Associative Processes in Differentially Reared Rhesus Monkeys (Macaca mulatta): Blocking ALAN J. BEAUCHAMP Department of Psychology Northern Michigan University Marquette, Michigan

JOHN P. GLUCK H. EDWARD FOUTY Department of Psychology University of New Mexico Albuquerque, New Mexico

MARK H. LEWIS Brain and Development Research Center and Department of Psychiatry University of North Carolina Chapel Hill, North Carolina

Nine isolate and 6 socially reared adult rhesus monkeys were examined in a standard blocking procedure. A tone was paired with a startle stimulus (US) during Phase 1. A tone-light compound CS was paired with a US during Phase 2. In Phase 3, the light was presented alone to test for blocking. Results showed that learning about the light was blocked in social controls, but not in isolates. These data suggest isolates processed information atypically, in that they developed an association to a redundant cue. A second group of isolates (n = 3) underwent the identical procedures. However, conditioned reactions to the tone were extinguished before testing. Test responding was significantly reduced in this group, that is, blocking was obtained. These data suggest the within-compound association developed during Phase 2 mediated the isolate blocking deficit. Together, these findings imply long-term intellectual consequences of early social impoverishment. Such deficits may be mediated by alterations in central dopamine systems. ~

Reprint requests should be sent to Alan J. Beauchamp, Department of Psychology, Northern Michigan University, Marquette, MI 49855. Received for publication 8 May 1989 Revised for publication 11 June 1990, 21 December 1990 Accepted at Wiley 28 January 1991 Developmental Psychobioiogy 24(3): 175-189 (1991) D 1991 by John Wiley & Sons, Inc.

CCC 00 12-1630/91/030175- 15$04.00

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The relationship between early rearing experiences and intellectual development has important social implications, and underlies contemporary controversies regarding the unique contributions of genetics, maturation, and learning (Holson & Sackett, 1984; Kamin, 1974). Given the critical importance of this issue, considerable attention has been devoted to testing the hypothesis that impoverished early experience results in deficient cognitive development. A valuable paradigm for examining the effects of early experience has involved depriving infant nonhuman primates of access to mother and peers (Harlow, 1959). In the 1960s and 1970s, several groups reared rhesus monkeys under such conditions for periods ranging between the first 3 and 12 months of life. While the effects of this developmental insult on emotional and social functioning were profound, deficits in intellectual functioning were not as easily demonstrated. Indeed, several investigations showed that rhesus monkeys reared in social isolation performed adequately in a wide range of learning procedures. For example, learning performance in the delayed response task, the two-choice discrimination task (Harlow, Schiltz, & Harlow, 1969), the avoidance procedure (Rowland, 1964), and continuous reinforcement operant conditioning (Gluck, 1970) did not appear to be altered. Atypical performance was, however, found on tasks such as extinction (Gluck & Sackett, 1976), the conditioned emotional response procedure (Frank, Gluck, & Strongin, 1977), and the oddity task (Gluck, Harlow, & Schiltz, 1973). Although some studies found a relationship between early social impoverishment and deficits in learning performance, how such deficits were mediated remained unclear. Specifically, isolate learning deficits could have been the product of nonintellectual factors, such as hyperreactivity or distractibility. Such potential artifacts have been documented as being part of the “isolate syndrome,” and clearly confound the assessment of intellectual competence and cognitive task performance. A recent study from our laboratory attempted to address these issues (Beauchamp & Gluck, 1988). The performance of adult isolate reared monkeys was examined in a sensory preconditioning task. Sensory Preconditioning (SPC) is a three-phase procedure designed to assess the development of an interstimulus association. In Phase 1, preconditioning, two neutral stimuli (S,-S,) are contiguously paired. In Phase 2, a specific response is conditioned to S,. In Phase 3, a transfer test is run on S,. Sensory preconditioning is demonstrated in experimental subjects when test responding to S, is greater than that of appropriate controls. This procedure offered the opportunity to minimize performance requirements, and thereby permitted a more valid examination of learning competence in isolates. Surprisingly, under the conditions employed isolates showed stronger and more durable SPC than socially reared monkeys. Isolates appeared to develop an unusually strong albeit irrelevant S,-S, association during Phase 1, which mediated the atypically high levels of SPC observed. We interpreted this result to reflect a habituation deficit in isolates. That is, the isolate performance difference found in this experiment could have resulted from an inability to habituate to preconditioning stimuli (i.e., a performance deficit), as opposed to an intellectual difference per se. Specifically, we examined attention, defined as visual/postural orientation to relevant stimulus events, and found that social controls did not attend as diligently to preconditioning stimuli when compared to isolates. Consequently, an attentional explanation could suffice to explain the findings. To circumvent a

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similar interpretive problem, isolate performance in the blocking procedure was examined. The blocking procedure (Kamin, 1968) also consists of three phases. In Phase 1, a neutral stimulus (e.g., a tone) is paired with an US until it reliably elicits a conditioned response. In Phase 2, a second neutral stimulus (e.g., a light) is paired in compound with the tone and followed by the US. In Phase 3, the light is presented alone to assess conditioning as a result of Phase 2 compound training. Blocking is said to have occurred if subjects show significantly less responding to the light when compared to proper controls. Kamin (1968,1969) assumed that unpredicted events engage learning processes that set up an association between the CS and US. Predicted events, however, do not. In our example, because Phase 2 reinforcement is already predicted by the tone-US association acquired previously, the added light element is redundant. Therefore, the processes required to develop a strong association between the light and the US are not engaged. Kamin’s (1969) explanation of blocking, essentially hinging upon whether the occurrence of the US is surprising or expected, has received strong support from the literature (Dickinson, Hall, & Mackintosh, 1976; Randich & Ross, 1984; Stickney & Donahoe, 1983). The blocking procedure is particularly well-suited to examine the hypothesis that isolates process redundant information. Further, with this procedure the interpretive problem that arose in the study of SPC can be circumvented. Specifically, in the blocking procedure the critical stimuli are presented in compound, and can be arranged so they are presented from approximately the same physical location. Because of Phase 1 conditioning, one element of the compound predicts the upcoming occurrence of the US. Since both elements of the compound stimulus will come from about the same physical location, it is likely that all monkeys will attend to (i.e., orient towards) these presentations. This should equalize the degree of attention directed to relevant stimuli and present a better opportunity to assess information processing between groups. Lastly, the learning situation is simple and can be arranged to control performance factors. It was concluded that this procedure would permit a relatively unconfounded examination of information processing in isolates.

Subjects Fifteen rhesus monkeys (Macaca mulatta) were tested (9 isolates, 6 social controls). All animals had participated in previous tests of learning and social behavior. These experiences should not affect the outcome of the present investigation since the learning tests involved discrimination training in the Wisconsin General Test Apparatus and used strictly three-dimensional objects. Social functioning was examined through naturalistic observation of brief multianimal encounters. All monkeys were housed in individual 2.54 cm stainless steel mesh cages (76 cm x 105 cm x 76 cm). Between 13 and 20 individually housed isolate and socially reared animals were kept together in separate colony rooms, allowing for visual, olfactory, and auditory exposure to conspecifics. The temperature in the

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colony rooms was maintained at approximately 70°F, 60% humidity. A 12-hr lightdark cycle was maintained. Isolate reared subjects (n = 9) were randomly selected from a population of 13. The specific details regarding the rearing of these animals has been presented elsewhere (Sackett, 1968), and will be reviewed only briefly here. Infants were removed from their mothers shortly after birth and placed in individual isolation chambers. The 0.6 m x 0.6 m x 0.6 m stainless steel chambers constituted the housing for these monkeys for the next 9 months of life. Initially, infants experienced limited handling to facilitate feeding (i.e., the first 20 days in the isolation chamber). After this, no further handling occurred. No attempts were made to deprive monkeys of sensory stimulation, and light was provided in a typical 12-hr cycle. Monkeys were placed into standard laboratory housing when they reached the age of 9 months. The mean age of the isolates at the start of the experiment was 20.3 years (SD = .96, 18-21 years). The isolate reared group consisted of 6 females and 3 males. Social controls ( n = 6 ) were randomly selected from a population of 17. These monkeys were reared with peer and maternal contact for the first 9 months of life, and then transferred to standard laboratory housing. The mean age was 19.2 years (SD = .44, 17-20 years). The socially reared group was comprised of 4 females and 2 males.

Apparatus Stimuli used in the study were of three types. Stimulus “A” was a 75 Hz tone (70 db) generated by a Grason-StadlerE6002A audio oscillator. Stimulus “X” was produced by two clear GE 1252 light bulbs. White noise (100 db), generated by the above mentioned audio oscillators, served as the US. Stimuli were controlled by electromechanical programming equipment located in an adjoining room. All procedures were carried out in a 60 cm x 60 cm x 60 cm Leigh Valley operant box. within a 91 cm x 91 cm x 1.9 m soundproof chamber. The tone and white noise were presented through a speaker 9 cm in diameter, centered in the front wall 56 cm from the floor of the operant chamber. The two light bulbs were located 15 cm from each side of the speaker 58 cm from the floor. Low level illumination was provided to the operant chamber with a 10 watt light. A JVC video camera and component audiovisual recording system were used for behavioral observation.

Procedure Subjects were randomly assigned to five groups ( n = 3) according to rearing history and condition. Socially reared monkeys were assigned to Groups SC and SE. Isolates were assigned to Groups IC, IE, and HRC. Groups SE and IE received the blocking treatment; Groups SC and IC served as blocking controls; Group HRC consisted of three isolates, and served as a hyperreactivity control group. As there was no reason to suspect hyperreactivity in socially reared monkeys, this factor was assessed only in isolates. Before beginning the procedure, all monkeys were habituated to the apparatus for five 1-hr daily sessions. Following habituation, subjects assigned to Groups SE, IE, and HRC underwent Phase 1 conditioning as follows. The tone was

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Table 1 Experimental Protocol f o r the Blocking Study Group

Phase 1

Phase 2

Phase 3 ~

IE IC HRC SE

sc

A+ A/+ A+ A+ A/+

Ax+ Ax+ A+ AX +

Ax+

~~

X

X X X X

presented for 10 sec and followed immediately at offset by a 0.5 sec presentation of the US. The US reliably elicited a startle reaction. Fifteen tone-US presentations were given over 2 consecutive days (i.e., 30 total pairings). Trials were separated by an average of 2 min. During Phase 1, blocking controls (i.e., Groups SC and IC) were given random presentations of the tone and US stimuli in a noncontiguous fashion. Specifically, for 2 consecutive days blocking controls received 15 random presentations of the tone (10 sec) and US (0.5 sec). Stimulus presentations were separated by an average of 2 min. Hence, all subjects were exposed equally to Phase 1 stimuli. The startle response, scored by trained observers, was identified through examination of behavioral topography. Operationally, the startle reaction consisted of either a rapid retreat (i.e., quickly moving away from the stimulus source), a quick postural hunch (e.g., ducking head down), or a brief shudder response. A conditioned startle reaction was scored if observed during CS onset but before US onset. Hyperreactive responses (Group HRC) were defined as startle to the onset of a novel, but neutral, stimulus. Although behaviors were disrupted by the US, there was no evidence of any prolonged distress. Monkeys were observed to return quickly to the activities they were engaged in before trial onset. In Phase 2, compound conditioning, subjects in Groups SE, SC, IE, and IC were given 15 tonehght-US pairings. The compound CS was presented for 10 sec and followed immediately by a 0.5 sec presentation of the white noise. Trials were separated by an average of 2 min. During Phase 2, orientation to compound stimulus presentations was also quantified using direct observations. Operationally, orientation was scored if the monkey showed direct visual and postural orientation to the compound CS for at least 5 sec of the 10 sec onset period. The Phase 2 treatment for Group HRC consisted of an additional 15 tone-US pairings on the identical temporal schedule. Immediately following Phase 2, Phase 3 testing was carried out. All monkeys were presented with 10 trials of the light alone to observe whether conditioned (Groups SC, SE, IC, and IE) or hyperreactive (Group HRC) startle reactions would be elicited. The US was not presented during Phase 3 testing. Light onset was for 10 sec and trials were separated by an average of 2 min. The overall design, outlined in standard blocking nomenclature (i.e., Tone = A, Light = X, US = +), is presented in Table 1. Interrater reliability for the scoring of CRs and orienting responses was evaluated with the Kappa statistic (K; Cohen, 1960). To establish interrater reliability, 1 subject from each group was randomly selected for review. Tapes were scored

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I&PHASE 1

Day 1

5

-- 4 a, L

(d

-3 (I)

C

2

(d

a1 5 0

1 2 3

PHASE 2

Day 2

1 2 3

1 2 3

Trial Blocks

Fig. 1 . Mean number of startle reactions within the blocking procedure to tone presentations as a function of treatment condition and rearing history in Phases 1 and 2 in rhesus monkeys.

by an independent observer uninformed as to rearing history and conditioning experience.

Results Interrater Reliability Results of the Kappa analysis indicated a highly significantdegree of agreement between independent raters for the identification of startle reactions and orienting responses ( K = 34, z = 10.6, p < .OOl).

Phase 1 The mean number of startle reactions to presentations of the tone were examined across all groups as a function of Trial Block and Training Session. These data are displayed in the first two panels of Figure 1. A 5 x 3 x 2 (Group X Trial Block x Training Session) Repeated Measures Analysis of Variance (RMANOVA) was employed. Specifically, the degree that monkeys in each of the five groups (i.e., SC, IC, SE, IE, and HRC) showed startle to tone presentations was averaged across five trials, yielding a total of six trial blocks (Le., three within each training session) summarizing the 30 Phase 1 training trials. The second within-subject factor, Training Session, looked for performance differences on Day 1 versus Day 2 training (ie., Training Trials 1-15 vs. 16-30) as a function of Group and Trial Block. The RM-ANOVA revealed a significant Session x Trial Block interaction, F(2,20) = 4.2, p = .03. As can be seen in Figure 1, during Day 1 training, when data were collapsed across groups the least amount of responding was observed during Trial Block 1 while elevated levels of response were observed across Trial

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Blocks 2 and 3. On Day 2 training, the reverse was true; that is, when collapsed across groups, more responding was observed on Trial Blocks 1 and 2 relative to Trial Block 3. This later finding is easily understood with an examination of Figure 1. It is apparent that during the third trial block of Day 2 training, Groups SC and IC show a dramatic decline in responding to tone presentations relative to Groups IE, SE, and HRC. The RM-ANOVA also revealed a Group x Trial Block interaction, F(8,20) = 3.7, p = .008. This indicates that when data were collapsed across training sessions, all groups showed similar levels of responding during Trial Block 1. However, groups undergoing conditioning (IE, SE, and HRC) showed elevated levels of responding relative to groups receiving noncontiguous random presentations of the tone and US (i.e., Groups IC and SC) across Trial Blocks 2 and 3. Taken together, both interactions suggest that monkeys receiving paired presentations of the tone and US developed a strong classically conditioned association by the conclusion of Phase 1 training, while monkeys receiving random noncontiguous presentations of the tone and US did not (see Fig. 1, Phase 1, Day 2). A post-hoc contrast between the Trial Block 3, Day 2 performance of Groups IE, SE, and HRC versus Groups SC and IC solidifies this interpretation, F(1,13) = 33.4, p < ,001.

Phase 2 Compound Conditioning The mean number of CRs observed to presentations of the tone-light compound in Groups IE, IC, SE, and SC were examined. A 4 x 3 RM-ANOVA (Group x Trial Block) revealed no significant differences. A post-hoc contrast between experimental and control groups at Trial Block 1 does, however, reveal that a significant difference existed at the beginning of Phase 2, F(1,lO) = 14.4, p = .003. As can be seen in Panel 3 of Figure 1, experimental groups (IE and SE) responded significantly more often during Trial Block 1 of compound training when compared to control groups (SE and SC). No such difference was apparent by the end of Phase 2 conditioning, F(1,lO) = 1.8, p > .05. A second analysis was employed to examine the degree to which these subjects oriented to compound stimulus presentations. The one-way ANOVA found no between-group differences, F(3,8) = .04, p > .05. On average, subjects oriented to the tone-light compound on 12.1 of the 15 trials. Group I-IRC did not receive compound training, although they continued to show a high degree of conditioned startle to presentations of the tone CS during their continued Phase 2 training (i.e., M = 13.33).

Phase 3 Testing To detect blocking, the mean number of CRs observed to the 10 test presentations of the light were analyzed. Data from Groups SC, SE, IC, and IE were entered into a 2 x 2 ANOVA (Rearing History x Conditioning Experience). A highly significant interaction between Rearing History and Conditioning Experience was revealed, F(1,8) = 26.7,p < .001. This interaction resulted from the

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Isolates

Socials

T T

Experimental

Control

HRC

Treatment Condition Fig. 2. Mean number of startle reactions within the blocking procedure to presentations of the Phase 3 test stimulus as a function of treatment condition and rearing history in rhesus monkeys.

failure of Group IE to demonstrate blocking (see Figure 2). The planned contrast between Group SE and IE supports this contention, F(1,4) = 73.5, p < .001.

Group HRC If hyperreactivity was responsible for the data obtained in Group IE, the degree of responding to the light should not have been different between Groups IE and HRC. Although the use of Group HRC was planned prior to initiating the experiment, data were not collected along with that of blocking and blocking C O R ~ I - O ~ Consequently, S. the contrast of performance between Group HRC and Group IE was treated as a post-hoc comparison. To minimize the probability of a Type I error, the studentized q distribution was employed (McCall, 1990). This analysis indicated a significant between-group difference in responding to light presentations, F(1,4)= 42.7, p < .01; q(2,4) = 13.4, p < .01. As can be seen in Figure 2, Group HRC responded much less to these presentations when compared to Group IE.

Locus of the Blocking Deficit Figure 2 indicates that isolates failed to show the robust phenomenon of blocking, implying that isolates showed a tendency to process redundant information (i.e., the light element). However, results did not, at the associative level, reveal how this tendency resulted in the blocking deficit observed. It was reasoned that if isolates show a tendency to process the redundant stimulus in the blocking procedure, the outcome of this processing should manifest itself in one of two ways: (a) through the development of a direct association between the light element and the US, or (b) through the development of a within-compound association between the tone and light. Previous data would suggest the latter possibility, as isolates have been found to develop strong within-compound associations in similar

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IE

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A-EXT Treatment Condition

Fig. 3. Mean number of CRs within the blocking paradigm as a function of whether responding to the tone had been extinguished (A-Ext) or not (IE) prior to testing in isolate reared rhesus monkeys.

procedures (Beauchamp & Cluck, 1988). Thus, it was hypothesized that the withincompound association developed during Phase 2 mediated the blocking deficit seen in isolates. Unfortunately, there were not enough experimentally naive isolates to permit a full test of this hypothesis. The locus of the blocking deficit was, however, explored post-hoc using 3 experimentally naive isolates (Group A-Ext). The 3 isolates (Mage = 20 years, SD = 1.3 years; 2 males, 1 female) underwent the blocking treatment described previously for Group IE. However, responding to the tone was extinguished (Phase 2a) before testing. Specifically, 30 presentations of the tone alone were given between Phase 2 compound training and Phase 3 testing. Tone onset was for 10 sec and stimulus presentations were separated by an average of 2 min. If test responding to the light was still observed after this procedure, it would suggest responding was a function of the light-US association; that is, the within-compound association will have been extinguished. However, if a significant reduction of responding was obtained, it would suggest the withincompound association mediated the absence of blocking observed in isolates. After establishing that interrater reliability was acceptable (K = .7, z = 4.95, p < .01) and demonstrating that a significant degree of extinction had taken place during Phase 2a, F(5,lO) = 8.1, p < .001], test data from Group A-Ext were contrasted post-hoc with Group IE. To minimize the probability of a Type I error the studentized q distribution was again employed. Results indicated a significant reduction of test responding to the light, F(1,4) = 15.1, p < .01; q(2,4) = 5.49, p < .05]. Compared to Group IE, Group A-Ext showed far less conditioned startle to test presentations of the light (see Figure 3).

Discussion Results clearly support the hypothesis that early social deprivation permanently affects cognitive functioning in the rhesus monkey. The procedure em-

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ployed was successful in obtaining the blocking phenomenon in socially reared animals, yet unsuccessful when using isolate reared monkeys. This finding implies that isolates developed and maintained an association based upon redundant information. Data from Group A-Ext lends further support to this hypothesis, and refines our understanding of the isolate blocking deficit. That is, during Phase 2 isolates apparently developed a within-compound association involving the redundant stimulus, as when this association was extinguished prior to testing, blocking was restored. Consequently, we suggest the within-compound association mediated the isolate blocking deficit. It is unlikely the present findings are a result of some nonspecific factor influencing performance. Thus, isolates display information processing deficits. Nonspecific factors such as hyperreactivity, hyperarousal, extreme fearfulness, and the inability to habituate can interfere with learning performance regardless of procedure (see Holson & Sackett, 1984). The present investigation, however, tried to address these issues directly. First, all monkeys were habituated extensively to the testing environment before beginning the experiment. Second, the contribution of hyperreactivity was directly assessed. Third, attention to the tone-light compound was assessed directly. The inability to habituate to the testing context can clearly interfere with learning performance. Data from the first two phases suggest this was not a factor, as no terminal performance differences were found within treatment conditions between social controls and isolates during Phases 1 and 2. That is, by the end of Phase 1, Groups SE and IE showed equivalent levels of learning, and Groups SC and IC did not differ either. By the end of Phase 2, these groups showed equivalent levels of conditioned responding to the compound CS. This finding implies the habituation procedure used was successful. The data from Group HRC suggest hyperreactivity was not a factor in the isolate blocking deficit. Group HRC, after receiving an equivalent conditioning experience within the same testing context, showed little startle to the light when tested immediately following conditioning with the tone CS. Lastly, whether isolates attended more closely to toneilight presentations, either as a function of hyperarousal or the inability to habituate, was also examined directly. Early attention theory suggests that blocking occurs because subjects ignore the noninformative element added during compound training (Mackintosh, 1975; Sutherland & Mackintosh, 1971). This contention has received some support. For example, Kaye and Pierce (1984) report that in rodents, postural orientation to this element drops out very quickly (i.e., by Trial 2). The present study found no postural orientation differences to the compound tone-light stimulus among groups. In fact, all groups oriented quite frequently to these presentations (i.e., 80% of the time). This finding probably occurred because both stimuli were at about the same physical location. Nonetheless, if one follows the logic of attention theory, all animals should have developed equivalent withincompound and light-US associations and therefore, should have responded similarly to test presentations of the light. However, only isolates showed reliable startle responding to the light alone. Consequently, an explanation based upon attention (i.e., exposure to relevant stimulus events) will not suffice to explain the isolate blocking deficit. Together, these data suggest it is unlikely the present

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findings resulted from some nonspecific factor disrupting isolate learning performance. Given the above findings, we attempted to identify the associative locus of the blocking deficit post-hoc in a group of three isolates (Group A-Ext). Reasoning that if isolates show a tendency to process redundant stimuli in their environment, the outcome of this processing should manifest itself within the blocking procedure in one of two ways: (a) through the development of a direct association between the light element and the US, or (b) through the development of within-compound association between the tone and light. We attempted to identify which of these associations was responsible for the blocking deficit observed. Specifically, in Group A-Ext the within-compound and tone-US associations were extinguished prior to testing. This resulted in a significant attentuation of responding to test presentations of the light. These data implied the within-compound (tone-light) association largely mediated the absence of blocking in isolates. That is, in Group A-Ext the light-US association was not disturbed. Thus, if this association mediated responding to the light in Group IE, a similar pattern of performance should have been found in Group A-Ext. This, however, was not the case. Although the Group A-Ext data are relatively straightforward, our conclusion regarding the role of the within-compound association in the isolate blocking deficit must be viewed as tentative. Recall that not enough isolates were available to permit a well-controlled examination of the associative locus of the blocking deficit. Consequently, there are two plausible alternate accounts for the decline in responding observed in Group A-Ext. The first possibility involves forgetting. Group A-Ext received 30 extinction trials between compound training and testing. However, group IE was tested immediately following Phase 2 training. It is therefore possible that the additional time away from compound training could account for the reduction of responding seen in Group A-Ext (i.e., they forgot the X-USassociation). Although theoretically plausible, this appears unlikely for several reasons. First, in analogous investigations of unblocking in which the within-compound association was attenuated prior to testing and the above mentioned time confound was controlled for, results are consistent with ours (e.g., Rescorla, 1983; Rescorla & Colwill, 1983; Rescorla & Durlach, 1981). A second reason to doubt the forgetting hypothesis involves the time required for Phase 2a. On average, 62 min were required, and it is unlikely that rhesus monkeys would forget an association between a CS and US within this limited time interval. A third reason to suspect the forgetting hypothesis involves the pattern of learning and forgetting typically displayed by isolate reared monkeys. Characteristically, isolate monkeys develop associations somewhat slowly (Gluck, Harlow, & Schiltz, 1973; for a review see Holson & Sackett, 1984). However, once developed they are abnormally durable (Beauchamp & Gluck, 1988; Gluck & Sackett, 1976). Taken together, this implies that it is unlikely time alone could account for the decline in responding found in Group A-Ext. At any rate, we cannot present data to rule this possibility out directly. A second plausible account for the restoration of blocking observed in Group A-Ext involves the possibility that the extinction experience generalized to the light. There are two ways such a generalization effect could have occurred: First,

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it is possible that Phase 2a resulted in an attenuation of associations between contextual cues and the US (Weaver & Gordon, in press). Second, it is possible that the extinction of responding to the tone simply generalized cross-modally to the light. The reduction in responding observed in Group A-Ext may have reflected the attenuation of contextual associations with the US, as opposed to the degradation of the within-compound association. In other words, the reduced responding observed in Group A-Ext could have occurred because the US was no longer associated with the testing context. Recall, however, the data from Group HRC which demonstrated that when a novel stimulus was presented in compound with the contextual cues present during conditioning, very few startle reactions were observed. This suggests that contextual cues alone were insufficient to elicit the CR in isolates, and by extrapolation, implies that extinguishing contextual cues prior to testing Group A-Ext probably had little to do with the reduced level of responding observed. Such an interpretation supports the inference that the isolate blocking deficit was mediated through the within-compound association. With respect to the second possibility, extinction of responding of the tone simply generalized to the light, some insight might again be gained from an examination of data from Group HRC. In this group, conditioning did not generalize to a cross-modal stimulus when presented within the same testing context. This might suggest that little cross-modal generalization of extinction should be expected. Although such a cross-modal generalization of extinction effect (Kasprow, Schachtman, Cacheiro, & Miller, 1984) would not be expected, no data to rule out this possibility directly can be presented. At any rate, an interpretation of the data obtained from Group A-Ext must consider the possibility that the light stimulus paired in compound with unattenuated contextual cues could have been responsible for the isolate blocking deficit, or that some cross-modal generalization of the extinction experience may have occurred. In short, without adequate control for the influence of forgetting, contextual cues, and generalization, we can only tentatively conclude that the isolate blocking deficit was mediated by the withincompound association. To summarize, data from the present investigation suggest that isolates show significantly aberrant associative processes as a result of the early experience manipulation they underwent 20 years ago. They show a tendency to allocate attenuation to anything in their perceptual field, and process this information regardless of whether it is required. Data supporting this interpretation has been presented, in that isolates failed to show the robust phenomenon of blocking. They appear to have developed unusually strong associations to cues within the blocking procedure which are typically incapable of mediating a response to the test stimulus. We present preliminary data suggesting, but not demonstrating definitively, that the associative mechanism mediating this deficit was the within-compound association. As a consequence of this information processing difference, isolates are likely to have trouble rapidly discriminating relevant from irrelevant stimuli in their environment. This cognitive style would become particularly apparent under conditions of changing contingency. Patterns of isolate learning performance reported in past studies is congruent with this notion (Beauchamp & Gluck, 1988). The

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question, of course, is why isolates demonstrate the tendency to process redundant information. Mechanisms underlying the isolates’ maladaptive cognitive style have been explored in rodent models. For example, the neurotransmitter dopamine (DA) has been shown to mediate, at least in part, the blocking phenomenon. Crider, Solomon, and McMahon (1982) examined blocking in rats using a two-way shuttle avoidance task. They found that five daily doses of the DA agonist d-amphetamine (4 mg/kg) disrupted blocking. Furthermore, the blocking effect could be restored by administration of the DA antagonist haloperidol. Crider, Blockel, and Solomon (1986) also showed that rats undergoing a daily regimen of haloperidol (21 days at 0.5 mg/kg/day), a standard treatment for inducing DA receptor supersensitivity , did not exhibit blocking. Similar studies using the latent inhibition paradigm, which also involve examining the presence of associations to redundant stimuli, suggest that mesolimbic DA pathways play an important role. Injections of d-amphetamine into the nucleus accumbens, for example, disrupts latent inhibition (Solomon & Staton, 1982), as do treatments resulting in DA receptor supersensitivity . In humans, alterations in mesolimbic DA activity are thought to be an important feature of the pathophysiology of schizophrenia. Schizophrenic subjects fail to exhibit pre-pulse inhibition or latent inhibition (Baruch, Hemsley, & Gray, 1988);two paradigms in which deficits also reflect associations based upon redundant or irrelevant stimuli. The clear failure of isolate monkeys to exhibit blocking implies possible longterm alterations in dopaminergic functioning; a hypothesis supported by recent evidence from our laboratory (Lewis, Beauchamp, Mailman, & Gluck, 1986; Lewis, Gluck, Beauchamp, Keresztury, & Mailman, 1990). In these experiments isolate and social controls were challenged with the DA agonist apomorphine (0.1 and 0.3 mg/kg), and drug effects on behavioral indices of DA function were examined (i.e., spontaneous blink rate, stereotyped behavior, and self-injurious behavior). At higher doses, apomorphine significantly increased the rate of blinking, whole-body stereotypies, and the intensity of stereotyped behaviors in isolates over that observed in control animals. Thus, permanent alterations in DA receptor sensitivity appear to be a consequence of early social deprivation. Such DA receptor supersensitivity may be related to the isolates’ failure to demonstrate blocking. In conclusion, the present investigation clearly showed a blocking deficit in rhesus monkeys reared 20 years earlier in social isolation. Post-hoc data tentatively suggest the associative mechanism underlying this deficit was the withincompound association. Information processing deficits did not appear to be a function of isolate syndrome behaviors interfering with learning performance, but reflected an important difference in cognitive function. This difference involved the tendency to process redundant information, and thereby develop associations capable of mediating atypical behavior. These data may have important implications for future studies on the long-term neurobiological sequelae of early social impoverishment.

Notes The present research was supported by National Institute of Health grant MH42938 awarded to Doctors Lewis and Gluck.

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