, S., J.R. Bloedel, and R. Lechtenberg. 1981. Disorders of the Cerebellum. F.A. Davis Co., Philadelphia, PA.

Glaser, E.M. and H. Van der Loos. 1981. Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J. Neurosci. Methods 4:117-125.

Gonyou, H.W., P.H. Hemsworth, and J.L. Barnett. 1986. Effects of frequent interactions with humans on growing pigs. Appl. Anirn. Behav. Sci. 16:269-278.

Grandin, T. 1988. Hog psychology: an aid to handling. Agri-Practice 9(4):22-26.

Grandin, T. 1987. Animal handling in E.O. Price (Ed.), Farm Animal Behavior. Vet. Clin. N. Amer. 3:323-338.

Grandin, T. 1986. Good pig handling improves pork quality. Proc. European meeting of Meat Res. Workers. Paper 2:12, pp. 105-108.

Grandin, T. 1984. Reducing PSE Losses. Meat Processing, March 23:53.

Grandln,.T. 1982. Pig behavior studies applied to slaughter plant design. Appl. Anim. Ethol. 9:141-151.

GrandIn T., S.E. Curtis, and W.T. Greenough. 1983. Objective measurements of the effects of environmental complexity In young pigs. Swine Res. Reports, Report 1983-18.

Grandin, T., S.E. Curtis, T.M. Widowski, and J.C. Thurmon. 1986. Electro-immobilization versus mechanical restraint in an avoid-avoid choice test for ewes. J. Anim. Sci. 62:1469-1480.

Grandin T., D.0. DeMotte, W.T. Greenough, and S.E. Curtis. 1988. Perfusion method for preparing pig brain cortex for Golgi-cox impregnation. Stain Tech. 63:77-181.

Graves, H.B., K.L. Graves, and G. W. Sherritt. 1978. Social behavior and growth of pigs following mixing during the growing-finishing period. Appi. Anim. Ethol. 4:169-180.

Green, E.J., W.T. Greenough, and B.E. Schlumpf. 1983. Effects of complex or isolated environments on cortical dendrites of middle-aged rats. Brain Res. 264:233-240.

Green, E.J. and J.M. Juraska. 1985. The dendritic morphology of hippocampal dentate granule cells varies with their position in the granule cell layer: a quantitative Golgi study. Exp. Brain Res. 59:582.

Greenough, W.T. 1984. Anatomical substrates of behavioral plasticity. In C.W. Cotman and R.F. Thompson (Eds.) Plasticity in Neurobiology: Cell to Behavior: 1984 Society for Neuroscience Short Course Syllabus. Soc. Neurosci. Washington DC, pp. 42-53.

Greenough, W.T. 1975. Experiential modification of the developing brain. Am. Sci. 63:37-46.

Greenough, W.T. 1982. Personal Communication.

Greenough W.T. and C.H. Bailey. 1988. The anatomy of a memory: convergence of results across a diversity of tests. Trends Neurosci. 11:142-147.

Greenough, W.T. and F.F. Chang. 1985. Synaptic structural correlates of information storage in mammalian nervous systems. In: Synaptic Plasticity, pp. 335-363. Guilford Press, New York, NY.

Greenough, W.T., H.N.F. Hwang, and C. Gorman. 1985. Evidence of active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proc. Nat. Acad. Sci. 82:4549.

Greenough, W.T. and J.H. Juraska. 1979. Experience induced changes in fine brain structure: their behavioral imolications. In: M. E. Hahn, C. Jensen, and B. C. Dudek (Eds.), Development and Evolution of Brair Size: Behavioral Implications, pp. 295-320. Academic Press, New York

Gross, W.B. and P.B. Siegel. 1983. Socialization, the sequencing of environmental factors, and their effects on weight gain and disease resistance of chickens. Poult. Sci. 62:592-598.

Gundlach, V.H. 1968. Brutforsorge, Brutpflege, Verhaltensontgenese und Tagesperiodek beim Europaeischen Wildschwein (Sus scrofa L.). Z. Tierpsychol. 24:955.

Hails, M.R. 1978. Transport stress in animals: a review. Anim. Regul. Stud. 1:289-343.

Harlow, H.F. and R.R. Zimmerman. 1959. Affectional responses in the infant monkey. Science 130:421-432.

Harrison, R. 1964. Animal Machines. Stuart, London, England.

Hediger, H. 1968. The Psychology and Behavior of Animals in Zoos and Circuses. Dover Publications, New York, NY.

Hemsworth, P.H., J.L. Barnett, and C. Hansen. 1981. The influence of handling by humans on the behaviour, growth and corticosteroids in the juvenile female pig. Horm. Behav. 15:396-403.

Hemsworth, P.H., J.L. Barnett, C. Hansen, and H.W. Gonyou. 1986. The influence of early contact with humans on subsequent behavioral response of pigs to humans. Appl. Anim. Behav. Sci. 15:55-63.

Hitchcock, D.K. and G.D. Hutson. 1979. The movement of sheep on inclines. Australian J. Exp. Agr. Anim. Husb. 19:176-182.

Hughes, B.0. 1976. Preference decisions of domestic hens for wire or litter floors. Appl. Anim. Ethol. 2:155.

Hughes, B.0. and A.J. Black. 1973. The preference of domestic hens for different types of battery cage floor. Brit. Poult. Sci. 14:615-619.

Hughes, B.0. and A.J. Black. 1976. The influence of handling on egg production, egg shell quality and avoidance behavior in hens. Brit. J. Poult. Sci. 17:135-144.

Hughes, G.P. and D. Reid. 1951. Studies on the behavior of cattle and sheep in relation of the utilization of grass. J. Agric. Sci. 41:350.

Hutson, G.D. 1981. Sheep movement on slatted floors. Australian J. Exp. Agr. Anim. Husb. 21:474-479.

Inhelder, E. 1978. Object play in the Indian rhino (Rhinoceros unicornis). In: D. Mueller-Schwarze (Ed); Evolution of Play Behavior. Benchmark Papers in Animal Behavior, Vol. 10. Dowden Hutchinson Ross, lnc., Stroudsburg, PA.

Jones, J.E.T. 1969. The incidence and nature of diseases causing death in pigs aged 2-7 months in a commercial herd. Br. \/et. J. 125:492-505.

Juraska, J. 1987. Personal Coinmunication.

Juraska, J.M. 1984. gender differences in dendritic response to differential experience in the rat visual cortex. Brair Res. 295:27-34.

Juraska, J.M. , J.M. Fitch, C. Henderson, and N. Rivers. 1985. gender differences in the dendritic branching of dentate granule cells following differential experience. Brain Res. 333:73-80.

Juraska, J.M., W.T. Greenough, and J.W. Conlee. 1983. Differential rearing affects responsiveness of rats to depressant and convulsant drugs. Physiol. Behavior 3:711-715.

Katz, H.B. and C.A. Davis. 1984. Effects of differential environments on the cerebral anatomy of rats as a function of previous and subsequent housing conditions. Exper. Neurol. 83.274-287.

Kelley, K.W., J.J. McGlone, and C.T. Gaskins. 1980. Porcine aggression: measurement and effects of crowding and fasting. J. Anim. Sci, 50:326-344.

Korn, J.H. and K.E. Moyer. 1968. Behavioral effects of isolation in the rat: the role of gender and time of isolation. J. Genetic Psych. 113:263-273.

Krech, D., M.R. Rosenzweig, and E.L. Bennett. 1963. Effects of complex environment and blindness on rat brain. Arch. Neurol. 8:403-412.

Kruska, D. 1972. Volumenvergleich optischer hirnzentren bei wild und hausschweinen. Anat. Entwickl. Gesch. 138:265-282.

Kruska, D. 1971. A volumetric comparison of some visual centers in the brains of wild boars and domestic pigs. Z. Anat Entwickl. 138:265-282

Lehner, P.N. 1979. Handbook of Ethological Methods. Garland STPM Press, New York, NY,

Levine, S., G.C. Haltmeyer, G. Karas, and V. Denenberg. Physiological and behavioral effects of infantile stimulation. Physiol. Behav. 2:55-69.

Markowitz, H. 1982. Behavioral Enrichment in the Zoo. Van Nostrand Reinhold Co. New York, N. Y. 1967.

Martin, P. 1984. The (four) whys and wherefores of play in cats: a review of functional, evolutionary, developmental and causal issues. In: P. K. Smith (Ed.), Play in Animals and Humans. Basil Blackwell, New York, NY.

Mason, W.A. 1960. The effects of social restriction on the behavior of rhesus monkeys. J. Comp. Physiol. Psych. 6:582- 589

Mason, J. and P. Singer. 1980. Animal Factories. Crown, New York, NY.

Mayes, H.F. and G.W. Jesse. 1980. Heartrate data in feeder pigs. Tech. Paper No. 80-4023, Amer. Soc. Agric. Engineers, St. Joseph, MI.

McBride, G., J.W. James, and N. Hodgens. 1964. Social behaviour in domestic animals: IV, Growing pigs. Anim. Prod. 6:129-139.

McFarlane, J.M., K.E. Boe, and S.E. Curtis. 1988. Turning and walking by gilts in modified gestation crates. J. Anim. Sci. 66:326-333.

McGlone, J.J. and S.E. Curtis. 1985. Behavior and performance of weanling pigs in pens equipped with hide areas. J. Anim. Sci. 80:20-24.

McGlone, J.J. and J.L. Morrow. 1987. Individual differences among mature boars in T-maze preference for estrous or non-estrous sows. Appl. Anim. Behav. Sci. 17:77-82.

McGray, G.M. 1978. Excessive masturbation of childhood: a symptom of tactile deprivation. Pediatrics 62:277-279.

Meese, G.B. and R. Ewbank. 1973. The establishment and nature of the dominance hierarchy in the domesticated pig. Anim. Behav. 21:328-334.

Melzack, R. 1969. The role of early experience in emotional arousal. Ann. N.Y. Acad. Sd. 159:721-730.

Melzack, R. 1954. The genesis of emotional behavior: an experimental study of the dog. J. Comp. Physiol. Psych. 47:166-188.

Melzack, R. and S.K. Burns. 1965. Neurophysiological effects of early sensory restriction. Exp. Neurol. 13:163-175.

Melzack, R. and W.R. Thompson. 1956. Effects of early experience on social behavior. Canad. J. Psych:. 10:82-90.

Morrison, S.R., H.F. Hintz, and R.L. Givens. 1968. A note on the effect of exercise on behavior and performance of confined swine. Anim. Prod. 10:341.

Nehring, A. 1981. One answer to the confinement pig problem. Int. J. Stud. Anim. Prob. 2(5):256-259.

Oppenheim, R.W. 1985. Naturally occurring cell death during neural development. Trends Neurosci. 8:487-493

O'Steen. 1970. Retinal and optic nerve serotonin and retinal degeneration as influenced by photoperiod. Exp. Neurol. 27:194-205.

Parnavelas, J.G., A. Globus, and P. Kaups. 1973. Continuous illumination from birth affects spine density of neurons in the visual cortex of the rat. Exp. Neurol. 40:742-747.

Peischel, A., R.R. Schalles, and C.E. Owenby. 1980 Effect of stress on calves grazing on Kansas Hills range. J. Anim. Sci. 24 (Suppl. 1):25 (Abstr.).

Phillips P.A., B.K. Thompson, and D. Fraser. 1988. Preference tests on ramp designs for young pigs. Can. J. Anim. Sci. 68:41-48.

Pysh, J.J. and G.M. Weiss. 1979. Exercise during development induces an increase in Purkinje cell dendritic tree size. Science 206:230-232.

Rakic, P., J.P. Bourgeois, M.F. Eckenhoff, N. Zecevic, and P.S. Goldman-Rakic. 1980. Concurrent overproduction of synapses the in diverse regions of primate cerebral cortex. Scence 232:232-235.

Randolph, J.H., C.L. Cromwell, and T.S. Stahly. 1981. Effects of group size and space allowance on performance and behavior of swine. J. Anim. Sci. 53:922-927.

Reid, R.L. and S.C. Mills. 1962. Studies of the carbohydrate metabolism of sheep. XVI. The adrenal response to physiological stress. Aust. J. Agric. Res. 13:282-426.

Riitinen, M.L., F. Lindroos, A. Kimanen, E. Pieninkeroinen, I. Pieninkeroinen, J. Sippola, J. Veilahti, M. Bergstrom, and G. Johansson. 1986. Impoverished rearing and conditions increase stress induced irritability in mice. Devel. Psychobiol. 19:105-111.

Rosenzweig, M.R. and E.L. Bennett. 1969. Effects of differential environments on brain weights and enzyme activities in gerbils, rats and mice. Devel. Psychobiol. 2:87-95.

Rushen, J, 1986. Aversion of sheep to electro-immobilization and physical restraint. Appl. Anim. Behav. Sci. 15:315-324.

Sachs, B.D. and V.S. Harris. 1978. gender differences and developmental changes in selected juvenile activities (play) of domestic lambs. Anim. Behav. 26:678-684.

Sandman, C.A., P.C. Dotta, J. Barron, F.K. Hoehler, C. Williams, and J.M. Swanson. 1983. Naloxone attenuates self-abusive behavior in developmentally disabled clients. Appl. Res. in Mental Retardation. 4:5-11

SAS. 1982. SAS/User's Guide: Statistics. SAS Inst., Inc. Cary, NC.

Schoen, A.M.S., E.M. Banks, and S.E. Curtis. 1976. Behavior of young Shetland and Welsh ponies (Equus caballus). Biol. Behav. 1:192-216.

Schultz, D, 1965. Sensory Restriction. Academic Press, New York, NY.

Shapiro, W. and K.R. Vukovich. 1970. Early experience effects upon cortical dendrites: A proposed model for development. Science 167:292.

Sherritt, G.W., H.B. Graves, and J.L. Gobble. 1974. Effects of mixing pigs during the growing finishing period. J. Anim. Sci. 39:834-837.

Sholl, D.A. 1956. The Organization of the Cerebral Cortex, Methuen & Co. Ltd., London.

Simons, D. and P. Land. 1987. Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326:694-697.

Singer, P. 1976. Animal Liberation. Random House, New York, NY.

Spinelli, D.N., F.E. Jensen, and G. Viana Di Prisco. 1980. Early experience effect on dendritic branching in normally reared kittens. Exper. Neurol. 68:1-11.

Squires, V.R. 1974. Grazing distribution and activity patterns of Merino sheep on Saltbush community in southeast Australia. Appl. Anim. Ethol. 1:17.

Stell, M. and A. Riesen. 1987. Effects of early environments on monkey cortex neuroanatomical changes following somatomotor experience: Effects on layer III pyramidal cells in monkey cortex. Behav. Neurosci. 101:341-346.

Stolba, A. 1981. Alternatives to Intensive Husbandry Systems. Universities Federation for Animal Welfare, South Mimms, Potters Bar, Hertfordshire, England.

Stolba, A. and D.G.M. Wood-Gush. 1980. Arousal and exploration in growing pigs in different environments Appl. Anim. Ethol. 6:382-383.

Struble, R.G. and A.H. Riesen. 1978. Changes in cortical dendritic branching subsequent to partial social isolation in stumptail monkeys. Devel. Psychobio. 11:479-486.

Sutula, T., H. Xiao-Xian, J. Cavazos, and G. Scott. 1988. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239:1147-1150.

Symoens, J. and M. van der Brande. 1969. Prevention and cure of aggressiveness in pigs using the sedative Azaperone. Vet. Rec. 85:64-67.

Thurley, D.C. and K.P. McNatty. 1973. Factors affecting peripheral cortisol levels in unrestricted ewes. Acta Endocrinologica 74:331-338.

Turner, A.M. and W.T. Greenough. 1985. Differential rearing effects on rat visual cortex synapses I. Synaptic and neuronal density and synapses per neuron. Brain Res. 329:195-203.

Tyler, S.J. 1972. The behavior and social organization of the new forest ponies. Anirn. Behav. Monog. 5:85-196.

Uylings, H.B.M., K. Kuypers, M.C. Diamond, and W.A.M. Veltrnan. 1978. Effects of different environments on plasticity of dendrites of cortical pyramidal neurons in adult rats. Exper. Neurol. 62:658-677.

Valzelli, L. 1973. The isolation syndrome in mice. Psychopharmacologia (Berl.) 31:305-320.

van Lawick, H. and J. Goodall. 1971. Innocent Killers. Houghton Mifflin, Boston, MA.

van Putten, G. 1969. An investigation into tail biting among fattening pigs. Brit. Vet. J. 125:511

van Putten, G. 1980. Objective observations on the behaviour of fattening pigs. Anim. Reg. Stud. 3:105-118.

van Putten, G. 1978. The so-called play of piglets reared in flatdeck cages. Deutsche Tieraerztl. Wochenschi. 85:462-464,

van Putten, G. and W.J. Elshof. 1978. Observations on the effect of slaughter and transport on the well being and lean quality of pigs. Anim. Regul. Stud. 1:247-271.

van Rooijen, J. 1982. The value of choice tests in assessing welfare of domestic animals. Appl. Anim. Ethol. 8:295-299.

Volkmar, F.R. and W.T. Greenough. 1972. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176:1445-1447.

Walsh, R.N. and R.A. Cummins. 1975. Mechanisms mediating the production of environmentally induced brain changes. Psych Bull. 82:986-1000.

Warriss, P.D., S.C. Kestin, and J.M. Robinson. 1983. A note on the influence of rearing environment on meat quality of pigs. Meat Sci. 9:271-279.

West, M.J. 1977. Exploration and play with objects in domestic kittens. Develop. Psychobiol. 10:53.

Wood-Gush, D.G.M. and R.G. Beilharz. 1983. The enrichment of a bare environment for animals in confined conditions. Appl. Anim. Ethol. 10-209.

Woolsey, C.N. and D. Fairman. 1946. Contralateral, ipsilateral, and bilateral representation of cutaneous receptors in somatic areas I and II of the cerebral cortex of pig, sheep, and other mammals. Surgery 19:684-701.

Zar, J.H. 1984. Biostatistical Analysis. Prentice Hall, Englewood Cliffs, NJ.

Zentall, S.S. and T.R. Zentall. 1983. Optimal stimulation: a model for disordered activity and performance in normal and deviant children. Psych. Bull. 94:446-471.

Zubek J.P., J. Flye, and M. Aftanas. 1964a. Cutaneous sensitivity after prolonged visual deprivation. Science 144:1591-1593.

Zubek, J.P., J. Flye, and D. Willows. 1964b. Changes in cutaneous sensitivity after prolonged exposure to unpatterned light. Psychon. Sci. 1:283-284

NOTE: The diagrams and tables are missing. If you want them write to:

Temple Grandin
Dept. of Animal Science
Colorado State University
Fort Collins, Colorado 80523 USA

Other sections of this dissertation that are not posted on this webpage can also be sent.

Click here to return to the Homepage for more information on animal behavior, welfare, and care