Environmental enrichment: The influences of restricted daily exposure and subsequent exposure to uncontrollable stress

Physiology & Behavior, Vol. 51, pp. 309-318. ©PergamonPress plc, 1992. Printedin the U.S.A.

0031-9384/92 $5.00 + .00

Environmental Enrichment: The Influences of Restricted Daily Exposure and Subsequent Exposure to Uncontrollable Stress D A V I D R. W I D M A N , G L E N N C. A B R A H A M S E N A N D R O B E R T A. R O S E L L I N I t

State University of New York at Albany, Department of Psychology, 1400 Washington Ave., Albany, N Y 12222 R e c e i v e d 17 J u n e 1991 WIDMAN, D. R., G. C. ABRAHAMSEN AND R. A. ROSELLINI. Environmental enrichment: The influences of restricted daily exposure and subsequent exposure to uncontrollable stress. PHYSIOL BEHAV 51(2) 309-318, 1992.--Environmental enrichment has been proposed to enhance an animal's subsequent ability to learn. While this proposal has received considerable support from experiments involving maze tasks, it has received equivocal support from experiments employing operant and pavlovian tasks. The purpose of the present study is two-fold. The first is to demonstrate that a regimen of restricted daily exposure to environmental enrichment is capable of producing effects similar to those using more standard exposure regimens when compared to the most appropriate control, a group given social exposure. The second is to examine the proposed learning enhancement of environmental enrichment on an operant task both before and following exposure to uncontrollable stress. Uncontrollable stress, as interpreted by learned-helplessness theory, results in the formation of an expectancy of response-reinforcer independence which proactively interferes with the subsequent acquisition of response-outcome associations. It may be possible, then, that environmental enrichment and uncontrollable stress may interact in such a way as to allow the potential learning effects of environmental enrichment to be assessed on an operant task. Rats were exposed to differential environments; one group exposed to an enriched environment and another exposed to a social environment 2 hours daily for 30 days. Each group was then tested on the object-exploration test. Following the acquisition of an appetitive-operant response, a subset of these two groups was exposed to either controllable, uncontrollable, or no stress using parameters known to induce learned helplessness. Animals were then tested on an appetitive-noncontingent test. It was found that, while the enrichment procedure was effective in producing effects on the object-exploration test, environmental enrichment did not modify the acquisition of the operant or the effect produced by uncontrollable stress on the appetitive-noncontingent test. Environmental enrichment Restricted daily exposure Appetitive-operant responding

Exploration

THERE are a number of experimental manipulations which have been theorized to affect learning. Two of these, which have separately received a considerable amount of experimental attention in the past two and a half decades, are environmental enrichment and exposure to uncontrollable stress. Environmental enrichment is thought to enhance an animal's ability to learn (35), while exposure to uncontrollable stress as interpreted by the learned-helplessness hypothesis, is thought to proactively interfere with the animal's ability to acquire response-outcome associations (22). First, we will briefly review each of these two areas of research and then present an experiment which is designed to answer two questions regarding these areas. Environmental enrichment has been associated with a specific set of behavioral as well as physiological consequences [for reviews see (6, 13, 35, 53)]. These effects are usually observed in the comparison of three sets of littermates, one reared in an enriched environment, another reared in a social environment and a third reared in an impoverished, isolated environment. The enriched environment usually consists of a group of animals housed

Uncontrollable stress

in a large cage with a number of stimulus objects. The social environment (also referred to as the Group Condition) is similar to the enriched environment, consisting of group-housed animals, except that there are no stimulus objects present. The impoverished environment consists of individually housed animals in standard laboratory cages without access to stimulus objects. Physiologically, environmental enrichment results in a specific set of neuroanatomical and neurochemical effects. The classic gross anatomical effects are an increase in the total cortical weight and a thickening of the cortex. These anatomical effects are particularly noticeable in the occipital cortex (13,35). The most consistent effect on anatomy is that of increasing the cortical to subcortical weight ratio (46). Environmental enrichment has also been demonstrated to affect the size, number, and configuration of synapses in the occipital cortex (14). It also leads to increased amounts of acetylcholinesterase and cholinesterase (35,53). This increased cholinesterase activity is seen even when the increase in cortical weight has been taken into account. Acetylcholinesterase activity per unit of brain, however, de-

IRequests for reprints should be addressed to Robert A. Rosellini.

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creases in animals exposed to environmental enrichment (35,53). Another common finding is that the levels of RNA relative to DNA are elevated in animals exposed to environmental enrichment (35,53). These effects, or subsets of these effects, have been observed with exposure durations ranging from several months exposure (4) to a minimum of 10 min per day for 4 days (10). Behaviorally, there are a number of tasks which distinguish enriched animals from their socially-housed and impoverished counterparts. Among these tasks, the most common is the HebbWilliams maze (15,30). The typical result is that enriched animals show fewer errors on a standardized set of maze problems (35, 44, 45, 50, 51). Environmental enrichment has also been demonstrated to affect performance on the Lashley III maze (11) and on discrimination-reversal tasks (9, 18, 26). It should be noted, however, that differences between the social group and the enriched group on the discrimination-reversal tasks are equivocal. Effects on performance in the Hebb-Williams maze have been observed following exposure durations ranging from several months (3) to as few as 10 days in the rat (4). Renner and Rosenzweig (34) and Renner (32) have demonstrated that daily 24-hour exposure to environmental enrichment for 30 days also can affect the amount and character of the exploration of objects in a familiar environment. Furthermore, Widman and Rosellini (58) have demonstrated similar effects on this object-exploration test with as little as 2 hours of daily exposure to environmental enrichment for 30 days. We will now turn to an overview of the effects of uncontrollable stress. Exposure to uncontrollable stress has been associated with a specific constellation of behavioral as well as physiological consequences for an organism. These include associative, attentional, motivational, neurochemical, and emotional effects, which specifically result from the uncontrollability of the stressor as they are not typically observed in animals afforded control over the identical stressor's termination (20, 22, 54). Uncontrollable stress proactively interferes with the organism's ability to acquire response-outcome associations when tested using either the termination of aversive events or the production of appetitive events as outcomes (21, 29, 36, 37). It also results in decreased general activity and deficits in initiating responding in the presence of electric shock (1, 25, 39). It has additionally been shown to have a variety of neurochemical effects such as modification of cholinergic, serotonergic, and GABAergic systems (49,57). Other physiological and neurochemical effects have also been reported following exposure to uncontrollable stress, such as analgesia and altered immune function (17, 18, 52). Furthermore, exposure to uncontrollable stress results in negative emotional consequences, such as increased ulcers (56), heightened levels of fear to the context in which the stressor is experienced (23, 27, 40, 41) and increased neophobia (24,42). Another finding from the learned-helplessness literature which is also of interest for the present experiment is that learned-helplessness effects appear to be reinforcer general. There have been demonstrations within the learned-helplessness literature of specific classes or modalities of reinforcers which, when presented uncontrollably, can have proactive effects on different classes or modalities of reinforcers. For example, it has been demonstrated that uncontrollable shock can lead to future deficits in the acquisition of a response for food (36). It has similarly been demonstrated that uncontrollable presentation of food can lead to future deficits in the acquisition of a shock-escape response (12). In another demonstration of this reinforcer generality, Rosellini, DeCola, Plonsky, Warren and Stilman (38) trained animals to respond for food on a random interval schedule, then administered stress training, either controllable, uncontrollable, or no

WIDMAN. ABRAHAMSEN AND R()SELI.IN[

shock. The animals were returned to the original operan~ task, but the task was changed such that reinforcers were delivered ',~ the same rate but now independent of the animals' responding. In this appetitive-noncontingent test, Rosellini et al. (38) found that uncontrollably stressed animals learned to cease responding sooner and to a greater extent than did the controllably shocked animals or the nonshocked animals. This demonstrates that un~ controllable shock can lead to future effects on appetitivenoncontingent as well as appetitive-contingent tasks (37-3el, 551, The purpose of the present study is two-fold. The first is to examine the effects of restricted exposure to an enriched environment compared with equivalent exposure to a strictl~ social environment on the object-exploration task. Widman and Rosellini (58) demonstrated that restricted daily exposure to environmental enrichment produced expected changes ia exploratory behavior as compared with an isolated group. However, as has been argued by others (43,46), the social condition is the best standard from which to assess environmental enrichment effects. Thus, the present study will assess whether the findings of Widman and Rosellini (58) were specifically due to environmental enrichment and not social exposure. The second purpose of the present study is to examine the effects of environmental enrichment on the consequences of future exposure to uncontrollable stress. Theoretically, an interaction between uncontrollable stress and environmental enrichment is of interest due to the elusive nature of the proposed enhancement of learning following exposure to environmental enrichment. While such an enhancement has been documented using a wide variety of maze problems, it has proven difficult to demonstrate such an effect using less spatial tests of learning ability, such as those from operant and Pavlovian conditioning paradigms. A small number of studies have reported enhancements in the performance of enriched animals on such tasks [for example: (11, 28, 31)]. However, other studies have failed to find such enhancements (8, 5, 26, 28). Generally, these failures to demonstrate enhanced learning ability have been interpreted as failures of the test task. Renner and Rosenzweig (35), for example, have proposed that environmental-enrichment effects will only be observed on tasks involving a high degree of difficulty or complexity. This proposal would argue that performance on simple tasks, such as simple operant acquisition, does not require the additional learning ability obtained from environmental enrichment. This would effectively leave intact the notion that environmental enrichment does induce an enhancement in the organism's general learning ability. We propose that environmental enrichment and uncontrollable stress may interact due to the fact that both are theorized to affect organisms' ability to learn. It is hypothesized that uncontrollable stress will amplify the learning effect of environmental enrichment and allow for a clear demonstration of enhanced learning by enriched animals even on an operant task. Specifically, it is proposed that enriched animals may show a more robust effect of uncontrollable stress than the socially exposed animals. That is, environmental enrichment will facilitate the acquisition of the expectancy of response-reinforcer independence hypothesized by learned-helplessness theory to result from exposure to uncontrollable stress (22) relative to the social group. In order to address these two issues, animals were first exposed to either an enriched environment or a social environment for 2 hours daily. These two groups of animals were then tested on the object-exploration test to assess the effectiveness of the restricted regimen of environmental enrichment exposure (32, 34, 58). All animals were then trained to respond for food on a random interval schedule. Following this operant training, animals were randomly assigned to one of three groups: controlla-

RESTRICTED ENRICHMENT AND STRESS

ble, uncontrollable, or no stress--the triadic design typically used to assess the effects of the controllability of stress. The resuiting 6 groups were then tested on an appetitive-noncontingent test (38). This test was chosen for its demonstrated sensitivity to the effects of uncontrollable stress. Furthermore, it may also be sensitive to the effects of environmental enrichment. Ough, Beatty and Khalili (28) found enriched animals to be better at inhibiting responses on a DRL schedule than their impoverished, isolated counterparts. On the basis of this finding, we expect the environmentally enriched animals to cease their responding faster than the socially exposed animals on the appetitive-noncontingent test, regardless of their stress history. This is expected because both the DRL test and the appetitive-noncontingent test share the property of producing a decrement in the rate of responding where previously high rates of responding were reinforced. METHOD

Subjects The animals were 46 experimentally naive male SpragueDawley rats obtained from Blue Spruce Farms, Altamont, NY, at 25 days of age. They were pair housed until the beginning of environmental exposure. Animals were maintained on a 12-hour light/dark cycle during all segments of the study.

Apparatus The enriched environment and the objects which were placed into it have been described elsewhere (58). The social environment was the same cage as the enriched environment, devoid of stimulus objects. The home cage consisted of standard laboratory single cage housing (18.0 x 24.0 × 18.0 cm). The top, sides and back of these cages were solid stainless steel, while the floor and front wall were wire mesh. All environmental exposure was conducted in the main colony of our facility. The object-exploration test arena has similarly been described elsewhere (58). Four chambers were used for stress exposure. These are identical to those used previously in our laboratory and are described in detail elsewhere (42). Six operant chambers were used for the appetitive operant test segment. Each measured 28.3 × 2 1 . 7 × 2 0 . 5 cm. The two side walls and ceiling were made of clear Plexiglas and the front and back walls were of aluminum. The floor consisted of stainless steel rods 0.3 cm in diameter and spaced 1.0 cm apart. Centered on the front wall 2.0 cm above the floor was a hole 5.0 cm in diameter. The food cup was recessed within this hole 3.4 cm deep. Two galvanized iron touch-pad manipulanda were placed on the front wall. Each measured 3.0 x 5.5 cm and extended 1.7 cm into the box on a flat tang 3 . 0 x 1.7 cm. The center of each manipulanda was placed 6.0 cm from the center of the box, one to the right and the other to the left of center, and 4.2 cm from the grid floor to the bottom of each manipulanda. Food pellets (45 mg Noyes food pellets, Formula A) were delivered to these chambers by pellet dispensers which were mounted outside the chambers. Each chamber was placed into a sound-attenuating box, equipped with a ventilating fan. Control of the apparatus and recording of data were accomplished through the use of TRS-80 microcomputers.

Procedure The experiment consisted of three segments: 1) Differential environmental exposure, 2) object-exploration test, 3) appetitiveoperant test. The design of the experiment was a 2 x 3 factorial

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with environmental exposure [enriched (EC) or social exposure (SC)] and stress type [escapable shock (ES), yoked shock (YS), and no shock (NS)] serving as the two factors.

Environmental Exposure Animals were randomly assigned to the enriched condition (n = 23) or the social condition (n = 23) at 29 days of age. All animals were then individually housed in the home cages. Environmental exposure began at 30 days of age, Day 1 of the experiment, at which point EC animals were removed from their home cage and placed into the enriched environment in groups of 11 and 12 for 2 hours daily, beginning approximately 5 hours after the onset of the light portion of the light/dark cycle. The enriched environment contained a minimum of 12 stimulus objects at any one time, 3 of which were replaced daily from a pool of 20. Following the exposure of the EC animals, SC animals were removed from their home cages and placed into the social environment, also in groups of 11 and 12. Environmental exposure continued for 30 days before testing commenced and continued until stress exposure unless otherwise noted. Animals were exposed to the environmental conditions for a total of 40 days.

Object-Exploration Test The object-exploration test consisted of two phases: 1) Preexposure to the arena, and 2) arena test. Subjects were not exposed to either the enriched or social environment during the two days of this segment. Preexposure to the testing arena. On Day 31 of the experiment, animals were preexposed to the arena approximately 2 hours after the beginning of the dark portion of the light/dark cycle. A set of two novel objects was placed into the arena, one in the right zone and one in the left. The objects used for preexposure were a small metal mixing bowl (placed upside down measuring 57.0 mm high and 133.0 mm dia. at the base) and a standard type A red light bulb (57.0 mm long and 64.0 mm dia. at the widest point) in the right and left zones, respectively. The objects were chosen such that one was manipulable and the other nonmanipulable [see (32, 34, 42, 58)]. The manipulable object was of a size and weight such that it could potentially be moved and manipulated by the animal while the nonmanipulable object could neither be moved nor manipulated by the animal. While there are a number of object characteristics which could affect exploratory behavior, manipulability was chosen so as to be consistent with previous literature (32, 34, 42, 58). Animals were individually transported from their home colony to the arena in a white opaque Plexiglas holding cage (18.0 x 18.0 × 18.0 cm). They were then placed into the start box of the arena and the cover was placed onto the start box. The sliding door of the start box was raised and the animal was allowed access to the arena for a 10 min period. It should be noted that this preexposure phase and the subsequent test phase were conducted under red light illumination, in a sound attenuating chamber, and that the experimenter was not present in the testing room. Arena test. The arena test, conducted on Day 32 of the experiment, was identical to the preexposure phase except that a different pair of novel objects was placed into the arena. The objects were a small plastic pipe end joint (approximately 69.0 mm in dia. 48.0 mm in height open in the center with a wall thickness of 6.0 mm) and a wooden pedestal (the base measuring 10.0 × 13.5 × 2.5 cm and the crown made of two pieces each measuring 9.0 × 10.0 × 3.5 cm laid flat on the base) in the right and left zones, respectively. Behavior during the session was video taped and scored according to the protocol described below.

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Behavioral scoring. The general procedures for scoring the animals' exploration of the objects were modelled after those of Widman and Rosellini (58). This behavioral protocol defines six categories of possible object exploration: low-risk behavior, paw contact, climb/enter the object, mouth contact, accidental contact, and object "behavior." Within each of these behavioral categories are a number of specific object-directed behaviors. The behaviors within each category are arranged heirarchically and are mutually exclusive within, but not across, categories for each second of object exploration. However, any combination of categories can occur during any given second of exploration. For example, an animal may be scored as sniffing at the object as well as leaning on it during a second of observation since these behaviors belong to different categories. However, the animal cannot be scored as pawing the object and leaning on it during the same second of observation since both these behaviors belong to the same category. The behavioral categories, the specific behaviors, and their definitions were those used previously in our laboratory (42,58), adapted from Renner (32). This scoring protocol allows for the subsequent categorization of the behaviors which have occurred into two higher order categor i e s - d i v e r s e and nondiverse behaviors. This dimension is based on the notion that certain behaviors expose the animal to a higher level of risk than others should the object or the situation contain unexpected characteristics [(32), p. 96], these behaviors which entail increased risk are labeled as diverse. For example, putting weight on the object is categorized as diverse while sniffing at the object is categorized as nondiverse. This distinction between diverse and nondiverse behaviors has been made previously with this object-exploration test (32, 34, 42, 58). The object-exploration test provides two sets of measures of the exploration of objects: quantitative and qualitative [see (42,58)]. The quantitative measures are indexed by: 1) total amount of contact with the object, 2) latency to contact the object. 3~ number of bouts of exploration with the object, and 4) average bout length. The qualitative measures of object exploration are assessed by three measures: the total number of diverse behaviors utilized by the animal and the diversity indices (the bouts diversity index and the seconds diversity index). The bout diversity index is defined as the number of bouts containing a diverse behavior divided by the total number of bouts. The seconds diversity index is defined as the number of seconds containing a diverse behavior divided by the total number of seconds of contact with the object. On Day 33 of the experiment, all animals were returned to the daily regimen of environmental exposure. Animals were also placed on a food-deprivation schedule and reduced to 80% of their free feeding weight over a 5 day period.

W1DMAN, ABRAHAMSEN AND R()SELI,INt

response, on a RI-10 sec schedule, For the three day~ ~q :icqtli sition (Days 39-41), as well as the one day of baseline (Da 3 42), animals were placed into the operan! chambers aud a!towed to respond for food on a R1-30 schedule. Stress exposure. On Day 43 of the experiment the envuonmental exposure was discontinued and animals were exposed m stressors. There were three stress exposure groups, one group which received escapable shock (ES), one group which received yoked shock (YS), and a final group which received no shock (NS). These stress groups were factorially combined with the environmental exposure groups yielding groups EC-ES (n :-8~. EC-YS ( n = 8 ) , EC-NS ( n = 7 ) , SC-ES (n=7), SC-YS (n 8!, and SC-NS (n= 8). Shock exposure for the ES and YS groups consisted of 80 trials of 0.9 mA intensity unsignalled scrambled footshock. For the ES groups, the initial 15 trials required a single barpress to terminate shock (FR-I), with the remaining trials requiring two responses (FR-2). If an animal failed t~ meet the ratio criterion, shock was terminated 30 s from onset. irials were administered on a Random Time 90-s schedule, with the ITI values equiprobable within a range of 60 !20 s. The animals in the YS condition were exposed to yoked shock such that they received the same pattern and duration of shock as animals in the corresponding ES groups, but were unable to terminate the shock with the emission of a response. These are stress parameters which are effective in producing reliable "'learnedhelplessness" phenomena in our laboratory (38,40). Animals in the NS groups were placed in the shock chambers for an equivalent period of time but were not exposed to electric shock. The measure of interest from this phase is the latency to perform an escape response on each trail for the ES groups, It should be noted that for this phase, animals were transported to the experimental chambers in their home cages. During this phase, one SC-YS animal was removed from the study due to apparatus failure. On Day 44, animals were given one dax of recovery in their home cage. Appetitive recovery and appetitive noncontingent t~'sl, On Days 45 and 46, animals were placed into the operant chambers and allowed to respond on a RI-30 schedule for tk)od. For the next 4 sessions, Days 47-50, animals were placed into the operant chambers for 30 rain sessions. Food was delivered on a RT-30 schedule such that the delivery of food was not contingent on the animals responding. Food was, however, still available on the average every 30 s. as in previous appetitive phases,

Statistics The data were analyzed using a repeated measures analysis of variance technique (ANOVA) with the significance level set at p<0.05 for all analyses.

Appetitive-Operant Test The appetitive-operant test consisted of six phases: 1) Preacquisition, 2) acquisition, 3) baseline, 4) stress exposure, 5) appetitive recovery, and 6) appetitive noncontingent test. All phases of the appetitive test sessions were 30 min in duration and the dependent measure of interest was the number of responses emitted by the animal with the exception of the stress exposure phase. Preacquisition, acquisition, and baseline. On the evening of Day 37 all animals were exposed to 10 45 mg Noyes pellets (Formula A) in the home cage. The following day, Day 38, 10 pellets were delivered to the food cups in operant chambers, animals were placed into the chambers and allowed 2 min to consume the pellets. Following this period, a session was begun in which one pellet was scheduled to be delivered, contingent on a

RESULTS

Object-Exploration Test The data from this segment of the experiment were generally analyzed using ANOVA with Environment (EC or SC) as the between-subject factor and Manipulability of the object as a within-subject factor. The object-exploration test provides two measures of novel-object exploration, the quantity and the quality of object exploration. The quantitative measures are indexed by l) tile seconds of contact, 2) latency to contact the object, 3) the number of bouts of contact with the object, and 4) average bout length. Figure l displays the quantitative data. As can been seen in panel A of Fig. 1, it appears that both groups spent more time in contact with the nonmanipulable ob-

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FIG. 1. Quantitative measures of object exploration for the EC and SC animals on both the MAN and NON objects. (A) Mean seconds of total object contact. (B) Mean latency to initiate first bout of interaction measured in seconds. (C) Mean number of bouts. (D) Mean bout length measured in seconds. (EC =enriched condition, SC =social condition, MAN = manipulable object, NON = nonmanipulable object.)

ject than with the manipulable object. It also appears that the amount of time in contact with each object is dependent upon previous environmental history; the enriched group spent less time in contact with the manipulable object than the social group while the enriched group spent more time with the nonmanipulable object. Analyses showed both a significant main effect of Manipulability, F(1,44)=30.84, and an interaction of Environment and Manipulability, F(1,44)= 10.02. Separate analyses revealed this interaction to stem from the enriched group spending significantly more time with the nonmanipulable object, F(1,44) = 6.51. However, the two groups did not differ in the amount of time spent with the manipulable object, F(1,44)= 2.57. Panel B of Fig. 1 shows the latency to contact the object for both the manipulable and nonmanipulable object. As can been seen in the panel, for both object types the enriched group had shorter latencies than the social group. There also appears to be an overall effect of manipulability such that there were longer latencies to contact the manipulable object than the nonmanipulable object. ANOVA confh'med the first of these observations, revealing a significant main effect of Manipulability, F(1,44)= 7.55. However, there was no main effect of Environment, F(1,44) = 2.70, nor an interaction of Manipulability and Environment, F(1,44) = 2.08. The number of bouts with each type of object for each group is displayed in panel C of Fig. 1. As can clearly be seen, there was no effect of Environment, F(1,44)=0.56, nor an interaction of Environment and Manipulability, F(1,44)=0.05. There was,

FIG. 2. Qualitative measures of object exploration for EC and SC animals on both the MAN and NON objects. (A) Mean total number of diverse behaviors. (B) Mean seconds diversity index. (C) Mean bouts diversity index. (EC = enriched condition, SC = social condition, MAN = manipulable object, NON = nonmanipulable object.)

however, a significant main effect of Manipulability, F(1,44)= 117.81, indicating that there was a greater number of bouts with the nonmanipulable object, regardless of previous environmental exposure, than the manipulable object. The final panel of Fig. 1, panel D, displays the average bout length. In this case, there was a significant interaction between Environment and Manipulability, F(1,44)= 17.64, but neither a main effect of Environment, F(1,44) = 0.98, nor Manipulability, F(1,44)=0.57. Separate analyses revealed that the interaction stemmed from the two groups not differing in average bout length with the manipulable object, F(1,44)=2.60, but the enriched group displaying a greater average bout length with the nonmanipulable object, F(1,44)= 14.79. The qualitative measures are indexed by the total number of diverse behaviors and the bouts and seconds diversity indices. The data for each of these is presented in Fig. 2. Panel A of Fig. 2 presents the total number of diverse behaviors. As can be seen in the figure, the two groups do not appear to have utilized a different number of diverse behaviors while exploring the manipulable objects, but the enriched group did appear to utilize more diverse behaviors than the social group while exploring the nonmanipulable object. ANOVA supported these impressions. It revealed a significant main effect of Environment, F(1,44)= 9.89, and a significant interaction of Environment and Manipulability, F(1,44) = 14.83. The main effect of environment stemmed from the enriched group displaying greater numbers of diverse behaviors than the social group (EC mean=90.46; SC mean= 43.35). Separate analyses on each object type revealed the interaction to stem from the two groups utilizing significantly different

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numbers of diverse behaviors on the nonmanipulable object, F(1,44)=27.63, while not differing on the manipulable object. F( 1,44) = 0.01. A similar pattern of results was observed in the seconds diversity index, depicted in panel B of Fig. 2. ANOVA revealed significant main effects of both Environment, F(1,44)= 23.00. and Manipulability, F(1,44) = 60.41, and a significant interaction of Environment and Manipulability, F(1,44) = 19.90. In the case of the main effect of Environment, the effect stemmed from the enriched animals having a greater mean seconds diversity index than the social group (EC mean=0.589, SC mean =0.458). The main effect of Manipulability resulted from there being a greater mean seconds diversity index on the manipulable object than that on the nonmanipulable object (MAN mean = 0.614, NON mean = 0.433). Separate analyses on each of the object types revealed that the interaction of Environment and Manipulability resulted from the two groups differing on the nonmanipulable object, F(1,44)=43.35, and not differing on the manipulable object, F( 1,44) = 0.574. Data for each group on the bouts diversity index is presented in panel C of Fig. 2. It appears from the graph that these data also followed a similar pattern of significance as the two previous measures of the quality of object exploration, no difference between the two groups on the manipulable object, but the EC group displaying a greater index than the SC group on the nonmanipulable. However, only the main effect of Manipulability reached an acceptable level of significance, F(1,44)=38.81. This was due to the greater average bout diversity index on the manipulable object (MAN mean=0.613, NON mean=0.453). Importantly, however, the Environment by Manipulability interaction attained a marginal level of significance, F(1,44)= 3.71, p = 0 . 0 6 1 . Due to the impressions of the figure and the potential theoretical importance of each of the three qualitative measures displaying similar results, we chose to examine the source of this marginal interaction. Separate analyses showed that the two groups did not differ on their average bout diversity indices on the manipulable object, F(1,44)=0.04, but did differ significantly on the nonmanipulable object, F(1,44)= 5.23.

Appetitive-Operant Test Preacquisition, acquisition, and baseline. ANOVA, conducted on the number of responses emitted during the preacquisition, acquisition and baseline phases, as a function of Environment (EC and SC) and Blocks of 5 min (6) and, where appropriate, Days (3), revealed no main effects of Environment, nor any interactions with Environment and the other factors (all Fs<2.12). There was, however, a significant effect of Blocks on the preacquisition day, F(5,205)=7.56. An examination of the means indicated that the number of responses increased across blocks for all groups. There was also a significant interaction between Days and Blocks on the three days of acquisition, F(10,440)=4.83. The pattern of means was similar to that of the preacquisition day, with the means increasing across blocks and days. Similarly, there was also a significant effect of Blocks on the baseline day, F(5,200)=5.82, which followed the same pattern of increasing means across the repeated measurements as observed on the previous phases. This pattern of results indicates that all of the groups acquired the appetitive response and that this acquisition was statistically equivalent across the different environmental conditions. Stress exposure. The pattern of means for both the EC-ES and SC-ES groups from the stress exposure phase showed a steady decline in escape latencies, indicating that both groups acquired the escape response. ANOVA conducted on the escape latencies on the final 13 blocks of 5 trials (the FR-2 trials) as a

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Blocks of 5 rnin FIG. 3. Mean number of responses during the appetitive-noncontingent test as a function of stress condition and 5 rain time blocks summed across days. (ES=escapable stress. YS=inescapable stress. NS=no stress.) function of Environment (EC and SC) and Blocks (13), showed a significant main effect of Blocks, F(12,156)=2.73, but no main effect of Environment and no interaction of Environment with Blocks, F(1,13) = 2.47 and F(12,156) = 1.19, respectively, indicating that the environmental manipulation did not differentially affect the acquisition of the escape response. Appetitive recovery. ANOVA conducted on the number of responses emitted on the two days of recovery as a function of Environment (EC and SC), Stress (ES, YS, and NS), Days (2), and Blocks of 5 min (5), revealed no main effects of Environment or Stress, nor any interactions of these two factors and other factors (all F s < l . 3 6 ) . The analysis did, however, reveal significant main effects of Days, F ( 1 , 4 0 ) = 2 4 . 9 3 , Blocks, F(5,40) = 38.07, and a significant interaction of Days and Blocks, F(5,200) =4.99, resulting from an increase in responding within and across Days. More importantly, this pattern indicates that the groups entered the subsequent noncontingent test with statistically equivalent levels of responding. Appetitive-noncontingent test. ANOVA conducted on the number of responses during the appetitive-noncontingent test, as a function of Environment (EC and SC), Stress (ES, YS, and NS), Blocks of 5 min (6) and Days (4), revealed no main effects of Environment, Stress, nor an interaction of Environment and Stress (all Fs< 1.0). The analysis did, however, reveal a significant Stress by Blocks interaction, F(10,200)= 3.03. This interaction is shown in Fig. 3. As can be seen in this figure, the YS group emitted fewer responses during each block of the test than either the ES or NS groups, which appeared to be similar to each other. Follow-up analyses revealed significant effects of stress at each block (all Fs>4.39). A set of post hoc Newman-Keuls multiple comparisons revealed the YS groups to be significantly different from both the ES and NS groups and the ES and NS groups to not be significantly different at blocks 1, 2, 3, and 5. On both blocks 4 and 6, the analysis showed the YS and NS groups not to differ, while showing the YS and ES groups and the ES and NS groups to differ from one another. DISCUSSION

There are three important findings in the present study. The first is that the limited environmental-exposure regimen was successful in differentially affecting the behavior of the enriched animals relative to the socially exposed control animals on the object-exploration test. The second is that environmental enrichment did not significantly affect the outcome of any of the oper-

RESTRICTED ENRICHMENT AND STRESS

ant tasks (the appetitive-operant acquisition, the acquisition of the escape response or the appetitive-noncontingent task). The third is that the environmental enrichment and the stress manipulations did not appear to interact with each other on the appetitive-noncontingent task. We will focus on each of these points in turn. The results of the object-exploration test indicate that limited exposure to environmental enrichment can produce effects similar to those using less restricted enrichment procedures. This conclusion is supported by the high degree of concordance between the results of the present study and those of Renner and Rosenzweig (34) which also compared the effects of environmental enrichment to those of social exposure. This concordance is observed across both the quantitative and qualitative measures. Both the present study and that of Renner and Rosenzweig (34) found significant interactions between the environmental enrichment manipulation and object manipulability on the total interaction time (seconds of contact with the object) as well as a main effect of manipulability on this measure. This main effect in both studies stemmed from a greater amount of time in contact with the nonmanipulable object than with the manipulable object. The present study and that of Renner and Rosenzweig (34) also did not observe significant effects of environmental enrichment on the number of bouts with the objects. These studies do, however, report significant main effects of manipulability on the number of bouts resulting from the nonmanipulable object eliciting a greater number of bouts. The present study extends the findings of Renner and Rosenzweig (34) in that environmental enrichment did not affect the average latency to contact the object and the average bout length. These results are similar to those reported by Widman and Rosellini (58), which compared enriched to impoverished animals. Examination of the qualitative measures reveals that in cases where environmental enrichment effects were observed both studies found a greater utilization of diverse behaviors by the enriched group than the socially exposed group. The concordance of the results of Renner and Rosenzweig (34), the present study and those of Widman & Rosellini (58) strongly suggest that a daily restricted regimen of environmental exposure is capable of producing typical environmental enrichment effects which cannot be attributed to social exposure alone. A detailed examination of the results does reveal two differences in the specific patterns of the means between the present study and that of Renner and Rosenzweig (34). Before examining these differences, there are two factors which must be considered. The first is that there were no statistical comparisons made among the various experimental groups within each object type in the Renner and Rosenzweig (34) study. Thus, while we may be able to discuss the pattern of the means, statistical significance is unknown. The second factor is that the study of Renner and Rosenzweig (34) utilized a sampling window of 6 seconds, while the present study utilized a sampling window of 1 second. While this might be expected to create absolute differences between the two studies, the general pattern of results would not be expected to be affected. The first difference between the present study and that of Renner and Rosenzweig (34) is the total amount of time in contact with the objects. While the two studies report an interaction between environmental enrichment and object manipulability, the pattern of means within each object type for the two environmental groups is reversed. For the nonmanipulable object, the present study reports that the enriched group had a greater amount of time in contact with the object than the social group. Renner and Rosenzweig (34) report the opposite; the social group, rather than the enriched group, displayed a greater amount of time periods in contact with the nonmanipulable object than the enriched group. A reversal simi-

315

lar to the previous was also observed on the manipulable object. The present study reports that the social group displayed a greater amount of time in contact with the manipulable object, although this difference was not statistically significant. The Renner and Rosenzweig (34) study once again reports the opposite; the enriched group, rather than the social group, displayed a greater mean amount of time periods in contact with the manipulable object. The second difference is an apparent reversal of the interaction between the environment and manipulability factor on the diversity indices. This difference is consistent across both diversity indices with the observed pattern of means within each object type being opposite that of the other study. Rennet and Rosenzweig (34) found the enriched group to have greater diversity indices on the manipulable object and found no differences between the two groups on the nonmanipulable object. [The means for the enriched and social groups on the seconds diversity index for the nonmanipulable object in the Rennet and Rosenzweig (34) study do differ absolutely. However, due to the lack of statistical comparisons, it is not possible to determine if this difference is significant. The difference is smaller than the difference between the two groups on the manipulable object, however, which is consistent with the results of present study.] The present study found the opposite; the enriched group displayed greater diversity indices on the nonmanipulable object and did not differ on the manipulable object. One potential source for the difference involving the total amount of time in contact can be found by closely examining the relationship between the total amount of contact and the use of diverse behaviors during the exploration of objects. The resuits of both studies would indicate that objects which elicit a greater utilization of diverse behaviors from the enriched subjects also tend to elicit greater amounts of time in contact with that object, regardless of that object's manipulability. Whereas, objects which do not elicit the differential use of diverse behaviors between the enriched and social groups tend to elicit greater amounts of time in contact by the social group. While this observation may account for the difference on the time in contact, it does not explain the second difference involving the reversal of the object type which elicited the differential use of diverse behaviors. One potential account for the second difference is object characteristics other than manipulability which may have influenced the exploration of the objects. As noted above, to be consistent with the literature in this area (32, 34, 43, 58), we purposely chose two different objects, one of which was manipulable and one of which was not. However, to further maintain consistency with the existing literature, other characteristics were left free to vary. It may be that differences in these additional object characteristics, which were left free to vary in both studies, may aid in explaining the differences in the results of the diversity indices. Renner, Bennett and Pierre (33) report a series of experiments which manipulated single-object characteristics while holding all others constant. In the first experiment, Renner et al. (33) found that altering the "topographical complexity" of the object could affect the diversity index such that the topographically complex object elicited more diverse behaviors during exploratory bouts. In the second experiment, Renner et al. (33) found that an object made nonmanipulable elicited more diverse bouts than an identical object made manipulable. While this series of experiments suggests that varying single-object characteristics does greatly influence the use of diverse behaviors, it does not specify which characteristics or which set of objects could have caused this difference on the diversity indices between the present study and that of Renner and Rosenzweig (34). However, because of the consistent nature of the

31(',

reversal across both indices, it certainly appears plausible that these other object characteristics played a role in producing this reversal. This analysis of the impact of various object characteristics emphasizes the importance of experimental control over as many object characteristics as possible when examining the influence of specific characteristics such as the series reported by Renner et al. (33). Given that the environmental-enrichment procedures were effective in producing typical environmental-enrichment effects, it is interesting to note that environmental enrichment did not affect either the acquisition of the appetitive-operant response or the acquisition of the escape response. These outcomes were anticipated and are consistent with the literature on the effects of environmental enrichment on the simple acquisition of operant responses, which typically has not found effects on basic response-acquisition processes [e.g., (5, 8, 26, 28)]. As expected, the Stress manipulation did affect the outcome of the appetitive-noncontingent test; the results essentially replicate those typically observed in our laboratory [e.g., (7, 38, 54)]. The uncontrollably stressed groups, regardless of their environmental history, responded less than either the controllably stressed or nonstressed groups when food was delivered noncontingently but at the same rate as during appetitive training. The lack of environmental-enrichment effects on the appetitive-noncontingent test was more surprising. As noted in the introduction, we had specifically chosen an appetitive-noncontingent test because of its resemblance to the DRL schedule employed by Ough et al. (28), which successfully demonstrated environmental-enrichment effects. However, the outcome of our appetitive-noncontingent test showed no evidence of an effect of environmental enrichment, either in the form of a main effect or an interaction with the stress manipulation. There are three possibilities which might account for the lack of a main effect of environmental enrichment in the present experiment and the presence of such an effect in that of Ough et al. (28). The first possibility involves a difference in the environmental-enrichment procedure. Ough et al. (28) used a 24-hour-per-day exposure regimen while the present study used a restricted-exposure regimen. While the results of the object-exploration test suggests that the restricted procedure was capable of producing typical environmental-enrichment effects, it is possible that restricted daily exposure is only capable of producing typical effects on the object-exploration test and not on other tasks. There are, however, reports of restricted-exposure regimens producing effects similar to the 24-hour-exposure regimen using other measures, both biochemical and behavioral (10, 47, 59). The second possible explanation for the difference between the results of the present study and that of Ough et al. (28) is based on a difference between the schedules employed. In the DRL of Ough et al. (28), although the animal is required to respond at a rate lower than that which was previously reinforced, there remains a positive contingency between the response and the outcome. The contingency between the response and the delivery of food on the appetitive-noncontingent test task was, however, set to zero. This would suggest that environmental-enrichment effects may only be detected on operant schedules which retain a nonzero response-reinforcer contingency. The third possible explanation is that the differential outcome is due to a difference in experimental design. Ough et al. (28) compared enriched and impoverished animals. The present experiment compared enriched animals to animals which were exposed to a social environment. This difference raises the possibility that the findings of Ough et al. (28) are due not to an effect of environmental enrichment but instead are due to an effect of impoverishment, as Ough et al. (28) themselves proposed. In the introduction we proposed a theoretical basis for antici-

WIDMAN. ABRAHAMSEN AN][) R()SEI.LIN~

pating an interaction between environmental enrichmenl ant1 uncontrollable stress. This position was based on the Renner and Rosenzweig (35) proposal that environmental enrichment generally improves the organism's future learning ability. Based or~ this proposition, it was expected that the enriched animals would be more susceptible to the effects of uncontrollable stress Specifically, the position anticipated that the EC-YS arfimals ,aould have suppressed responding to a greater extent on the appetitive.noncontingent test than any other group. This was ,.learly not the case. The results of the appetitive-noncontingent test did not reveal an interaction of environmental enrichment and uncontrollable stress. There are three speculative accounts which could explain this lack of an interaction. The first is simply that. while both manipulations could affect learning in a general manner, they may do so via different mechanisms which could preclude their interaction. While this is certainly possible, it would appear to be the least interesting explanation of the data The second is that the appetitive-noncontingent test was not a sufficiently complex learning task to detect environmental enrichment effects. Were this the case, the present findings would be consistent with Renner and Rosenzweig's (35) notion that the effects of environmental enrichment may only be expressed on more " c o m p l e x " learning tasks. As discussed above, there were differences between the procedures of Ough et al. (281 and those of the present study, specifically the schedules of reinforcement during testing, which could have lead to a difference in the complexity of the two procedures. While this is a possible interpretation of the present data, task "complexity" is difficult to determine without resorting to post hoc analysis and potential circular logic. The third account is that environmental enrichment may not affect learning in a general sense, but instead may affecl only a specific form of learning. It may be the case that environmental enrichment affects only the acquisition of spatial inlbrmation. but does not affect the acquisition of response-reinforcer relations or information regarding the temporal distribution of events. The abundance of data indicating an enriched organisms' enhanced learning on maze tasks and the scarcity and ambiguity of data indicating environmental enrichment effects in operant and Pavlovian situations is certainly suggestive of this account. Viewed in this manner, the lack of an effect of environmental enrichment is not surprising given the nonspatial nature of the appetitive-noncontingent test. While each of these three accounts appears plausible, the present study cannot distinguish between them. They do, however, indicate future directions for investigation. For example, to test the third account, it would be necessary to utilize a behavioral test which is spatial in nature but is sensitive to both the effects of environmental enrichment and those of uncontrollable stress. In summary, the present study provides three contributions to the understanding of the effects of environmental enrichment. First, it extends a previous finding of the effectiveness of limited daily exposure to environmental enrichment (58), utilizing a social-exposure control procedure. Secondly, it provides a further example of environmental enrichment's failure to affect basic instrumental conditioning (5, 8, 26, 28). Importantly, it does so in animals which have demonstrated an environmental-enrichment effect on a previous behavioral measure. The third contribution is the demonstration of the lack of an interaction of environmental enrichment and a manipulation known to affect a wide variety of learning tasks, uncontrollable stress under conditions where the effectiveness of environmental enrichment and uncontrollable stress is demonstrated within the same animals. Therefore, the absence of an interaction between the two cannot simply be attributed to a failure of either manipulation.

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ACKNOWLEDGEMENT The authors would like to thank Anne M. Bassuk for her assistance in the analysis of the videotape.

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