STIMULUS CONTROL OF INSTRUMENTAL REFLEXES IN DOGS: A COMPARISON OF ALIMENTARY AND AVOIDANCE BEHAVIORS AFTER PREFRONTAL DAMAGE

Transcription

1 ACTA NEUROBIOL. EXP. 1982, 42: 5-28 Lecture delivered at the Symposium <'Brain and behavior'* held in Jabtonna near Warsaw May 1981 STIMULUS CONTROL OF INSTRUMENTAL REFLEXES IN DOGS: A COMPARISON OF ALIMENTARY AND AVOIDANCE BEHAVIORS AFTER PREFRONTAL DAMAGE James BRENNAN, Danuta KOWALSKA and Kazimierz ZIELIfiSKI Department of Neurophysiology, Nencki Institute of Experimental Biology Pasteura 3, Warsaw, Poland Key words: Stimulus contr,ol, prefrontal lesions, nature of reinforcement, dogs Abstract. Two experiments involving parallel procedures to investigate stimulus generalization in prefrontal dogs under alimentary and defensive reinforcement were compared. Twelve dogs in the alimentary study were trained on a 50 /o partial reinforcement schedule, and 24 dogs were trained to avoid shock with either continuous shock availability and response contingent CS termination or with only 50 /o partial shock availability and response independent CS termination. One third of the subjects received bilateral medial prefrontal lesions, 12 dogs were given bilateral lesions of the lateral prefrontal cortex and the remaining subjects served as nonoperated controls. Generalization along the frequency dimension of the tonal CS was assessed during a sampling procedure within normal acquisition training, during complete extinction and following differentiation training. The results indicate specific effects from both the quality and the contingency of reinforcement. Within the limits of each reinforcement treatment, a dissociation occurred such that medial subjects tended to show heightened sensitivity to reinforcement density, while lateral subjects showed characteristic elevated reactivity during all generalization tests.

2 INTRODUCTION It has been well established that prefrontal cortex participates in controlling a number of behavioral tasks, although they are evidently ~?ot correlated. The most difficult and controversial problem faced in studies involving destruction of a particular brain structure is related to understanding of functional meaning of the observed symptoms. When performance of a given behavioral task is impaired after removal of a certain part of the prefrontal cortex, we often can not answer the question which of the components involved in this task is responsible!or the deficit. A long series of experiments performed in the Nencki Institute showed that prefrontal dogs are deficient in retention of a go, no-go differentiation tasks (3, 5, 7, 9, 11, 12, 18, 23, 28, 29). Postoperative changes of the performance were labelled as the "disinhibitory prefrontal syndrome", since only small changes in execution of the conditioned response (CR) to the "go" stimulus were observed, whereas the ability of the prefrontal animals to inhibit performance of the same CR to the "no-go" stimulus and during the intertrial intervals (ITI) was markedly poorer than in control animals. Different brain functions may be responsible for this syndrome: impairment in discriminatory capacity, '.drive disinhibition", inability to suppress orienting reactions and other primitive modes of behavior, response perseveration, and so on. Moreover, some experimental variables, such as localization of the lesion (10, 11, 13, 14, 17, 30, 31), duration of the ITIs (lo), and reinforcement contingency on no-go trials (14, 16, 17) influence severity of the postoperative impairment. Further, in contrast to experiments with alimentary responding prefrontal effects on the go, no-go differentiation involving defensive reflexes were either small or absent (1-3, 15, 20, 21, 28, 29). Highly controversial opinions were raised concerning differences in prefrontal effects on retention of the go, no-go differentiation involving alimentary and defensive responding (7, 8, 16, 18, 19, 33, 35, 36). Having in mind the complexity of the prefrontal effects on differential responding, we undertook series of experiments concerning the effects of medial and lateral prefrontal lesions on stimulus control of instrumental responses in dogs, assessed through tests of stimulus generalization (4, 22, 34). We have examined generalization functions under conditions of both alimentary and aversive motivation, and during differing extinction influences as well as after differentiation training. Specifically, both alimentary and avoidance studies provided generalization measures through sampling procedures interspersed with normal acquisition training trials, during complete extinction and after differentiat- Ion training with a conditioned stimulus value (CSS) associated with the

3 external reinforcement event and another stimulus value (CS-) never paired with primary reinforcement. For both alimentary and aversively motivated behaviors, the training and testing dimension of tonal frequency was used. The purpose of this paper is to compare these parallel studies in terms of similarities and differences in stimulus control after prefrontal lesions under conditions of alimentary and aversive reinforcement. OVERVIEW OF METHODOLOGY A total of 36 male, experimentally nalve mongrel dogs were used in both studies, 12 in the alimentary experiment and 24 in the avoidance experiment. Training trials in both experiments consisted of the presentation of the CS of 5 s duration prior to the unconditioned stimulus (US) onset. Table I shows the sequence of stages for the alimentary and avoidance experiments. Both studies followed parallel procedures, except for three differences. The first, which accounts for the doubling of the number of subjects in the avoidance experiment, compared to the alimentary procedure, concerns the issue of partial reinforcement training in the context of aversive conditioning. In the alimentary experiment, a partial reinforcement schedule was employed to generate resistance to extinction, so that subsequent generalization tests could be conducted in extinction. In order to devise analogous procedures for the avoidance conditioning experiment, a partial shock schedule was introduced for 12 of the subjects. After initial training with shock potentially available on all trials, these 12 subjects were given acquisition training trials on which only half of the CS onsets was followed by shock if an avoidance response was not emitted. Moreover, on the nonshock trials, the CS tone of 1000 Hz was not response contingent and remained on for a fixed duration of 5 s, independent of the subject's behavior. The remaining 12 subjects in the avoidance experiment were trained with more traditional avoidance acquisition, insofar as a continuous schedule of shock delivery was potentially available on each trial, and the CS duration was always response contingent. The second exception in the parallel between the alimentary and avoidance experiments, as seen in Table I, involved the duration of generalization testing, which was longer in the avoidance experiment. Specifically, we were able to take advantage of heightened resistance to extinction, generated by the reinforcement properties of avoidance conditioning (27), to prolong generalization testing in extinction during the avoidance experiment. The third difference between the alimentary and avoidance experiments involved the duration of test stimuli during all of the generalization tests. In the alimentary experiment the response made within 9 s

4 Outline of the procedures of both the alimentary and the defensive experiments. CS refers to reinforced value during single stimulus training, and CS+ indicates the reinforced stimulus during differentiation training, while CS- refers to the nonreinforced stimulus value during differentiation training. CRs indicate conditioned responses. Stage Performance and testing criteria Alimentary Defensive PRF Defensive CRF 1. Preliminary training CS = 1,000 Hz A. Continuous rein- 80% CRs for 3 80% CRs for 3 80% CRs for 3 forcement sessions sessions sessions (CRF), 10 daily trials B. Partial reinfor- 90% CRs for 5 90% CRs for 5 cement (PRF), sessions sessions 20 daily trials Prolonged CRF, 90% CRs for 5 20 daily trials sessions 2. Surgery Bilateral medial prefrontal lesions, followed by 10 days recovery. Bilateral lateral prefrontal lesions, followed by 10 days recovery. Normal control given 10 days of rest from experimental procedure. 3. Resumed training PRF, 20 daily trials 90% CRs for 5 90% CRs for 5 sessions sessions CRF, 20 daily trails 90% CRs for 5 sessions 4. Sampled generali- 5 test trials in 20 5 test trials in 20 training trials for 20 sessions zation training trials for 16 sessions 5. Resumed training PRF, 20 daily trials 90% CRs for 5 90% Rs for 5 sessions sessions CRF, 20 daily trials 90% Rs for 5 sessions 6. Generalization in 20 test trials per 20 test trials per session complete extinction session for 5 sessions for 10 sessions. (5 test values) 7. Resumed training, 90% CRs for 5 sessions all groups - CRF, 10 daily trials 8. Differentiation train- 90% CRs to CS+ and 90% Rs to CS+ and ing 90% response omis- 90% response omission to CS- CS+ = 1,000 Hz, sion to CS - for 10 for 10 sessions or 100 days CS- = 600 Hz, sessions 10 daily trials for each stimulus 9. Postdifferentiation 21 test trials per 21 test trials per session for 10 sessions - generalization session for 5 sessions (7 test values)

5 terminated the test stimulus and if a subject failed to respond the test stimulus automatically terminated after the elapse of 9 s. On the other hand the durations of test stimuli in the avoidance experiment were fixed at 9 s, independent of the subject's behavior. The fixed duration of test stimuli in the avoidance experiment was seemed necessary because termination of the CS provide secondary reinforcement of the avoidance responding. Thus in conditions of response contingent test stimuli termination rapid transfer of CR to all test stimuli values was expected. Moreover, the CS duration on nonshock trials in the partial shock schedule was also constant, and the comparison of effects of response contingent CS termination in the continuous and partial reinforcement groups comprised a secondary purpose of the avoidance study. In both experiments, the repeated generalization tests were designed to measure different acquisition and extinction influences. The first generalization test involved a sampling procedure, wherein one block of 5 trials, consisting of tonal presentations of 600; 800; 1,000; 1,200 and 1,400 Hz, was administered within the remaining 15 trials of normal acquisition under each respective reinforcement procedure. The sequence of testing blocks was counterbalanced across subjects and testing sessions. The aim of the sampling test was to assess generalization performance under conditions of minimal extinction. Accordingly, under both partial schedules of the alimentary and avoidance experiments, the maximum density of reinforcement available during sampled generalization sessions was maintained at approximately 40 /o, while the continuous reinforcement schedule of the avoidance experiment was reduced to a density of shock availability of approximately 75O/o per session. The second type of generalization test measured performance to the same test frequencies as used in the sampled test, but the influence of extinction was maximized. Subjects were first required to meet the criterion of response reacquisition of the respective reinforcement schedules, following sampled generalization and prior to generalization testing in complete extinction. The test itself consisted of 20 daily test trials in extinction conducted over 5 sessions in the alimentary experiment and 10 sessions in the avoidance experiment. The third tonal frequency test of generalization followed frequency intradimensional differentiation training. After the second generalization test, subjects were trained with a CS+ of 1000 Hz, associated with the respective reinforcement agent, and a CS- of 600 Hz never paired with primary reinforcement. While the durations of both CS+ and CS- were response contingent in the alimentary experiment, the duration of CS-

6 for subjects that had been earli'er trained with either the continuous or the partial shock schedules in the avoidance experiment, was fixed at 5 s. Again, as with the rationale for constant test stimuli duration during generalization testing, the fixed duration of CS- during differentiation training was used to provide conditions necessary for extinction of the avoidance response. The postdifferentiation generalization test, as with the second test, was conducted in complete extinction, but the test values were expanded to include 400 and 1,600 Hz for a total of 7 test stimuli. The surgical tr'eatment in both the alimentary and the defensive experiments was the same. Four of the subjects in the alimentary experiment and 4 dogs from each of the reinforcement procedures of the defensive experiment underwent bilateral removal of the medial aspect of the prefrontal cortex. These lesions were largely confined to the pregenual and subgenual areas, the medial parts of the proreal and subproreal gyri, the anterior parts of the medial precruciate cortex and the polar cortex. Twelve additional subjects, 4 in the alimentary experiment and 8 in the defensive experiment, received bilateral damage to the lateral pror'eal and orbital gyri (for additional histological analyses, see 4, 22). Lesioned subjects were permitted 10 days of recovery before resumption of the respective experimental procedures. The remaining 4 alimentary and 8 defensive subjects served as intact controls and were allowed a 10 days rest pause from the experimental sessions. MAJOR FINDINGS In the comparison of the alimentary and defensive experiments, the results may be considered under several headings, dealing with the critical independent and dependent variables studied. Primary emphasis, in this presentation, is given to an integrative consideration of the results, so that examples of the major areas of interest are emphasized rather than a complete recasting of the results that may be found in the earlier reports (4, 22, 34). Prefrontal medial and lateral effects of predifferentiation acquisition In general, lateral prefrontal lesions produced a rapid acceleration of post-surgical instrumental responding in both experiments. while medial lesions tended to slow response latencies, relative to normal dogs. However, these trends in prefrontal effects w'ere sensitive to the generalization testing procedure and to the particular nature of the reinforcing agents underlying behavior.

7 Specifically, subjects from both experiments acquired the instrumental pedal pressing response with reasonable facility. Table I1 shows the mean number of daily, 20-trial sessions required to meet the acquisition The mean number of sessions to meet the acquisition criteria of presurgical, postsurgical and postsampled generalization training in the normal (N), medial (M) and lateral (L) surgical treatments of the alimentary and defensive experiments. Acquisition Stages Presurgery Postsurgery Post-Sampled Alimentary N Defensive M (continuous reinforcement) L N Defensive M (partial reinforcement) L criterion during presurgical training, postsurgical reacquisition and retraining following the first, sampled generalization test. As the performance levels in Table I1 indicate for each of the surgical treatment groups in the alimentary experiment, the acquisition and reacquisition stage were remarkably consistent over the three training periods. Similarly, in the surgical groups of the continuous reinforcement training condition in the defensive experiment, subjects showed rapid criterion performance with little interference from the surgical manipulations. While subjects in the partial reinforcement condition of the dtefensive experiment showed minimal adjustment to the presurgical introduction of the partial schedule itself, there was some postsurgical, or post-rest, disruption for the medial and normal groups, respectively, in the number of sessions needed to meet the reacquisition criterion. However, as the numbers of reacquisition sessions after the sampled generalization test indicate, subjects in the medial group recovered as did the normal subjects for the most part. The analysis of the numbers of postsurgical acquisition trials did not reveal any systematic diff,erences due to the three types of reinforcement procedures, indicating that the within group differences in trials to criterion of the partially reinforced avoidance groups were large and the mean scores were attributable to variability from a few subjects.

8 Response latencies provided a more sensitive index of acquisition and reacquisition performance. For the acquisition stages of each experiment, trial latencies were organized into cummulative frequency distributions. To compare the response latency distributions across successive acquisition stages, Kolmogorov-Smirnov tests of the point of maximal difference between pairs of distrilbutions were conducted. Table I11 shows the mean median latencies of each surgical group during the acquisition stages of both experiments. Also shown in Table I11 are the relationships The mean median latencies during presurgical acquisition and reacquisition following surgery and after sampled generalization test for the normal (N), medial (M) and lateral (L) subjects of the alimentary and the defensive experiments. Below the group mean medians for each stage are given the relative positions of the group scores in terms of the significant differences among the Dm,, values of the Kolmogorov-Smirnov tests of the point of maximum differences between pairs of response latency distributions. For example, the relationship signified by L > N > M indicates that the lateral group had a significantly greater number of short latency responses below Dm,, than did the normal and medial groups, and the normal group had a significantly greater number of short latency response than the medial group. Thus, the relative positions of the three groups showed fastest responding in the lateral and slowest in the medial group. Acquisition Stages - - Presurgery Postsurgery Post-sampled N Alimentary M L L>N>M L>N>M L>N>M N Defensive M (continuous reinforcement) L N>M>L L>N>M L>N>M N Defensive M (partial reinforcement) L L>N=M L>N>M M>L>N derived from statistical comparisons among the surgical treatment groups for each stage. In the alimentary experiment, the lateral lesioned subjects showed consistently greater numbers of short latency responses than either the normal and the medial lesioned subjects, which were, in turn, different from each other. A similar hierarchical arrangement of fastest lateral and slowest medial responding emerged after the surgical treatment in the groups given either continuous or partial shock availability during defensive reflex training. Thus, it appears that postsurgical acquisition performance was comparable for all three reinfor-

9 cement groups in terms of the fastest responding in subjects with lateral lesions and the slowness in response latencies in subjects after medial lesions. However, a different pattern of group arrangements emerged in the response latency distributions following the sampled generalization lest. After the 20 sessions of sampled generalization testing, the frequency of short latency avoidance responses in the medial lesioned, partially reinforced group increased dramatically, so that these subjects were responding most rapidly. Moreover, the overall speed of median response latencies in the two avoidance reinforcement groups was more rapid than in the alimentary reinforced groups. These differences in post-sampled reacquisition behavior reflect the underlying bases of acquisition between alimentary and avoidance responses. Specifically, reacquisition after sampled generalization in the alimentary experiment showed the residual effects of limited extinction from the sampled test itself, since all surgical groups had longer response latencies at this stage, compared to reacquisition training immediately after surgery. In contrast, with the single exception of the normal, partially reinforced avoidance groups, all subj'ects trained in the avoidance procedures had shorter response latencies after the sampled generalization test than obtained earlier after surgery. On the basis of traditional two-process theory of avoidance conditioning (26), it is reasonable to interpret this shortening of response latencies in the avoidance groups as an indication of continued improvement of instrumental avoidance acquisition. Whereas, as the limited extinction of the sampled test was detected by the alimentary subjects, the nature of instrumental avoidance behavior apparently precluded detection of the contingency changes by the subjects trained in avoidance responding, which resulted in continual improvement of response speeds at later stages of reacquisition. Dissociated medial and lateral prefrontal effects on predifferentiation generalization behavior The diss~ciativ~effects of prefrontal damage on generalization and differentiation were rather similar, given the constraints from the quality and contingency of reinforcement during the respective training procedures. The medial prefrontal lesions produced a marked sensitivity to reinforcem'ent availability, while the lateral lesions tended to result in elevated responding. The first assessment of stimulus control in both experiments was designed to restrict the influence of extinction during generalization testing by interspersing a block of 5 test trials among 15 trials of continued acquisition under the respective training contingencies. Overall statistics1 analyses of response latencies to the five test

10 frequencies across testing sessions indicated common effects in both experiments from stimuli presentation, the interaction of stimuli x surgery and proglressive testing sessions. Accordingly, response latencies during sampled generalization differed within each training contingency according to prefrontal effects, and there was some evidence of extinction over testing sessions. To compare group differences further during sampled generalization testing, distributions of cummulative response latencies to each frequency test value were constructed for each group. Among the normal subjects, both the alimentary and continuously reinforced avoidance groups differentiated the original CS value of 1000 Hz from the other four frequency values, and in the avoidance group, the 600 Hz value was differentiated as well. In both groups, responding to the 1,000 Hz test value was fairly close to the response level of the reinforced 1,000 Hz CS during the 15 trials outside of the testing block. In contrast, responding in the partially reinforced avoidance group was not well differentiated. Only in the 2nd, 3rd and 4th secs of cummulative 1000 Hz test action was there any evidence of differential responding, and even this level dissipated at later seconds in the cummulative distribution. Also of interest in the generalization of the normal groups during the sampled test was the comparable level of all three groups in the number of intertrial responses. Fig. 1. Cummulative frequency distributions of response latencies to the test stimuli during sampled generalization of the medial lesioned groups trained with alimentary (Panel A), continuous avoidance (Panel B) and partial avoidance (Panel B) reinforcement contingencies. Open symbols represent response latencies to the nonreinforced test stimuli: 0 - denotes responses to the 600 Hz tone; A 800 Hz; 0-1,000 Hz; V - 1,200 Hz; - 1,400 Hz tone. Filled circles show the d,istribution of response latencies to the 1,000 Hz CS presented in the 15 train.ing trials outside of the block containing the testing tonal frequencies. The end of the CS-US interval during training trials is marked by the short vertical line. The monotonic line of each panel shows the level of responding that might be expected on the basis of spontaneous intertrial responding.

11 The cummulative frequency distributions of the medial lesioned groups are shown in Fig. 1 for the alimentary (Panel A), continuously reinforced (Panel B) and partially reinforced defensive (Panel C) groups. As the Lrigure panels show, differential responding in the medial lesioned groups was minimal, and only in the continuously reinforced avoidance group did some differentiation of the 1,000 Hz frequency emerge at latencies greater than 4 s. Moreover, despite the comparable nondifferential performance of the alimentary and the partially reinforced avoidance subjects, these groups were distinguished in terms of the level of Intertrial responses that was noticeably higher in the latter group. Indeed, statistical comparisons of the number of intertrial responses indicated that the level of the partially reinforced avoidance group was reliably h~gher than the other medial lesioned groups during the entire course of sampled generalization testing. One additional measure of behavior during generalization testing, not depicted in the figure panels, consisted of the numbers of extra responses to each test value, i.e., responses emitted after the initial CR during the remaining time of stimulus action. This measure was available only during the avoidance experiment that included a fixed duration of 9 s for all generalization test trials independent of behavior, whereas in the alimentary experiment generalization responses terminated the test value presentations. Comparisons of extra responses during sampled generalization indicated significantly higher levels in the medial and lateral, partially reinforced groups than in their continuously reinforced counterparts; the normal groups were similar. Responding during sampled generalization after lateral prefrontal damage indicated that the alimentary group responded differentially to the 1,000 Hz test value at a level that exceeded the reinforced presentations of the 1000 Hz CS. Moreover, there was some evidence of differentiation of the 600 Hz value, especially at longer latencies. In contrast, the levels of responding in both avoidance groups were quite elevated and nondifferential. Indeed, the levels of responding to all test values by subjects in the partially reinforced avoidance group exceeded the response level to the reinforced presentations of the 1,000 Hz CS value, as early as the 2nd s commulative test stimuli action. Compared to their respective normal and medial counterparts, all lateral lesioned groups showed a higher level of intertrial responding that was especially pronounced after partial reinforcement avoidance training. In addition, the level of extra responses in the partially reinforced avoidance group after lateral lesions was higher than in the continuously reinforced lateral group, and this difference was greater than noted earlier between the medial lesioned groups of both avoidance training contingencies.

12 The results of the sampled generalization test indicated clear evidence of stimulus control in the normal and the lateral lesioned subjects given alimentary reinforcement and in the normal subjects trained with the continuous schedule of shock availability. In the avoidance experirnent only minimal stimulus control was obtained in the normal partially reinforced and the medial continuously minforced groups. Among the medial and the remaining lateral groups, elevated, but nondifferential levels responding em'erged. In addition, this overall activity, especially after partially reinforced avoidance training, persisted consistently throughout training. Thus, this testing condition with minimal extinction influences produced results that are attributable to the interaction between surgical effects and the quality and sch'edule of reinforcement training. The second generalization test in both experiments assessed performance under conditions of maximal extinction influences, since reinforcement was omitted during all testing sessions. The overall statistical analyses of response latencies in both experiments showed that extinction was evident in producing an overall decrease in performance levels across testing sessicns, and the extinction effect was differential among stimuli, as reflected by the interaction between extinction and the effect cf stimuli in each experiment. The effect of surgical treatment was also present, which in turn interacted with the effects of stimuli and progressive extinction. Among the normal groups tested in complete extinction, the alimentary subjects clearly differentiated the CS value of 1,000 Hz from the very beginning of the test stimuli action, and later, responding to the 600 Hz value was clearly slower than to the other test values. The nonoperated, avoidance group trained with continuous shock availability and response contingent CS termination, which had responded with reasonable differentiation in the sampled test, showed a deterioration in differential responding as well as an overall decrease in the level of responding during the test in complete extinction. This finding may have been attributable to the influence of extinction, since the testing procedure for this group, involving no shock and test stimuli prolongation, was a sharp departure from their training procedure. This interpretation supports the view that the underlying basis of avoidance acquisition led to the detection of the rapid switch to an extinction testing procedure. This difference between training and testing procedures is also relevant in the interpretation of clear differentiation present in the normal avoidance group trained with partial shock availability and 50 /o noncontingent response termination of the CS. That is, the testing procedure and training contingencies were more similar for this group

13 than for the continuously reinforced avoidance group. The level of intertrial responding in the alimentary group decreased to a negligible rate during this second test, whereas both avoidance training groups continued their rate of intertrial responses at levels similar to the number of intertrial responses during th'e sampled test. Also, as in the sampled test, the levels of extra responses in the second test for both normal avoidance training groups were consistent and fairly low. Despite their nondifferential, elevated response lev'els during sampled generalization, the medial alimentary group showed a dramatic decrease in response levels and differentiated reslponding beyond 3 s of stimuli action. This sharp difference in medial, alimentary behavior between the sampled test and the test in complete extinction reflects their sensitivity to the diff'ering influences of reinforcement present in each testing procedure. It has been shown in other experiment that medial dogs are sensitive to changes in amount of food reinforcement and pattern of its presentation (24). Neither of the medial avoidance groups showed differentiated responding, but there was a sharp contrast between the levels of generalization responses and intertrial responses. The continuously reinforced medial group had an overall low level of responding to the test stimuli and few intertrial responses, while the opposite was found in subjects trained with the partial shock schedule after medial damage. Again, the extinction influence was marked in both the alimentary and the continuously reinforced avoidance groups, in which a greater difference between training and testing procedures cccurred, than for bhe partially reinforced avoidance group. In turn, the similarities between training and testing accounted for the very rapid overall response level of the partially reinforced group that had medial lesions. The numbers of extra responses in both medial avoidance training groups diminished from sampled to the complete extinction test, but the partially reinforced group still had a significantly higher level of extra responses in the second test than the continuously reinforced group. The distributions of cummulative frequencies of response latencies for the lateral alimentary (Panel A), continuously reinforced defensive (Panel B) and partially reinforced defensive (Panel C) groups during the generalization test in complete extinction are shown in Fig. 2. Rather clearly defined differentiation among all stimuli, ranging from fastest responding to the 1,000 Hz to slowest responding to 600 Hz, emerged in the lateral alimentary group. However, as with the medial performance, generalization responding in the avoidance training groups was not as clear. Subject trained with the continuous reinforcement schedule responded at an overall depressed level, with some evidence of 2 - Acta Neurobiol. Exp. 1/82

14 Tlme bn seconds Fig. 2. Cummulative frequency distributions of response latencies to the test stimuli during the generalization test in complete extinction for the lateral lesioned groups trained with alimentary (Panel A), continuous avoidance (Panel B) and partial avoidance reinforcement 'contingencies. Denotations as in Fig. 1. discriminating the 1,000 Hz value and, to a lesser extent, the 600 Hz valuce, from the other test stimuli. Conversely, the lateral group trained with partial reinforcement had elevated, but nondifferential responding. As with the medial, partial reinforcement group, the partially reinforced laterals had a very high rate of intertrial responding, and their extra responses, which dec~easedfrom the sampled test, were nevertheless much higher than the continuously reinforced lateral group. The extinction effect from this second generalization test succeeded in modifying generalized responding especially in the alimentary experiment. While differences in surgical treatment were appearent, stimulus control was generally improved in the alimentary groups compared to their performanoe in the sampled test. However, the extinction influence interacted with both the reinforcement training histories and the surgical treatment to produce a more complicated situation in the avoidance training groups. The normal subjects did show some stimulus control, however the nondifferential responding in thle medial and lateral lesioned groups were distinguished both by their reinforcement training contingencies and by specific surgical effects. In summary, the dissociated medial and lateral effects during the prediffe~entiation assessments of stimulus control were apparent from the very beginning of testing. Taking the medial effects in the alimentary experiment, the dramatic difference in the level of extent of differentiatled responding between sampled testing and the test in complete extinction may be readily explained by the differing d,ensities of reinforcement available in the two tests. In the defensive study, both medial lesioned groups showed elevated response speeds during sampled generalization, and subjects given continuous reinforcement had some

15 evidence of differentiated responding. However, with testing in complete extinction, the nonavailability of shock produced a sharp decrease in response lev'els in the medial lesioned group trained with continuous reinforcement, which may be attributed to the sharper difference in reinforcement availability for these subjects, compared to the procedural shift from training to testing for the medial lesioned partially reinforced group. The heightened activity of the lateral subjects of the alimentary experiment was especially evident during the sampled test when the level of the nonreinforced 1,000 Hz test value exceeded that of the reinforced presentations of the 1,000 Hz CS. During the test in complete extinction, subjects trained with alimentary reinforcement and given lateral lesions retained an overall higher level of responding, relative to the other groups, and differ'entiated responding to the test stimuli was evident as well. In the avoidance experhent, the laterals of both reinforcement training conditions showed heightened nondifferential response levels in the sampled test. The response levels of the group that had been continuously reinforced decreased somewhat and showed differentiated responses during the first test in complete extinction, which seem'ed to reflect some detection of the shift in procedure from reinforcement availability to extinction. However, the partially reinforced group, which pr,esumably had more difficulty discriminating between acquisition and testing phases, retained their higher level of nondifferentiated responding during the test in complete extinction. Dissociated prefrontal effects and reinforcement influences on differentiation training Following the second generalization test, all subjects from both experiments were given 10 daily reacquisition trials with the 1,000 Hz CS on a continuous reinforcement schedule, i.e., the respective reinforcement agents of food or shock were available on each trial. All subjects easily met the reacquisition criterion of 90 /o correct responses during three consecutive sessions. Differentiation training to the reinforced CS+ of 1,000 Hz and the nonreinforced CS- of 600 Hz continued until subjects attained 90 /o correct responses to CSf and 90 /o inhibited responses to CS-, or if 100 sessions had elapsed, whichever occurred first. Table IV shows the total number of differentiation training sessions for the normal, medial and lateral lesioned subjects of each experimental training contingencies. As these data indicate, the course of differentiation training was markedly different between the alimentary and

16 The total number of sessions to the criteria of differentiation training for the normal, medial and lateral subjects of both alimentary and defensive experiments. Alimentary Defensive (continuous) Defensive (partial) Normal Medial Lateral avoidance experiments. For the alimentary training subjects, overall acquisition of the differentiation was relatively rapid. Three of the medial lesioned subj~ects had near perfect differentiation from the beginning of training and met the criterion in minimal sessions. The lateral lesioned subjects given alimentary reinforcement tended to have somewhat more difficult acquisition than the normals, but the sessions to criterion measure of acquisition indicated similar numbers of sessions for these two groups. Moreover, response latencies to CS+ and to CSconfirmed that the difficulty in mastering the differentiation in lateral lesioned subjects was due to their overall faster response levels to both CS+ and CS-. The latencies for medial lesioned subjects showed rapid responding to CSf and slow responding to CS-, reflecting their easy acquisition of the differentiation task. In contrast to the results of the alimentary experiment, the numbers of sessions to the differentiation criteria for the defensive subjects, indicated in Table IV, show the overall difficulty in mastering the differentiation task in subjects initially trained with both avoidance contingencies. Statistical evaluation did not reveal any trends specific to training or surgical treatments. To examine further the course of differentiation training in the defensive experiment, Mann-Whitney U tests of response latencies to CSf and to CS- were conducted independently for each training session. Comparison of the number of sessions in which responding to CS+ was significantly faster than to CS- indicated

17 that subjects trained earlier with response contingent CS termination and shock potentially available on all trails had better differentiation performance than the partially reinforced groups. Moreover, the continuously reinforced groups had significantly fewer errors to CS+ and to CS- than did the partially reinforced subjects. However, the effect of the surgical manipulation was not present in any of the statistical comparisons of differentiation training in the avoidance experiment. Accordingly, quite clear and marked differences between the alimentary and aversively reinforced subjects emerged during differentiation training. The alimentary subjects acquired differentiated performance after relatively few sessions, and dissociated effects from the surgical treatment accounted for the variability among groups. That is, the extinction influence, especially exaggerated after medial lesions, in the alimentary reinforced subjects facilitated acquisition of the differentiation task. In contrast, although subjects that had continuous reinforcement training tended to show sop-ewhat bett,er differentiation than the partially reinforced groups, overall performance in the subjects trained in avoidance behavior indicated an inability to acquire the differentiation task after extensive single stimulus training and repeated generalization testing, reflecting rather minimal extinction influences. Thus, in the avoidance experiment, deficits in differential responding were attributable to initial training contingencies, rather than to the surgical effects. Reinforcement training and prefrontal lesions effects during postdifferentiation generalization The last generalization test took place following differentiation training and included seven test values. The statistical analysis of generalized responding indicated significant effects in both experiments from test stimuli, progressive testing sessions and their interaction. The surgical effect in both experiments and the type of reinforcem'ent schedule in the avoidance experiment did not attain significance in the analysis of response latencies. The overall similarity in the cumulative distributions of response latencies to the test frequency values confirmed that the surgical effects during this last generalization test were minimal, but the effects of reinforcement history were more potent. Among the normal subjects very clear differentiation of the CS+, 1,000 Hz, value occurred in both the normal alim'entary and partially reinforced avoidance groups. Moreover, the value of CS- was differentiated from the other stimuli in the partially reinforced avoidance group, while both lower frequencies and 400 Hz evoked minimal response speeds in the normal ali-

18 mentary group. In contrast, the normal continuously reinforced avoidance group responded in a manner that may be described as bimodal. That is, two characteristic response levels were evident, one containing CSf and four of the higher frequency values, while the frequency value of the CS- stimulus, 600 Hz, and the value lower than CS-, 400 Hz, had similar slow response speeds. During postdifferentiation generalization performance in subjects after medial lesions revealed differences among all three training contingencies, which is obvious from Fig. 3, showing the cumulative fre- Fig. 3. Cumulative frequency distributions of response intencies to test stimuli during postdifferentiation generalization in the medial lesioned groups trained with alimentary (Panel A), continuous avoidance (Panel B) and partial avoidance (Panel C) reinforcement contingencies: <I>, denotes responses to the 400 H z test - 1,400 X value; Hz; A Hz; 0-1,000 Hz; V - 1,200 Hz; 1,600 H z tones. quency distributions of response latencies for the alimentary (Panel A), continuous shock reinforcement (Panel B) and partial shock reinforcement (Panel C) groups. In the alimentary group, the overall response levels were depressed, but the 1000 Hz CS+ value was differentiated from the rest of the test stimuli, the response levels of which, in turn, were minimal. The overall distributions of response latencies in the medial lesioned group trained with partial shock reinforcement and noncontingent CS termination were quite vigorous, and a hierarchy of responding, with the values of CSf and CS- evoking maximum and minimum levels, respectively, were apparent. The bimodal response character of the normal group was also present in the medial lesioned group trained with continuous shock availability, and responding to the 1,000 Hz value was differentiated aftmer 4 s. Postdifferentiation generalization in lateral lesioned subjects is shown in Fig. 4 for the alimentary (Panel A), continuous shock reinforcement

19 Fig. 4. Cumulative frequency distributions of response latencies to test stimuli during postdifferentiation generalization in the lateral lesioned groups trained with alimentary (Panel A), continuous avoidance (Panel B) and partial avoidance (Panel C) reinforcement contingencies. Denotations as in Fig. 3. (Panel B) and partial shock reinforcement (Panel C) groups. In the alimentary lateral lesioned group, as with their normal and medial counterparts, the response level to the 1000 Hz value was most vigorous, reflecting a nearly all-or-nothing response style, relative to other test stimuli. In the lateral lesioned partially reinforced avoidance group, a hierarchical arrangement ordered from the CSf to the CS- values emerged, although not as clearly differentiated as in the medial, partially reinforced group. The bimodal character of the normal and medial continuously reinforced avoidance groups was not evident in the lateral group, since this group tended to differmentiatethe 1,000 Hz value from the rest of the test stimuli at longer latency values, and the remaining stimuli were clearly nondifferentiated. One final note in the postdifferentiation training generalization test in the avoidance experiment concerns the level of extra responses. In particular, the numbers of extra responses during this test were noticeable. Analysis of the absolute number of extra responses revealed systematic variation according to test frequency values, so that generalization gradients of extra responses were obtained from after both avoidance training contingencies. Accordingly, the number of extra responses provided a measure of stimulus control, in addition to the distribution of r,esponse latencies. The results of postdifferentiation generalization suggested clear differences between the alimentary and avoidance reinforcement. In the alimentary study, where all subj~ectslearned the differentiation, similar extents of stimulus control were obtained from all groups regardless of surgical treatment. Conversely, in the avoidance experiment, where acquisition of the differentiation was variable and less clear, group

20 diff'erences were obtained. However, th'ese differences were more readily attributable to the reinforcement contingencies from earlier training, and only secondarily from surgical effects. STIMULUS CONTROL AND THE NATURE OF REINFORCEMENT The differences in both quality and contingency of reinforcement provided the most sali'ent distinction among the alimentary, continuously reinforced avoidance, and partially reinforced avoidance training conditions. In terms of the quality of reinforcement, both differentiation acquisition and generalization performance in the alimentary groups assum'ed a superior course from the avoidance training groups. With the sing1,e exception of the sampled generalization test in medial lesioned subjects, all other testing procedures produced some evidence of stimulus control in the alimentary groups. Moreover, differmentiation training among all alimentary groups was relatively easy and required only minimal numbers of sessions. In contrast, while differentially sensitive to the schedule contingencies and, to a lesser extent, the surgical effects, generalization and differentiation in the avoidance training groups were lnferior to the alimentary performance. In comparing the quality of reinforcem,ent, it is necessary to consider the underlying motivations specific to shock avoidance and to food reward. As primary reinforcement, the contingency of food reinforcement involved the association between the CS predictor of food and the response produced reward, in this delayed conditioning procedure. The overall generalization performance in the first two tests showed that subjects easily acquired control by the 1,000 Hz CS, since this value was differentiated from the other test values, that in turn were not differentiated very well. Their generalization behavior presumably facilitated acquisition of the differentiation task. Despite their easy acquisition of the differentiation, the postdifferentiation generalization test resulted in a continued restricted range of differentiated responding involving vigorous response speeds to th'e 1,000 Hz test value and relatively slow, nondifferentiated responding to the r'emaining test values. Accordingly, the alimentary results generally support the view that primary food reinforcement successfully generated substantial stimulus control among all surgical groups. In contrast to alimentary performance, two-process theory of avoidance acquisition (25, 26) suggests another reinforcing agent in addition to the primary reinforcement of shock avoidance. Specifically, the secondary reinforcing!properties of CS termination dissipates the acquired fear to the CS, which accumulates as a result of successful pairings with shock during acquisition. The overall gen,eralization performance after

21 both avoidance training contingencies tend'ed to be broader than found in the alimentary experiment, suggesting generalization to the fearevoking properties of tone onset, to the detrim'ent of stimulus control by frequency. The comparison between avoidance procedures offers an opportunity to assess performance in light of the differing contingencies of underlying motivation suggested by two-process th,eory. Specifically, the partial shock schedule did not interfer with avoidance acquisition, as indicated by the comparable acquisition rates of both the continuous and the partial shock schedule groups. However, the 50 /o noncontingent CS termination of the partial shock schedule did not allow the comp1,ete dissipation of the fear evoked by the CS. It was shown recently that procedure in which CS was not terminated by the avoidance response resulted in higher l'evel of fear conditioned both to the CS and to the experimental situation (37). Accordingly, the broader, nondifferential generalization during the sampled test, especially in the normal, partial shock reinforcement group in comparison to that of their continuous shock reinforcement counterparts, is consistent with this interpretation of the effects of partial CS termination as a product of residual fear to the CS (see also 34). However, comparison of the normal groups in the avoidance experiment tested in complete extinction reveal'ed more differentiation and less generalization in the partial shock reinforcement group. This finding may be attributed to the greater similarity between training and testing procedures of the partially reinforced groups, which produced less disruption and better stimulus control than obtained from the continously reinforced group. Similarly, the trend toward somewhat better differentiation acquisition in subjects with a history of the continuous shock schedule of reinforcement is consistent wlth their prior training that allowed them to differentiate better the response contingent CSf termination from the response independent termination of CS-. In contrast, the partially reinforced group had extensive experience with the 1,000 Hz CS+, the termination of which only sometimes had been response contingent. Presumably, the overall better stimulus control during the postdifferentiation generalization test in the partially reinforced avoidance groups resulted from the positive transfer from their earlier history with partial response contingent CS termination. Thus, the type of training in the avoidanc'e experiment remained a consistent influence on subsequent generalization testing and differentiation training, which depended on the similarity or disimilarity of the testing procedures with initial avoidance acquisition procedures. The results of these experiments, employing parallel procedures,

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