Probability learning in pigeons (Columba livia) is not impaired by hyperstriatal lesions

Physiology&Behavior,Vol. 31, pp. 279-284. Pergamon Press Ltd., 1983. Printed in the U.S.A.

Probability Learning in Pigeons (Columba livia) is not Impaired by Hyperstriatal Lesions E U A N M. MAcPHAIL A N D S T E V E R E I L L Y Department o f Psychology, University o f York, Heslington, York, UK.YO1 5DD R e c e i v e d 2 A u g u s t 1982 MAcPHAIL, E. M. AND S. REILLY. Probability learning in pigeons (Columba livia) is not impaired by hyperstriatal lesions. PHYSIOL. BEHAV. 31(3) 279--284, 1983.--three experiments investigated the effects of hyperstriatal lesions on spatial and visual probability learning in pigeons. The lesions did not affect choice accuracy although they did reduce positional responding on error trials in the visual task. The results gave support to a perseverative, as opposed to an attentional, interpretation of the lesion effects. Increasing intertrial interval in the visual task resulted in decreased accuracy in both lesion and control groups, and the absence of a differential effect on the lesioned birds ran counter to an earlier suggestion that increased perseveration might be due to increased frustration. A fourth experiment confirmed that the lesions disrupted both acquisition and reversal of a conventional orientation discrimination; the deficits again appeared to be due to increased perseveration rather than to shifts in attention. Pigeons Hyperstriatal lesions Perseveration

Probability learning

IT IS well established that lesions of the avian hyperstriatal complex (hyperstriatum accessorium, hyperstriatum dorsale and hyperstriatum ventrale) disrupt performance in reversals of simultaneous discriminations [7, 8, 9, 18]. It is also clear that both acquisition and non-reversal shifts may be disrupted by hyperstriatal lesions [10, 12, 15], and it seems likely that failures to find disruption in hyperstriatal birds of those tasks (e.g., [7]) may have been due, at least in part, to the relative insensitivity of the tasks, performance in them probably being affected by uncontrolled sources of variance. Two regions within the hyperstriatal complex (the intercalated nucleus of the hyperstriatum accessorium, and the hyperstriatum dorsale) receive direct thalamic visual projections [4], but it does not seem likely that the deficits obtained in simultaneous discriminations are a result o f gross impairment of visual perception, since retention of pre-operatively acquired brightness and pattern discriminations is minimally affected by damage to hyperstriatal visual areas [2]. Two current interpretations of hyperstriatal damage are, first, that hyperstriatal birds m a y show perseveration of central sets [12] (a concept originally advanced by Mishkin in 1964 [14] to account for the deficits of monkeys with frontal cortex damage) and, second, that they may show unstable attention in the face of non-reward [15,17]. The two hypotheses generate opposing predictions concerning performance in a probability learning task. In this paradigm, animals are required on each trial to choose between one stimulus (S+, the majority stimulus) which is

Reversal learning

Central sets

Attention

rewarded (typically) on 70% of trials and another ( S - , the minority stimulus) which is rewarded on the remaining trials. Optimal performance on these problems consists in choosing the majority stimulus on 100% of occasions (maximising). In general, birds and mammals do tend towards optimal performance [11], although they rarely show perfect performance. Mackintosh [5] has suggested that " e r r o r s " (choices of the minority stimulus---whether or not they are rewarded) are generated by the tendency of even well-trained subjects to show shifts of attention from the relevant dimension (e.g., color) to some irrelevant dimension (e.g., position). Mackintosh, Lord and Little [6] found, for example, that pigeons performing probability learning tasks in which either position or color was the relevant dimension showed strong preferences, on trials on which errors occurred, for one value or the other on the irrelevant (color or position) dimension. These attentional shifts are taken to be a consequence of the occurrences of non-reward that are inevitable in the probability learning task, and the more labile an animal's attention in the face of non-reward, the more errors will be made. If hyperstriatal pigeons show enhanced perseveration of central sets then, once attention has been directed to the appropriate dimension, it should be less likely to deviate, so that, if Mackintosh's account is valid, performance should be facilitated by hyperstriatal damage. If, on the other hand, hyperstriatal damage increases lability of attention then, of course, performance should be disrupted in lesioned birds.

Copyright © 1983 Pergamon Press Ltd.--0031-9384/83/090279-06503.00

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M A C P H A I L AND R E I L L Y

Experiments 1 and 2 test acquisition of, respectively, a spatial and a visual (color) probability learning task. A third experiment was designed to explore a further hypothesis which arose from a recent study of short-term memory (STM) in hyperstriatal pigeons [13]. That investigation found performance deficits in hyperstriatal birds at long, but not at short, inter-trial intervals (ITIs), and it was tentatively suggested that this result might reflect an exaggerated susceptibility to frustration in hyperstriatal birds (the possibility being raised that increased perseveration might be a secondary consequence of frustration). However, a recent report [16] has provided the novel suggestion that part of the improvement seen in STM tasks in normal birds at long ITIs (an improvement conventionally attributed-solely to a decline in the influence of proactive interference) may be due to an increase in the signal-value of the sample stimulus as a predictor of f o o d - - a phenomenon comparable to autoshaping [1]. Unpublished studies in our laboratory have found that hyperstriatal birds show low levels of autoshaped responding, and this suggests an alternative account of the deficit seen in hyperstriatal birds at long ITIs in the STM task, namely, a failure to benefit from an increased signalvalue of the sample stimulus. The "frustration" account of hyperstriatal function would anticipate a differential effect of long ITIs on the performance of normals and hyperstriatals in all tasks, whereas the account in terms of deficient autoshaping would expect disruption only on tasks which benefit from an increased signal-value of the stimuli (and this would be manifested by an improvement in the performance of control birds at long ITIs). Experiment 3 explored the effects of a long ITI on probability learning: it was anticipated (correctly) that control birds would not show improved performance at a long ITI, so that the task was expected to provide a test of the frustration hypothesis, since that hypothesis, unlike the "autoshaping" hypothesis, would expect disruption by hyperstriatal lesions. These experiments were intended to test hypotheses which had been advanced to explain the deficits obtained in conventional simultaneous discriminations and, most reliably, in the reversal of those discriminations. It was therefore important to show that such deficits were present in the lesioned birds used in these experiments so that, on completion of Experiment 3, reversal training was explored. A first study simply reversed the majority and minority stimuli used in Experiment 3, keeping all other conditions identical. That investigation was terminated after 10 sessions, however, since neither group at that stage had made much progress and it seemed likely that there would be a large amount of variance in both groups in errors to reversal criterion in that probability learning paradigm. Experiment 4 investigated the effects of hyperstriatal damage on acquisition and reversal of a conventional simultaneous visual orientation discrimination; it has previously been shown that neither sham operations nor neostriatal lesions affect acquisition or reversal of simultaneous discriminations [7, 8, 9], and unoperated controls were therefore used in the present experiments.

METHOD

Animals Ten naive pigeons (Columba livia) were used. Their ad lib feeding weights ranged from 315-440 g. The birds were housed individually in cages in which water was freely available.

Apparatus In Experiments 1, 2 and 3, the birds were trained in one of two identical pigeon chambers (35×35×35 cm); each chamber was placed in a dark sound-attenuated cubicle, and contained three response keys, each 3 cm in diameter. The center key was mounted directly over a grain feeder at a height of 27.5 cm above the floor. The remaining two keys were mounted on either side of the center key at the same level. The keys were 11 cm apart, center to center. The center key could be illuminated from behind with yellow light, and the two side-keys, with either red or green light. There was a houselight mounted on the front wall of the chamber, 5 cm above the center key. In Experiment 4, the birds were trained in one of two identical chambers, which were similar to those described above except that the center key could be illuminated with white light and the side-keys, with patterns of three white lines on a dark background running either horizontally (stimulus H) or vertically (stimulus V). Control of the sequence of events in the chambers and collection of data were carried out online by a Nova 3 computer. Programs were written in the Act-N language (Campden Instruments Ltd.)

Surgery Five experimental subjects received bilateral electrolytic lesions o f the hyperstriatal complex. A 2.5 mA anodal current was delivered for 20 sec to each of six placements in each hemisphere, via a stainless steel insect pin electrode, insulated to within 0.05 mm of its tip. During the operation, subjects were held in a modified stereotaxic instrument while anesthetized with sodium pentobarbital (30 mg/kg), supplemented where necessary with ether. The locations of the placements were determined using the Karten and Hodos [3] atlas; in each hemisphere there were two placements, at 1.5 and 3.5 mm lateral to the midline, at each of three levels, 9, 11 an 13 mm anterior to the interaural zero. The electrode tip was lowered 2 mm below the brain surface for all the lesions. The remaining five subjects served as unoperated controls.

Histology Birds were killed with an overdose of sodium pentobarbital following completion of Experiment 4. Their brains were extracted and placed in Bouin's solution for 24 hours, following which they were dehydrated and embedded in paraffin wax. Serial sagittal sections were cut at 16 ~ m , and every 10th section was mounted and stained with cresyl fast violet. Reconstructions of the lesions were made on standard drawings derived from the Karten and Hodos [3] atlas, with the aid of a microscope and projection equipment.

Procedure Pretraining, Birds were maintained on an ad lib diet for some 3 months following surgery, and during this time they were weighed daily. Both groups showed small weight gains and there were no reliable differences between the groups in changes in weight over this period. At the end of this phase, ad lib weights ranged from 320-465 g. Pigeons were then reduced to 80% of their ad lib weights and behavioral training began. The birds were first trained to

HYPERSTRIATUM AND PROBABILITY LEARNING eat from the feeder and then, by the use of an autoshaping procedure [1], to peck all three keys when illuminated by yellow light (the center key) or by red or green light (the side-keys). On the final day of pretraining all birds received a single test trial, to assess any side-key preference. The sequence of events on that trial was as follows: The center key was illuminated with yellow light; a single response to that key extinguished it and illuminated both side-keys with red light. A single response to either side-key extinguished it and obtained a 4-sec time-out. The houselight was illuminated throughout the trial except during the time-out. Experiment I: Spatial probability learning. Each trial began with the illumination of the center key with yellow light. A response to the center key extinguished it and illuminated the side-keys, one with red, the other with green, light. A single response to a side-key extinguished both keys and constituted a choice. A correct choice was followed by 4-sec access to grain in the feeder, and this terminated the trial. An incorrect choice was followed by a 4-sec time-out which in turn was followed by a " g u i d a n c e " trial. The guidance trial was identical to the initial trial, except that only the correct side-key was illuminated following response to the center key; guidance trials terminated, following a response to the lit side-key, with 4 sec access to the feeder. The ITI following correct initial choice trials or guidance trials was 5 sec, and the houselight was on throughout except during time-outs and feeder operation. There were 40 trials (excluding guidance trials) in each session, arranged so that on 7 trials of each block of 10 the majority stimulus (S+), which was the side-key opposite to that chosen on the test trial at the end of pretraining, was correct, the minority stimulus ( S - ) being correct on the remaining 3 trials. S + was never correct on more than 3 trials in succession, and S - , on more than 2 consecutive trials. On 5 of every 10 trials, the left key was lit by green light, the right by red, the reverse being the case on the remaining 5 trials. The same color did not appear on a side-key for more than 3 consecutive trials. Two different trial sequences were used on alternate sessions. The birds were trained using these procedures for 30 sessions, which were spaced a minimum of 24 hours apart. Experiment 2: Visual probability learning. Training began immediately following completion of training in Experiment 1. The birds were run for 40 trials (excluding guidance trials) each session. Trials were organized exactly as in the final 30 sessions of Experiment 1, except that the majority (70%) stimulus in the experiment was the green stimulus; restrictions on the sequencing of trials were identical to those of Experiment 1. There were 40 sessions in which ITI was set, as in Experiment 1, at 5 sec. Experiment 3: Long-lTl visual probability learning. The procedures used were those of Experiment 2, except that ITI was set at 30 sec; the interval between an incorrect choice and the guidance trial remained 5 sec. There were 20 sessions in this experiment.

Experiment 4: Acquisition and reversal of an orientation discrimination. Following termination o f the 10 sessions of unsuccessful training on reversal of the probability learning problem, birds were given two sessions of pretraining during which they learned, through the use of an autoshaping procedure, to respond in the new apparatus to all three keys when illuminated by white light (the center key) or by the H or V stimulus (the side-keys). On the following session, acquisition and reversal training began. Each trial began with

281 the illumination of the center key with white light. A response to the key extinguished it and illuminated the two side-keys, one with the H, the other with the V stimulus, the allocation of the stimuli to the side-keys being ordered according to Gellermann sequences so that neither stimulus appeared on the same side-key for more than three trials in succession. A single response to either side-key constituted a choice and resulted in either 4-sec access to food (following a correct choice) or in a 4-sec time-out (following an incorrect choice), following which there was a 10-sec ITI. The houselight was on throughout, except during feeder operation or time-outs. H was the correct stimulus during acquisition, and V, during reversal; neither guidance nor correction trials were used in this experiment. Training continued each day until the criterion of 15 consecutive correct responses had been achieved. Reversal training began on the day following achievement of criterion on acquisition training, and continued until criterion was again reached. RESULTS

Anatomical All 5 birds showed bilateral damage to the 3 major components of the hyperstriatal complex (the hyperstriatum accessorium, hyperstriatum dorsale and hyperstriatum ventrale), although in no case was any of these structures wholly destroyed; there was in 2 birds also some invasion of the neostriatum. The range of the total extent of the lesions was relatively small, and Fig. 1 shows reconstructions of the lesions of the two birds having, respectively, the least and the most damage; it may be noted that these were in fact the 2 birds that showed neostriatal damage. These lesions are generally comparable to those used in a recent study of perseveration in hyperstriatal pigeons [12], and, as was observed in that report, the lesions produce only restricted invasion of the hyperstriatal areas known to receive direct visual projections from the thalamus, and much damage to areas which do not appear to receive such projections (see [4] for an account of the location of hyperstriatal visual areas in pigeons).

Behavioral Experiment 1. The results of Experiment 1 will not be presented in detail. Both groups rapidly became proficient, and their performances were generally similar, there being considerable overlap of individual scores from the groups. The significance of the study was reduced, however, by two features of the results: First, one of the control birds developed a preference for S - over Sessions 21-24, and maintained that preference until the end of training; second, there was no evidence that the irrelevant (color) dimension provided salient distractors, since the birds (of both groups) failed to show, on error trials, any marked preferences for either of the color stimuli. Experiment 2. The performance of the two groups over the 40 sessions is summarized in Fig. 2, which shows the mean percentage green (S+) choice for each group, pooled over blocks of 5 sessions. Figure 2 shows that performance throughout the experiment was similar in the two groups. Analysis of variance of the data shown on Fig. 2 found a significant effect of blocks, F(7,56)=40.36, p<0.001, and no main effect of groups or of the interaction, both F s < l . There was in this experiment good evidence for a role in errors by the irrelevant position dimension: Over the first

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MACPHAIL AND REILLY

, , B,,

FIG. 1. Left: Sagittal sections through the intact pigeon telencephalon. (The number next to each section indicates the plate in the Karten and Hodos [4] atlas from which the drawings were derived. Abbreviations: A, Archistriatum; AD, archistriatum, pars dorsalis; APH, area parahippocampalis; AV, archistriatum, pars ventralis; BAS, nucleus basalis; BO, bulbus olfactorius; CA, commissura anterior; CDL, area corticoidea dorsolateralis; DA, tractus archistriatalis dorsalis; E, ectostriatum; EP, periectostriatat belt; FA, tractus fronto-archistriatalis; FT, tractus frontothalamicus et thalamofrontalis; HA, hyperstriatum accessorium; HD, hyperstriatum dorsale; HIS, hyperstriatum intercalatus suprema; HP, hippocampus; HV, hyperstriatum ventrale; LFM, lamina frontalis suprema; LFS, lamina frontalis superior; LH, lamina hyperstriatica; LMD, lamina medullaris dorsalis; LPC, lobus parolfactorius; NC, neostriatum caudale: NF, neostriatum frontale; NI, neostriatum intermedium; PA, paleostriatum augmentatum; PP, paleostriatum primitivum; TN, nucleus taeniae; V, ventriculus.) Center: Serial reconstructions of the lesions (marked in black) of the bird having the least damage. Right: Serial reconstructions of the lesions of the bird having most damage.

block of 5 sessions, 9 of the 10 birds showed most errors on the side which had previously been the majority stimulus in the position discrimination, the 10th bird being the control bird which had in any case shown a preference for the minority side-key at the end of that training. The mean percentage errors occurring on the preferred side-key (i.e., the side on which most errors actually occurred) over the first 5 sessions was, for the hyperstriatal birds, 83% and, for the controls, 91%, t < l . Over the last 5 sessions of training 9 of the 10 birds still showed most errors on the side-key preferred at the outset of color training and corresponding scores were, for the lesion group, 67% and, for the controls, 86%, t(8)= 1.86, 0.05
106 96 4o'1

) 86 0

6~

L~ BLOCKS OF

----~------

0

LESION

CONTROL

5 SESSIONS

FIG. 2. Performance of the two groups in the color probability learning task, using a 5-sec 1TI (Experiment 2).

phases, birds were at asymptote over those sessions, so that it appears that increasing ITI in probability learning problems has a detrimental effect on performance. In order to analyse possible accounts of the effect of increasing ITI, side-key preferences shown on error trials in this experiment were compared with those seen in Experiment 2. For this purpose, birds were once again assigned a preferred side (the side to which most errors occurred) and for each bird the percentage of errors made on that side over

HYPERSTRIATUM AND PROBABILITY LEARNING

283

TABLE 1 MEAN SCORES (-+S.E.) ON THREE MEASURES OF PERFORMANCE IN EXPERIMENT 4 Acquisition

Group

Errors

Hyperstriatal

Perseverative Blocks

Positional Blocks

Errors

Perseverative Blocks

Positional Blocks

5:6 -+ 2.5 2.4 _+ 0.5

12.2 - 1.6 9.4 - 1.1

322.2 -+ 45.1 178.2 - 33.7

26.2 _+ 2.6 12.8 _+ 5.7

32.0 + 10.5 19.8 _+ 5.6

111.6 _+ 16.6

Control

Reversal

63.6 _+ 7.8

100

+90 lad ¢..) O I-.z hi J J

L~

~r 70

I

--

11

2i

--

--

- 0 -

--

--

--

o 3i

LESION

CONTROL 4I

BLOCKS OF 5 SESSIONS F I G . 3. P e r f o r m a n c e o f the t w o g r o u p s in the c o l o r p r o b a b i l i t y l e a r n ing task. using a 30-sec ITI (Experiment 3).

choices were incorrect, and as position responding if 8 or more choices were of the same side-key. This same technique of analysis, which reduces the chance of any given block being scored as both perseverative and positional, was used by Macphail [12]. Separate analyses of variance were carried out on the scores of the two groups for the three measures in acquisition and reversal. Analysis of the error scores found significant effects of both group, F(1,8)=7.13, p<0.03 and phase (acquisition versus reversal), F(1,8)=57.40, p<0.001; the interaction narrowly failed to achieve the 0.05 significance level, F(1,8)=5.00, 0.05 0 . 2 , nor of the Group × Phase interaction, F < I ; the main effect of phase was once again significant, F(1,8)=6.05, p <0.04. These analyses show, then, that by all three measures, reversal was a more difficult task than acquisition, that the lesion group were impaired on both acquisition and on reversal, the reversal deficit being somewhat more marked, and that the source of the deficit lay in exaggerated perseverative responding. DISCUSSION

the final 5 sessions was scored. The mean score of the hyperstriatal birds was 69%, and of the controls, 90%; these differ very little from the corresponding scores over the final 5 sessions of Experiment 1 (67% and 86%), and analysis of variance confirmed that there was no main effect of experiment, F < I . Although the interaction of group and experiment also failed to reach significance, F < I , the main effect of group was significant, F(1,8)=11.47, p<0.01; it will be recalled that analysis of the data from the final 5 sessions of Experiment 2, taken alone, narrowly failed to achieve significance, 0.05
The results o f these e x p e r i m e n t s show clearly that hyperstriatal damage that is sufficient to disrupt conventional simultaneous discrimination and reversal performance does not affect overall level of performance in probability learning. The lack of disruption suggests that attention to the relevant dimension was adequately maintained despite nonreward, and so goes against the predictions of the "attentional" interpretation of hyperstriatal damage [15]. The fact that hyperstriatal birds in Experiments 2 and 3 showed less marked side-key preferences on error trials suggests, as predicted from the "central sets" account, that in fact their attention was less likely to deviate than that of controls. It is, t h e n , s u r p r i s i n g , given M a c k i n t o s h ' s [5] a c c o u n t o f probability learning, that the birds did not show enhanced overall accuracy. It has been suggested elsewhere [11] that there are grounds for doubting whether deviations in attention are the major cause of errors in avian probability learning performance, and it can be argued that the pattern of results obtained here supports that scepticism: Hyperstriatai pigeons showed less sign of control by irrelevant stimuli than controls, but made no fewer errors, and both hyperstriatal

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and control birds showed more errors at a long than at a short ITI (cf., E x p e r i m e n t s 2 and 3), but showed no change in the apparent level of control by irrelevant cues. The fact that increasing ITI did influence probability learning, but did not differentially affect the two groups, suggests that the deficit in hyperstriatal birds noted at long ITIs in an STM task [13] is at least to s o m e extent taskspecific and so unlikely to be a c o n s e q u e n c e o f e x c e s s i v e frustration, the effects of which would be general. This in turn encourages further investigation of the possible link between hyperstriatal autoshaping deficits and the long-ITI STM deficit. The deterioration in probability learning at a long ITI is of considerable intrinsic interest, and should be further explored in unoperated birds; one possibility is, of course, that it is indeed caused by frustration induced by long inter-reinforcement intervals. The pattern of responding shown by hyperstriatal birds in E x p e r i m e n t 4 gives further support to the p e r s e v e r a t i o n o f central sets hypothesis: The problem of the hyperstriatal birds appeared to be not one of lapses of attention to the irrelevant (position) dimension, but, on the contrary, of excessive perseveration to the incorrect stimulus on the relevant dimension. The use of unoperated controls lends the more force to the fact that lesioned birds were no less accurate than controls in their choices in E x p e r i m e n t s 1, 2, and 3, and it has already been noted that neostriatal lesions do not obtain deficits in acquisition or reversal learning [8]. The other lesion effect found here, a decreased t e n d e n c y to deviate attention to an irrelevant dimension, resembles the finding reported previously [8] that hyperstriatal pigeons showed a

significantly reduced tendency to deviate from an initial side-key preference in the face of non-reinforcement. That effect too was absent in birds with neostriatal lesions, and it may therefore be concluded that the effects obtained here are specific to the area damaged, and not the c o n s e q u e n c e s of, say, surgery or of brain damage in general. One final observation should be added. Performance of individual birds in Experiments 1 and 2 c a m e close to the optimal level: 6 birds (3 experimental, 3 control) made no errors on at least one of the final 5 sessions of Experiment 1 and 3 (2 control, 1 hyperstriatal) on at least one of the final 5 sessions of E x p e r i m e n t 2, 2 of those birds achieving perfect p e r f o r m a n c e on at least one session of both experiments. Mackintosh [5] has suggested that birds show quantitavely inferior performance to rats in probability learning tasks, and that this reflects an inferior stability of attention. The present results indicate that given appropriate conditions pigeons can perform perfectly in probability learning tasks even when salient irrelevant cues are present, so that they connot be taken to be generally inferior to any species, let alone rats, in this type of problem.

ACKNOWLEDGEMENTS This research was supported by a grant from the U.K. Medical Research Council. We are grateful to Geoff Hall, for making the suggestion upon which the experiments were based, and for his comments on a draft of the manuscript; to Jane Mitchell for her comments on the draft; and to David Whiteley and Gordon Smith for photographic assistance in preparing Fig. 1, which used diagrams kindly supplied by Bill Hodos.

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