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Some paradoxical effects of bilateral lesions in the frontal cortex in rats
Neuropsychologia, 1967, Vol. 5, pp. 73 to 84. Pergamon Press Ltd. Printed in England
SOME PARADOXICAL EFFECTS OF BILATERAL LESIONS IN THE FRONTAL CORTEX IN RATS M. A. JEEVES Department of Psychology, University of Adelaide, S. Australia (Received 6 July 1966)
Abstract--Rats with bilateral lesions of the frontal cortex were trained to discriminate between patterns of horizontal and vertical black and white stripes. The preference established on the initial discrimination learning was then reversed a total of eight times, e.g. if vertical stripes were positive on Reversal R0, horizontal stripes were positive on Reversal RI, vertical stripes on Reversal R2, and so on. On the initial discrimination and each of the eight successive reversals, the frontal animals required fewer trials to reach criterion than a mock operated control group. Detailed analyses of the results enabled a comparison to be made between several possible competing explanations of the observed differences. It is concluded that the explanation which best fits the present results and those of other relevant studies is that the effect of frontal lesions is to reduce the anxiety and frustration which are otherwise generated by a task in which every lime the animal reaches criterion with one set of stimuli, the signs of the stimuli are immediately reversed. THE STUDY r e p o r t e d here is one o f a series designed to investigate the relative sensitivity o f d i s c r i m i n a t i o n a n d reversal learning as measures which m a y reflect structural and developmental changes in the central nervous system [1, 2]. The m a i n object o f the experiment was to study the effects o f bilateral p r e f r o n t a l lesions on the initial learning a n d eight successive reversals o f a visual p a t t e r n discrimination task. By continuing the experiment for eight successive reversals extending over a n i n e - m o n t h period, it was p l a n n e d to investigate the longer term effects o f such lesions in a situation where task difficulty for the a n i m a l is assumed to increase for the first reversals a n d then to steadily decrease as 'learning to learn' begins to take effect. Several p a r t i c i p a n t s (PRIBRAM, p. 145; HARLOW, p. 146) in the 1962 conference on the F r o n t a l G r a n u l a r Cortex a n d Behaviour (WARREN a n d AKERT [3]) expressed the need for c a u t i o n before t o o easily ignoring or attributing to chance factors the finding o f several investigators that frontal lesions either did n o t p r o d u c e b e h a v i o u r a l deficits o r that they might even result in an a p p a r e n t i m p r o v e m e n t in performance. The recent p a p e r by CRoss et al. [4] provides yet a n o t h e r study in which certain types o f frontal lesions fail to p r o d u c e a deficit in a maze learning task, in this case the H e b b - W i l l i a m s Maze. M o r e o v e r an inspection o f their d a t a presented in the form o f a h i s t o g r a m (p. 62) suggests a slightly i m p r o v e d p e r f o r m a n c e following lesions to the anterior cortex. Whilst it is difficult to m a k e exact c o m p a r i s o n s o f the results o f different studies because o f slight differences in such things as the type o f learning task used, the m e t h o d o f r e w a r d e r p u n i s h m e n t given a n d the surgical p r o c e d u r e s employed, it does nevertheless seem reasonable to summarise the m a i n findings from relevant earlier studies with rats by saying that anterior cortical lesions p r o d u c e no observable deficits in learning the following types o f 73
74
M . A . JEEVES
t a s k s : (i) a p o s i t i o n d i s c r i m i n a t i o n [5, 6]; (ii) a b r i g h t n e s s d i s c r i m i n a t i o n [6]; (iii) a b r i g h t n e s s d i s c r i m i n a t i o n r e v e r s a l [6]; (iv) t h e H e b b - W i l l i a m s M a z e [4, 7]. O n tile o t h e r h a n d a n t e r i o r c o r t i c a l l e s i o n s t o p r o d u c e a deficit (i) in p o s i t i o n h a b i t r e v e r s a l l e a r n i n g [6]; (ii) in v i s u a l p a t t e r n d i s c r i m i n a t i o n l e a r n i n g [8] a n d (iii) i n t a s k s w h i c h a r e s a i d t o i n v o l v e s y m b o l i c p r o c e s s e s s u c h as d o u b l e a l t e r n a t i o n [9], d e l a y e d a l t e r n a t i o n [10] a n d l e a r n i n g t o r u n a fixed d i s t a n c e d o w n a m a z e [11]. I n t h e l i g h t o f t h e s e e a r l i e r f i n d i n g s it h a d b e e n o u r e x p e c t a t i o n t h a t w h i l s t t h e a n i m a l s w i t h f r o n t a l l e s i o n s m i g h t b e s o m e w h a t s l o w e r in l e a r n i n g t h e i n i t i a l d i s c r i m i n a t i o n [8] t h e y w o u l d b e a p p r e c i a b l y s l o w e r i n l e a r n i n g t h e first r e v e r s a l . M o r e o v e r t h e a d v e r s e effect o n t h e l e a r n i n g o f t h e r e v e r s a l s w o u l d b e e x p e c t e d t o become greater on the second and possibly third reversal but thereafter the difference might b e e x p e c t e d t o b e r e d u c e d as t a s k difl]culty l e s s e n e d w i t h t h e o n s e t o f ' l e a r n i n g t o l e a r n ' .
METHOD Subjects The S's were twenty naive, male hooded rats 150-days-old at the start of the experiment. They were assigned at random to two equal groups, and housed in individual cages. Throughout the experiment they had water continuously available in their home cages and were fed for 1 hr a day following running in the learning task. Procedure One unit of a discrimination apparatus previously described [12] was used with a start box and a goal box. Two aluminium gates were hinged at the top and either could be locked by placing a nail behind it. The rats were adapted to the apparatus by a series of steps ending with a limited number of forced choices in which grey gates were used. All animals were running freely through the doors at the end of this pretraining. Immediately the pretraining was completed all animals were operated upon. Surgery was performed under intraperitoneal nembutal anaesthesia. An incision was made in the mid-line of the scalp. The fascia were removed, the coronal suture was identified and two burr holes were made with a dental drill 3 mm anterior to the coronal suture and 0.5 mm either side of the mid-line. The lesions were made by placing the positive electrode through the burr hole, piercing the meninges and lowering the electrode approximately 0.5 mm into the cortex. The other electrode was placed in the right hind leg. A current of 3mA at 600V d.c. was passed for 10 sec. This was then repeated in the other hemisphere. Because of the electro-cauterising effects of such lesions there was little bleeding. If it were a control animal the same procedure was adopted as far as making two small burr holes in the skull but no electrodes were placed in the cortex and no current was passed. In both cases the incision was dusted with antibiotic powder and closed with Michel clips which were usually removed five days post-operatively. After a recovery period of I0 days the animals were again run in the maze with grey doors to renew their acquaintance with the apparatus. The experiment proper was then begun using stimuli of horizontal and vertical black and white stripes matched for brightness. In both groups half the animals began with horizontal and hall' with vertical stripes as the positive stimulus in the initial discrimination learning task. The patterns were changed from right to left in accordance with the randomized sequence devised by GELLERMAN [13]. Selfcorrection of errors was permitted. An error was defined as touching a gate with the nose. In the goal box S was allowed a few seconds to eat before being returned to the start box. Each animal was run for ten trials a day for 7 days a week. As soon as an animal made 18 out of 20 correct responses on two successive days, the signs of the stimuli were reversed on the following day and the procedure continued until criterion was again reached when the signs of the stimuli were again reversed until eight successive reversals had been learned to criterion. The animals were then sacrificed under nembutal anaesthesia and their brains were perfused with saline solution and formalin. The brains were embedded in wax and stained with methyl blue. Examination of serial sections of the brains at a separation of 40/t, allowed reconstruction of the lesions which are shown diagrammatically in Fig. 1. RESULTS General rate of" learnh~g and reversal The frontal group (E) required fewer trials to reach criterion on the original discrimination learning and on each of the eight successive reversals than the control group (C). These results are presented graphically in Fig. 2 and an inspection of Table 1 shows that on the first discrimination (R0) and on reversals mnnbers 2, 3, 4 and 5 these differences were significant at better than the 6 ~ level using a t test.
SOME PARADOXICALEFFECTSOF BILATERAL LESIONSIN THE FRONTAL CORTEX IN RATS
75
7
27
24
29 FIG. 1.
Learning and reversal of matched sub-groups A l t h o u g h the animals were littermates assigned at r a n d o m to the two groups and although earlier studies using the same m e t h o d of assignment had been s h o w n to produce groups only one point apart o n H e b b - W i l l i a m s Maze scores [14] it still nevertheless remains possible that the r a n d o m assignment had o n this occasion resulted in two u n m a t c h e d groups. Since n o behavioural tests were used to match the t w o
M. A. JEEVES
76
Table 1. M e a n n u m b e r of trials to reach criterion on the initial discrimination (R0) a n d on eight reversals (Rj to Rs)
Frontal g r o u p ( N - - 10) Control g r o u p ( N = 10) Significance on a 2tail t-test
Ro
RI
R2
R3
R4
R5
R6
R7
R8
61
205
245
257
235
205
216
201
180
93
249
323
361
328
307
241
218
227
0.01
N.S.
0.05
0.06
0.06
0.02
N.S.
N.S.
N.S.
~ ~Confrol --o--Frontal 400
( N =lO) ( N =10)
-
~
_200
o
// ,°0.7 0
:
I
I
i
3
2
i
4
I
5
I
6
8
Reversal number
FIG. 2. g r o u p s prior to surgery a n d since as SPERLING [15] suggests there is s o m e evidence in ERLEBACHER'S [16] results to s u p p o r t the view that fast learners are fast reversers, it was clearly essential to e x a m i n e this as a possible explanation of the observed differences. This could be done by selecting f r o m the experimental a n d control g r o u p s two s u b - g r o u p s m a t c h e d on their p e r f o r m a n c e on the initial discrimination learning task. W e could then see whether these m a t c h e d groups deviated on the successive reversals in the s a m e way as the full groups h a d done. It was possible to select five animals f r o m each g r o u p exactly m a t c h e d on trials to criterion on the initial discrimination learning. T h e p e r f o r m a n c e of these s u b - g r o u p s on the eight successive reversals is s h o w n in Fig. 3. It will be seen that the s a m e trend in the data appears when these s u b - g r o u p s are considered alone.
--o--
--Control (N:5) Fronfat (/V:5)
400
g -~_ 3 0 0 u 4? 2 0 0 0 EbIOO
i J
I 2
~, ~
i 4
Reversal
number
FIG. 3.
~
, 6
; :
SOME P A R A D O X I C A L E F F E C T S O F B I L A T E R A L L E S I O N S I N T H E F R O N T A L C O R T E X I N R A T S
77
A measure o f short-term memory In view o f the unexpected direction o f the difference between the two g r o u p s a n d in the light of the e m p h a s i s in m u c h previous work on frontal lobe lesions u p o n a resulting deficit in s h o r t - t e r m m e m o r y it seemed desirable to extract f r o m the data a m e a s u r e which could be expected to reflect a s h o r t - t e r m m e m o r y deficit if this were present. If the result o f the lesions is to m a k e it m o r e difficult for the animal to retrieve information f r o m a short-term store then we m i g h t s u p p o s e that the frontal animals would find it more difficult to learn the initial discrimination a n d m i g h t also be less hindered in the learning o f each reversal by their previous learning t h a n would the controls, a n d would accordingly learn the reversal m o r e quickly. A s regards the first prediction concerning the initial discrimination, the results s h o w that the frontals in fact learned m o r e quickly t h a n the controls. O n e way o f testing the second prediction is to e x a m i n e the error scores m a d e by the two g r o u p s at the start o f each reversal a n d for the first few days after reversal. W h e n we do this we find no suggestion of any consistent difference between the two g r o u p s (see Table 2). It would seem therefore that it is n o t possible to explain the results in terms o f the frontals suffering f r o m a short-term m e m o r y deficit. Evidence for position habits Inspection of the records of individual animals in the two g r o u p s suggested that there m i g h t be a greater tendency in the control g r o u p for animals to go repeatedly to one side o f the apparatus. A s a r o u g h m e a s u r e of this tendency we c a n c o u n t up the n u m b e r of occasions u p o n which animals in the two g r o u p s go to the s a m e side on ten successive trials. If we c o u n t each ten successive responses to one side as one position habit response unit, we find, as Fig. 4 indicates, a greater incidence o f position habits in the
~3 12
~Confrol
II
(,'V=[0)
IO 9 o
8 +-
7 t5
6 5 t3_
4 5 2 I
l
2
5
4
5
6
7
8
Reversol number F[o. 4.
control g r o u p t h a n in the frontal group. W h e n one considers position habit responses o n each reversal separately we find that the two g r o u p s differ at the 5 per cent level only on reversals n u m b e r s 2 a n d 7. This still leaves u n a c c o u n t e d for reversals R3, R4 a n d R5 where the differences between trials to criterion scores for the two g r o u p s are greatest, b u t which do n o t s h o w evidence o f differences in position habit scores. A n o t h e r way o f assessing differences in position habit responses is to c o m p u t e the total n u m b e r of errors each a n i m a l m a k e s to each side a n d then to express the departure f r o m r a n d o m n e s s as a percentage o f the total errors made. T h u s , if En is total errors m a d e to the right, a n d EL is the total errors m a d e to the left, then departure f r o m r a n d o m n e s s is
[En/(ER + EL)] × 100 '~ 50.
M. A. JEEVES
73
t"q tt~
Z
~b
Z e~
Z ~A Z
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Z ~0
.=. .=.
Z Z Z r~
tt~
t--- i
E
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t¢-5
e.i
o
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[..,
9 ~b
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SOME PARADOXICAL EFFECTS OF BILATERAL LESIONS IN THE FRONTAL CORTEX IN RATS
79
These departures from randonmess were computed and are given in Table 3. There is no consistent picture of a significant difference between the experimental and control groups on this measure. Table 3. Position habits to either side in the frontal and control groups given as the mean departure from randomness (50 per cent)
Frontal group ( N = 10) Control group ( N = 10) Significance
R0
R1
R2
g3
R4
R5
R6
R7
R8
11.5
14.9
20.2
30.2
39-5
33.1
36'7
24.8
27.3
9.2 N.S.
21.2 N.S.
40'8 0.01
38.4 N.S.
39-2 N.S.
39-1 N.S.
40.9 N.S.
39.1 0.05
40.0 0.01
Differential rates o f learning In view of the above finding that when computed in one way the control group made mere position habits than the frontal group, it seemed just possible that these position responses could ~e masking a real difference between the two groups in rate of learning when an animal was free from position habit responses. Inspection of individual records made it clear that position habits occurred in the middle of the learning and not at the beginning or the end of each fresh learningto criterion. It may thus have been the case that at the beginning of learning each reversal and towards the end of learning each reversal the control animals may in fact have been learning faster than the frontal group and that the overall scores which included position habits were masking this difference. One way to examine this was to plot the learning curves for the frontal and normal groups and to compare the slopes of the curves at the start of each reversal when inspection had showed that animals were not making position habit responses. The results of doing this are shown in Fig. 5 and it is clear that there were no marked or consistent differences between the two groups.
Frontal
Normal
Frontal
Normal Reversal 5
Reversal
2 I
Reversal 6
o
g6 ~5
Reversal 3
I
I Reversal7
d Z
I
Reversal4
FIG. 5.
Reversal 8
80
M.A. JEEVES Frontal
Normal
Frontol
Normal
A
m
J© [-
O
g~
-o
g
10F
c0
s o "6 d z
IOF
F
8 7 6
-
5
FIG.
6.
Yet another way of studying this is to plot the backward learning curves since, as was said earlier, it is evident from the records that position habits have disappeared in the latter part of the course of learning each reversal. The backward learning curves for the two groups are shown in Fig. 6 and once again there is nothing to suggest that the controls are learning any faster than the frontal group during this position habit free part of their learning. DISCUSSION A t first sight, the m a i n finding o f this experiment that the frontal g r o u p p e r f o r m s at a consistently higher level, t h a t is, takes fewer trials to learn to criterion, than the control g r o u p on d i s c r i m i n a t i o n a n d reversal learning over a n i n e - m o n t h p e r i o d is in c o n t r a s t with m o s t previous w o r k on the b e h a v i o u r a l effects of frontal lesions [3]. The m o s t recent studies which at first sight are at variance with those r e p o r t e d here, are the ones r e p o r t e d by DABROWSKA. H e f o u n d m a r k e d deficits in what he calls reversal learning in frontal rats [17, 18]. However, on close inspection, it is evident t h a t DABROWSKA'S use of the term 'reversal' is different from t h a t o f m o s t other workers. He used a f o u r - u n i t - m a z e with four d o o r s at each choice point. If we label the choice points A, B, C a n d D and the d o o r s at each choice p o i n t 1, 2, 3 a n d 4, then the succession of three tasks which he labels reversals were in fact (1) A4, B2, C3, D1 ; (2) A2, B4, C I , D 3 ; (3) A3, B1, C4, D2. It is evident that there was no real reversal at any stage in the experiment, b u t simply the selection o f a succession o f new paths t h r o u g h the a p p a r a t u s . N o r m a l l y , when we speak o f reversal, we refer to situations in which there is a two choice situation where, when t h r o u g h learning one stimulus has acquired a positive response and the other a negative, we then switch the signs
SOME P A R A D O X I C A L EFFECTS OF B I L A T E R A l . LESIONS 1N T H E F R O N T A L CORTEX IN RATS
8I
of the stimuli so that the positive stimulus becomes negative and the previously negative becomes positive. Since this was clearly not the case in DABROWSKA'S experiments, the superficially conflicting results are in fact, on closer scrutiny, not strictly comparable. There is, on the other hand, some support for the results of the present experiment from three earlier studies. LANDS~LL'S[7] rats with bilateral anterior lesions made at 74-76 days had a mean error score on the Hebb-Williams Maze of 176.5 whereas his control group had a mean error score of 194.0. This looks an appreciable difference although LANDSELLreports that it does not reach the normally accepted level of statistical significance and he attributes the lack of deterioration to the locus of the lesions which did not extend back beyond LASHLEY'S level 9, and not to the size of the lesion. He also comments that the anterior lesion, in rats and humans, does not appear to be important for the efficient solution of simple problems which are not too unfamiliar. This finding of his, is of particular relevance to the present results since in another study to be reported elsewhere [14], we found that both discrimination and reversal learning using the same stimuli and apparatus as in this experiment correlated significantly with performance on the shortened form of the H e b b Williams Maze test suggested by LAVERY and BELANGER [19]. In the recent study reported by GROSS et al. [4] it is of interest that when presenting the results comparing the performance of the control group with the group with bilateral anterior lesions, the histograms show that the lesion group were slightly superior. BOURKE[6] explains his result that frontal lesions produce a deficit in learning a position habit reversal, but not a brightness discrimination reversal, by suggesting that the deficit is only apparent on more difficult problems. On this view, position habit learning is the more difficult problem because it is not solved by external cues and hence shows the deficit whereas the brightness discrimination does not. However, in the present experiment, the task was visual pattern discrimination which, measured in terms of trials required to reach criterion, is certainly a more difficult task for rats than either position or brightness discrimination and therefore presumably according to BOURKE'S line of argument, the frontal group should show a deficit on reversal learning, but they do not. However, if as BOURKEalso suggests spatial habits are likely to be impaired in frontals, then presumably they would be less likely than the controls to entertain or use position habits in the course of learning and this is in line with the finding of fewer position habits amongst frontals than controls. Certainly BOURKE'S general conclusion that "the ability to learn the reversal of any given task does not appear to be necessarily associated with the integrity of the frontal cortex" is supported by our own results. All this, however, is still dodging the most striking aspect of the results, namely, the superior performance of the frontal group, a superiority which is evident over a nine-month
period and only seems to wash out as 'learning to learn' draws the two groups together. How can we explain this ? Several possibilities come to mind. The first, already mentioned in presenting the results, is that there is a deficit in short-term retention, or at least a deficit in recovery of information from what is stored in a short-term store. As we have already indicated this possibility is not supported by a more detailed analysis of the results (see above). The second possibility is that there is no real superiority in rate of learning, but that it only appears so because the mean trials to criterion of the control group is artificially inflated by strong position habits made in the middle of learning each reversal. Again, a closer inspection of rate of learning of individual animals and of different parts of the course of learning fails to support this explanation. Next we may refer back to the suggestions put forward by KRECHEVSKY [20] who concluded that "cortical destruction results in (a) diminishing the number o ~ 'hypotheses' an animal can bring with him to a novel problem
82
M . A . JEgvtis
situation; (b) decreasing the complexity of such 'hypotheses' as are available, and (c) decreasing the plasticity or adaptability of these remaining, relatively simply 'hypotheses'. According to this formulation, we could propose that our control animals are throughout entertaining both more 'hypotheses' and more complex 'hypotheses' so that the number of hypotheses they must search through and try out is greater than the experimental group and they therefore take longer to hit upon the correct hypothesis and hence they learn more slowly. Moreover, following from KRECHEVSKY'Spoint (c) we may suppose that at the start of each reversal because of the frontal groups reduced 'plasticity' they consider relatively 'simple' hypotheses, whereas the controls must again search through a wider repertoire. There is one corollary of this line of argument, namely that although the control group must search through more hypotheses, presumably some will land on the correct one quickly and others only after a long time, and the net result will be a greater variance in the scores of the control group than of the experimental group. When we compute the variances for ['or each group on R0 to R8 we find that three of the variance ratios are significant, using an F test and in the direction expected (Table 4). However, the reversal R 5 with the greatest Table 4. A c o m p a r i s o n of the wtriances of the trials to criterion scores of the frontal a n d control g r o u p s R0
Ri
R2
R3
R4
R5
R6
R7
R8
Frontal g r o u p (N :10) Control group ( N - - I0)
188
10,739
5006
I 1,357
4450
3872
2916
4010
2200
957
6143
8623
14,966
15,507
8912
1988
4284
6719
F ratio
5.1
1.7
1.7
1.3
3.5
2.3
1.5
1- 1
3. I
Significance
0.01
N.S.
N.S.
N.S.
0.05
N.S.
N.S.
N.S.
0.05
difference between groups on trials to criterion (Table l) does not show a significant variance ratio and it thus seems that in fact, a significant difference in variance does not correlate in the expected manner with the differences in scores to criterion in Table I. In short, this explanantion is not supported by the data either. Another possible explanation could suggest with some reason that the task of successively reversing the sign of the positive and negative stimuli eight times would produce considerable frustration in the rats and it could then be argued that the frontal lesions constituted a form of lobotomy having a similar effect to that reported by GONZALEZ and Ross [21], who showed that the administration of chlorpromazine resulted in a relative improvement in reversal performance. The plausibility of an explanation in these terms is strengthened by the results of the study of STREB and SMITH [22]. In their experiment rats were first conditioned to display anxiety in a grill box. it was discovered that the experimental group who had been subjected to frontal lobotomy subsequently displayed fewer of the responses indicative of anxiety than the sham operated controls. They conclude that the common notion that lobotomy tends to abolish anxiety thus receives considerable support. If the response of rats to a situation where every time they have mastered a discrimination learning task the sign of the stimuli is promptly reversed is that it produces anxiety and frustration, then it could well be that the frontal group in our experiment performed better because their anxiety and frustration were both reduced and thus minimised as interfering factors within the course el" learning.
SOME PARADOXICAL EFFECTS OF BILATERAL LESIONS IN THE FRONTAL CORTEX IN RATS
83
A similar hypothesis has been proposed by STAMM [23] in a recent study in which he was able to compare the response to frustration of normal monkeys with that of a group with ablations to the prefrontal cortex. Following AMSEL'S [24] suggestion, he conceptualises frustration as an implicit reaction elicited by non-reward after a number of prior rewards. Thus, in the normal animal, the withholding of a reward after training which leads to the expectation of rewards, results in a frustrative behaviour. In STAMM'S experiment [23] monkeys were first trained on a D R L schedule with a short delay setting so that they obtained a high ratio of rewarded responses. The delay setting was then suddenly lengthened and frustrated responses were elicited following lever presses which had previously been rewarded. In such a situation STAMM found that the monkeys with pre-frontal cortical ablations exhibited lower rates of frustrative responses than the controls. Their behaviour was thus less disrupted and their overall performance was consequently superior to the controls. Such an explanation as that proposed above suggests that it is only in situations where there is clear reversal of stimulus signs and not simply change to a new stimulus that frustration and anxiety will be generated to such an extent as to impair the performance of normal animals as compared with that of fi'ontals. The latter being less prone to frustration will, in fact, perform more efficiently. Applying this to DABROWSKA'S set-up referred to earlier, we see that there the main variable being manipulated was the integration of chains of motor responses, and not frustration, hence the difference between our results and his. SUMMARY The effects of bilateral lesions in the lrontal cortex in rats upon learning a visual discrimination task and then successively reversing the sign of the positive and negative stimuli eight times have been studied. It had been expected that the frontal group would show slower initial and reversal learning than the control group. Instead, the frontal group consistently required fewer trials to reach criterion than the control group. The possibility that this may have been due to an initial sampling error which had resulted in the frontal group being brighter than the control group was discounted by selecting matched subgroups on the initial discrimination. These matched sub-groups still showed the superiority of the frontal group on the successive reversals. A number of possible explanations are advanced, the most plausible being that the effect of frontal lesions is to reduce anxiety and frustration which is otherwise generated in a task in which every time the animal reaches criterion the signs of the stimuli are promptly reversed. This being so, the frontals are less hindered in their learning than the controls whose efficiency is impaired by the anxiety and frustration arising from the successive reversal learning task. Such an explanation finds support from a study by GONZALEZ and Ross [21] with rats and from a recent experiment by STAr,Ira [23] with monkeys. Acknowledgement--The author wishes to acknowledge the help received from several discussions with Dr. ALANCOWEYof the Cambridge Psychological Laboratory in interpreting the results reported here.
REFERENCES 1. RAJALAKSHMI, R . a n d JEEVES, M. A. J. genet. Psychol. 106, 149, 1965.
2. RAJALAKSHMI,R. and JEEVES,M. A. Anita. Behav. 13, 203, 1965.
3. WARREN, J. M. and AKERT, K. (Editors) The Frontal Granular Cortex and Behaviour, McGraw-Hill, New York, 1964. 4. GROSS,C. G., CHOROVER,S. L. and COHEN,S. M. Neuropsychologia 3, 53, 1965. 5. THOMPSON,R. Science, N. ]I. 129, 1223, 1959.
84 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24.
M.A..IFEvtS BOURKE, W. T. J. comp. physiol. Psycho/. 47, 277, 1954. LANDSELL, H. C. J. comp. physiol. Psycho/. 46, 461, 1953. MAHER, B. A. J. comp. physiol. P,wchol. 48, 102, 1955. HUNTER, W. S. and HALL, B. E. J. comp. physio/. Psychol. 32, 253, 1941. LOUCKS, R. B. J. cornp. Neurol. 53, 511, 1931. STELLAR, E., MORGAN, C. T. and YAROSH, M. J. comp. physiol. Psycho/. 34, 107, 1942. JEEVES, M. A. and NORTH, A. L. J. exp. Psycho/. 52, 90, 1956. GELLERMAN,L. W. J. genet. Psychol. 42, 207, 1933. RAJALAKSHMI,R. and JEEVES, M. A. Can. J. P.wchol. (in press). SI'ERLING, S. E. P.tvchol. Bull. 63, 281, 1965. ERLEBACHER,A. J. exp. Psychol. 66, 84, 1963. DABROWSKA,J. Acta Biol. Exper. (Warsaw) 24, (1), 19, 1964. DABROWSKA,J. Acta. Biol. Exper. (Warsaw) 24, (2), 99, 1964. LAVERY,3. J. and BELANGER, D. Can. J. Psychol. 14, 220, 1960. KRECHEVSKY, 1. J. comp. physiol. Psycho/. 19, 425, 1935. GONZALEZ, R. C. and Ross, S. J. comp. physiol. PsychoL 54, 645, 1961. STRER, J, M. and SrvnTZE, K. J. comp. physiol. P.wchoL 48, 126, 1955. STAMM,J. S. Acta Biol. E.vper. (Warsaw) 24 (1), 27. 1964. AMSEL,A. Psycho/. Bull. 55, 102, 1958. R~sum6--Des rats pr6sentant des 16sions bilat6rales du cortex frontal furent entra~n6s ia choisir entre des dessins consistant en bandes horizontales et verticales noires et blanches. La pr6f6rence 6tablie pendant la discrimination initiale fut ensuite renvers6e jusqu'~_ huit fois; c'est-a-dire que si les bandes verticales 6talent positives lors du Renversement R0, les bandes horizontales 1'6taient en Renversement R~, les bandes verticales en Renversement R2, et ainsi de suite. I1 s'est avdr6 que, Iors de la discrimination initiale et pendant chacun des huit renversements successifs, les sujets avec ldsions frontales eurent besoin de moins d'essais pour atteindre le critbre qu'un groupe de contr61e soumis ~_ une op6ration simulde. Des analyses d6tailldes des rdsultats obtenus ont permis de confronter plusieurs explications possibles des diffdrences observ6es. On en conclut que celle qui convient le mieux aux rdsultats actuels, ainsi qu"a ceux d'autres 6tudes comparables, est que l'effet des ldsions frontales consiste ~'t r6duire l'angoisse et l'irritation qui risquent d'etre provoqudes par une fftche dans laquelle, chaque lois que le sujet parvient au crit~re ~?l la suite de telle s6rie de stimuli, les signes de ces stimuli sont aussit6t invers6s.
Zusammenfassung--Ratten, die vorne am O rosshirn operiert worden waren, wurden abgerichtet, zeischen zwei M ustern von horizontalen und vertikalen Schwarzweissstreifen zu unterscheiden. Der Vorzug, welcher wfihrend der ersten Versuchsreihe gegrtindet wurde, wurde dann insgesamt achtmal ins Gegenteil verkehrt, das heisst, wenn bei der Umkehrung R0, die vertikalen Streifen positiv waren, waren bei der Umkehrung Rj die horizontalen die positiven, bei R~ wiedes die vertikalen positiv, u.s.w. Sowohl bei der ersten Lernperiode als auch bei den darauffolgenden Umkehrungen ergab es sich, dass die operierten Ratten weniger Versuche brauchten, um das gestellte Ziel zu erreichen, als die Ratten der Kontrollgruppe welche bloss scheinoperiert waren. Genaue Auswertungen der Resultate erm6glichte einen Vergleich zwischen verschiedenen annehmbaren Erkl/irungen der wahrgenommenen Unterschiede. Die Erkl'arung, die unseren Resultaten und auch anderen, verwandten Studien--am besten zu passen seheint ist diese: die Wirkung der Grosshirnoperation /iussert sich als eine Verringerung der Angst und Frustration, die normalerweise jedesmal hervortreten, wenn ein Versuchstier das gew~inschte Ziel erreicht habend, pl6tzlich seine Zielsetzung ins Gegenteil verkehrt sieht.
SOME PARADOXICAL EFFECTS OF BILATERAL LESIONS IN THE FRONTAL CORTEX IN RATS M. A. JEEVES Department of Psychology, University of Adelaide, S. Australia (Received 6 July 1966)
Abstract--Rats with bilateral lesions of the frontal cortex were trained to discriminate between patterns of horizontal and vertical black and white stripes. The preference established on the initial discrimination learning was then reversed a total of eight times, e.g. if vertical stripes were positive on Reversal R0, horizontal stripes were positive on Reversal RI, vertical stripes on Reversal R2, and so on. On the initial discrimination and each of the eight successive reversals, the frontal animals required fewer trials to reach criterion than a mock operated control group. Detailed analyses of the results enabled a comparison to be made between several possible competing explanations of the observed differences. It is concluded that the explanation which best fits the present results and those of other relevant studies is that the effect of frontal lesions is to reduce the anxiety and frustration which are otherwise generated by a task in which every lime the animal reaches criterion with one set of stimuli, the signs of the stimuli are immediately reversed. THE STUDY r e p o r t e d here is one o f a series designed to investigate the relative sensitivity o f d i s c r i m i n a t i o n a n d reversal learning as measures which m a y reflect structural and developmental changes in the central nervous system [1, 2]. The m a i n object o f the experiment was to study the effects o f bilateral p r e f r o n t a l lesions on the initial learning a n d eight successive reversals o f a visual p a t t e r n discrimination task. By continuing the experiment for eight successive reversals extending over a n i n e - m o n t h period, it was p l a n n e d to investigate the longer term effects o f such lesions in a situation where task difficulty for the a n i m a l is assumed to increase for the first reversals a n d then to steadily decrease as 'learning to learn' begins to take effect. Several p a r t i c i p a n t s (PRIBRAM, p. 145; HARLOW, p. 146) in the 1962 conference on the F r o n t a l G r a n u l a r Cortex a n d Behaviour (WARREN a n d AKERT [3]) expressed the need for c a u t i o n before t o o easily ignoring or attributing to chance factors the finding o f several investigators that frontal lesions either did n o t p r o d u c e b e h a v i o u r a l deficits o r that they might even result in an a p p a r e n t i m p r o v e m e n t in performance. The recent p a p e r by CRoss et al. [4] provides yet a n o t h e r study in which certain types o f frontal lesions fail to p r o d u c e a deficit in a maze learning task, in this case the H e b b - W i l l i a m s Maze. M o r e o v e r an inspection o f their d a t a presented in the form o f a h i s t o g r a m (p. 62) suggests a slightly i m p r o v e d p e r f o r m a n c e following lesions to the anterior cortex. Whilst it is difficult to m a k e exact c o m p a r i s o n s o f the results o f different studies because o f slight differences in such things as the type o f learning task used, the m e t h o d o f r e w a r d e r p u n i s h m e n t given a n d the surgical p r o c e d u r e s employed, it does nevertheless seem reasonable to summarise the m a i n findings from relevant earlier studies with rats by saying that anterior cortical lesions p r o d u c e no observable deficits in learning the following types o f 73
74
M . A . JEEVES
t a s k s : (i) a p o s i t i o n d i s c r i m i n a t i o n [5, 6]; (ii) a b r i g h t n e s s d i s c r i m i n a t i o n [6]; (iii) a b r i g h t n e s s d i s c r i m i n a t i o n r e v e r s a l [6]; (iv) t h e H e b b - W i l l i a m s M a z e [4, 7]. O n tile o t h e r h a n d a n t e r i o r c o r t i c a l l e s i o n s t o p r o d u c e a deficit (i) in p o s i t i o n h a b i t r e v e r s a l l e a r n i n g [6]; (ii) in v i s u a l p a t t e r n d i s c r i m i n a t i o n l e a r n i n g [8] a n d (iii) i n t a s k s w h i c h a r e s a i d t o i n v o l v e s y m b o l i c p r o c e s s e s s u c h as d o u b l e a l t e r n a t i o n [9], d e l a y e d a l t e r n a t i o n [10] a n d l e a r n i n g t o r u n a fixed d i s t a n c e d o w n a m a z e [11]. I n t h e l i g h t o f t h e s e e a r l i e r f i n d i n g s it h a d b e e n o u r e x p e c t a t i o n t h a t w h i l s t t h e a n i m a l s w i t h f r o n t a l l e s i o n s m i g h t b e s o m e w h a t s l o w e r in l e a r n i n g t h e i n i t i a l d i s c r i m i n a t i o n [8] t h e y w o u l d b e a p p r e c i a b l y s l o w e r i n l e a r n i n g t h e first r e v e r s a l . M o r e o v e r t h e a d v e r s e effect o n t h e l e a r n i n g o f t h e r e v e r s a l s w o u l d b e e x p e c t e d t o become greater on the second and possibly third reversal but thereafter the difference might b e e x p e c t e d t o b e r e d u c e d as t a s k difl]culty l e s s e n e d w i t h t h e o n s e t o f ' l e a r n i n g t o l e a r n ' .
METHOD Subjects The S's were twenty naive, male hooded rats 150-days-old at the start of the experiment. They were assigned at random to two equal groups, and housed in individual cages. Throughout the experiment they had water continuously available in their home cages and were fed for 1 hr a day following running in the learning task. Procedure One unit of a discrimination apparatus previously described [12] was used with a start box and a goal box. Two aluminium gates were hinged at the top and either could be locked by placing a nail behind it. The rats were adapted to the apparatus by a series of steps ending with a limited number of forced choices in which grey gates were used. All animals were running freely through the doors at the end of this pretraining. Immediately the pretraining was completed all animals were operated upon. Surgery was performed under intraperitoneal nembutal anaesthesia. An incision was made in the mid-line of the scalp. The fascia were removed, the coronal suture was identified and two burr holes were made with a dental drill 3 mm anterior to the coronal suture and 0.5 mm either side of the mid-line. The lesions were made by placing the positive electrode through the burr hole, piercing the meninges and lowering the electrode approximately 0.5 mm into the cortex. The other electrode was placed in the right hind leg. A current of 3mA at 600V d.c. was passed for 10 sec. This was then repeated in the other hemisphere. Because of the electro-cauterising effects of such lesions there was little bleeding. If it were a control animal the same procedure was adopted as far as making two small burr holes in the skull but no electrodes were placed in the cortex and no current was passed. In both cases the incision was dusted with antibiotic powder and closed with Michel clips which were usually removed five days post-operatively. After a recovery period of I0 days the animals were again run in the maze with grey doors to renew their acquaintance with the apparatus. The experiment proper was then begun using stimuli of horizontal and vertical black and white stripes matched for brightness. In both groups half the animals began with horizontal and hall' with vertical stripes as the positive stimulus in the initial discrimination learning task. The patterns were changed from right to left in accordance with the randomized sequence devised by GELLERMAN [13]. Selfcorrection of errors was permitted. An error was defined as touching a gate with the nose. In the goal box S was allowed a few seconds to eat before being returned to the start box. Each animal was run for ten trials a day for 7 days a week. As soon as an animal made 18 out of 20 correct responses on two successive days, the signs of the stimuli were reversed on the following day and the procedure continued until criterion was again reached when the signs of the stimuli were again reversed until eight successive reversals had been learned to criterion. The animals were then sacrificed under nembutal anaesthesia and their brains were perfused with saline solution and formalin. The brains were embedded in wax and stained with methyl blue. Examination of serial sections of the brains at a separation of 40/t, allowed reconstruction of the lesions which are shown diagrammatically in Fig. 1. RESULTS General rate of" learnh~g and reversal The frontal group (E) required fewer trials to reach criterion on the original discrimination learning and on each of the eight successive reversals than the control group (C). These results are presented graphically in Fig. 2 and an inspection of Table 1 shows that on the first discrimination (R0) and on reversals mnnbers 2, 3, 4 and 5 these differences were significant at better than the 6 ~ level using a t test.
SOME PARADOXICALEFFECTSOF BILATERAL LESIONSIN THE FRONTAL CORTEX IN RATS
75
7
27
24
29 FIG. 1.
Learning and reversal of matched sub-groups A l t h o u g h the animals were littermates assigned at r a n d o m to the two groups and although earlier studies using the same m e t h o d of assignment had been s h o w n to produce groups only one point apart o n H e b b - W i l l i a m s Maze scores [14] it still nevertheless remains possible that the r a n d o m assignment had o n this occasion resulted in two u n m a t c h e d groups. Since n o behavioural tests were used to match the t w o
M. A. JEEVES
76
Table 1. M e a n n u m b e r of trials to reach criterion on the initial discrimination (R0) a n d on eight reversals (Rj to Rs)
Frontal g r o u p ( N - - 10) Control g r o u p ( N = 10) Significance on a 2tail t-test
Ro
RI
R2
R3
R4
R5
R6
R7
R8
61
205
245
257
235
205
216
201
180
93
249
323
361
328
307
241
218
227
0.01
N.S.
0.05
0.06
0.06
0.02
N.S.
N.S.
N.S.
~ ~Confrol --o--Frontal 400
( N =lO) ( N =10)
-
~
_200
o
// ,°0.7 0
:
I
I
i
3
2
i
4
I
5
I
6
8
Reversal number
FIG. 2. g r o u p s prior to surgery a n d since as SPERLING [15] suggests there is s o m e evidence in ERLEBACHER'S [16] results to s u p p o r t the view that fast learners are fast reversers, it was clearly essential to e x a m i n e this as a possible explanation of the observed differences. This could be done by selecting f r o m the experimental a n d control g r o u p s two s u b - g r o u p s m a t c h e d on their p e r f o r m a n c e on the initial discrimination learning task. W e could then see whether these m a t c h e d groups deviated on the successive reversals in the s a m e way as the full groups h a d done. It was possible to select five animals f r o m each g r o u p exactly m a t c h e d on trials to criterion on the initial discrimination learning. T h e p e r f o r m a n c e of these s u b - g r o u p s on the eight successive reversals is s h o w n in Fig. 3. It will be seen that the s a m e trend in the data appears when these s u b - g r o u p s are considered alone.
--o--
--Control (N:5) Fronfat (/V:5)
400
g -~_ 3 0 0 u 4? 2 0 0 0 EbIOO
i J
I 2
~, ~
i 4
Reversal
number
FIG. 3.
~
, 6
; :
SOME P A R A D O X I C A L E F F E C T S O F B I L A T E R A L L E S I O N S I N T H E F R O N T A L C O R T E X I N R A T S
77
A measure o f short-term memory In view o f the unexpected direction o f the difference between the two g r o u p s a n d in the light of the e m p h a s i s in m u c h previous work on frontal lobe lesions u p o n a resulting deficit in s h o r t - t e r m m e m o r y it seemed desirable to extract f r o m the data a m e a s u r e which could be expected to reflect a s h o r t - t e r m m e m o r y deficit if this were present. If the result o f the lesions is to m a k e it m o r e difficult for the animal to retrieve information f r o m a short-term store then we m i g h t s u p p o s e that the frontal animals would find it more difficult to learn the initial discrimination a n d m i g h t also be less hindered in the learning o f each reversal by their previous learning t h a n would the controls, a n d would accordingly learn the reversal m o r e quickly. A s regards the first prediction concerning the initial discrimination, the results s h o w that the frontals in fact learned m o r e quickly t h a n the controls. O n e way o f testing the second prediction is to e x a m i n e the error scores m a d e by the two g r o u p s at the start o f each reversal a n d for the first few days after reversal. W h e n we do this we find no suggestion of any consistent difference between the two g r o u p s (see Table 2). It would seem therefore that it is n o t possible to explain the results in terms o f the frontals suffering f r o m a short-term m e m o r y deficit. Evidence for position habits Inspection of the records of individual animals in the two g r o u p s suggested that there m i g h t be a greater tendency in the control g r o u p for animals to go repeatedly to one side o f the apparatus. A s a r o u g h m e a s u r e of this tendency we c a n c o u n t up the n u m b e r of occasions u p o n which animals in the two g r o u p s go to the s a m e side on ten successive trials. If we c o u n t each ten successive responses to one side as one position habit response unit, we find, as Fig. 4 indicates, a greater incidence o f position habits in the
~3 12
~Confrol
II
(,'V=[0)
IO 9 o
8 +-
7 t5
6 5 t3_
4 5 2 I
l
2
5
4
5
6
7
8
Reversol number F[o. 4.
control g r o u p t h a n in the frontal group. W h e n one considers position habit responses o n each reversal separately we find that the two g r o u p s differ at the 5 per cent level only on reversals n u m b e r s 2 a n d 7. This still leaves u n a c c o u n t e d for reversals R3, R4 a n d R5 where the differences between trials to criterion scores for the two g r o u p s are greatest, b u t which do n o t s h o w evidence o f differences in position habit scores. A n o t h e r way o f assessing differences in position habit responses is to c o m p u t e the total n u m b e r of errors each a n i m a l m a k e s to each side a n d then to express the departure f r o m r a n d o m n e s s as a percentage o f the total errors made. T h u s , if En is total errors m a d e to the right, a n d EL is the total errors m a d e to the left, then departure f r o m r a n d o m n e s s is
[En/(ER + EL)] × 100 '~ 50.
M. A. JEEVES
73
t"q tt~
Z
~b
Z e~
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Z ~0
.=. .=.
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SOME PARADOXICAL EFFECTS OF BILATERAL LESIONS IN THE FRONTAL CORTEX IN RATS
79
These departures from randonmess were computed and are given in Table 3. There is no consistent picture of a significant difference between the experimental and control groups on this measure. Table 3. Position habits to either side in the frontal and control groups given as the mean departure from randomness (50 per cent)
Frontal group ( N = 10) Control group ( N = 10) Significance
R0
R1
R2
g3
R4
R5
R6
R7
R8
11.5
14.9
20.2
30.2
39-5
33.1
36'7
24.8
27.3
9.2 N.S.
21.2 N.S.
40'8 0.01
38.4 N.S.
39-2 N.S.
39-1 N.S.
40.9 N.S.
39.1 0.05
40.0 0.01
Differential rates o f learning In view of the above finding that when computed in one way the control group made mere position habits than the frontal group, it seemed just possible that these position responses could ~e masking a real difference between the two groups in rate of learning when an animal was free from position habit responses. Inspection of individual records made it clear that position habits occurred in the middle of the learning and not at the beginning or the end of each fresh learningto criterion. It may thus have been the case that at the beginning of learning each reversal and towards the end of learning each reversal the control animals may in fact have been learning faster than the frontal group and that the overall scores which included position habits were masking this difference. One way to examine this was to plot the learning curves for the frontal and normal groups and to compare the slopes of the curves at the start of each reversal when inspection had showed that animals were not making position habit responses. The results of doing this are shown in Fig. 5 and it is clear that there were no marked or consistent differences between the two groups.
Frontal
Normal
Frontal
Normal Reversal 5
Reversal
2 I
Reversal 6
o
g6 ~5
Reversal 3
I
I Reversal7
d Z
I
Reversal4
FIG. 5.
Reversal 8
80
M.A. JEEVES Frontal
Normal
Frontol
Normal
A
m
J© [-
O
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-o
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10F
c0
s o "6 d z
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8 7 6
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6.
Yet another way of studying this is to plot the backward learning curves since, as was said earlier, it is evident from the records that position habits have disappeared in the latter part of the course of learning each reversal. The backward learning curves for the two groups are shown in Fig. 6 and once again there is nothing to suggest that the controls are learning any faster than the frontal group during this position habit free part of their learning. DISCUSSION A t first sight, the m a i n finding o f this experiment that the frontal g r o u p p e r f o r m s at a consistently higher level, t h a t is, takes fewer trials to learn to criterion, than the control g r o u p on d i s c r i m i n a t i o n a n d reversal learning over a n i n e - m o n t h p e r i o d is in c o n t r a s t with m o s t previous w o r k on the b e h a v i o u r a l effects of frontal lesions [3]. The m o s t recent studies which at first sight are at variance with those r e p o r t e d here, are the ones r e p o r t e d by DABROWSKA. H e f o u n d m a r k e d deficits in what he calls reversal learning in frontal rats [17, 18]. However, on close inspection, it is evident t h a t DABROWSKA'S use of the term 'reversal' is different from t h a t o f m o s t other workers. He used a f o u r - u n i t - m a z e with four d o o r s at each choice point. If we label the choice points A, B, C a n d D and the d o o r s at each choice p o i n t 1, 2, 3 a n d 4, then the succession of three tasks which he labels reversals were in fact (1) A4, B2, C3, D1 ; (2) A2, B4, C I , D 3 ; (3) A3, B1, C4, D2. It is evident that there was no real reversal at any stage in the experiment, b u t simply the selection o f a succession o f new paths t h r o u g h the a p p a r a t u s . N o r m a l l y , when we speak o f reversal, we refer to situations in which there is a two choice situation where, when t h r o u g h learning one stimulus has acquired a positive response and the other a negative, we then switch the signs
SOME P A R A D O X I C A L EFFECTS OF B I L A T E R A l . LESIONS 1N T H E F R O N T A L CORTEX IN RATS
8I
of the stimuli so that the positive stimulus becomes negative and the previously negative becomes positive. Since this was clearly not the case in DABROWSKA'S experiments, the superficially conflicting results are in fact, on closer scrutiny, not strictly comparable. There is, on the other hand, some support for the results of the present experiment from three earlier studies. LANDS~LL'S[7] rats with bilateral anterior lesions made at 74-76 days had a mean error score on the Hebb-Williams Maze of 176.5 whereas his control group had a mean error score of 194.0. This looks an appreciable difference although LANDSELLreports that it does not reach the normally accepted level of statistical significance and he attributes the lack of deterioration to the locus of the lesions which did not extend back beyond LASHLEY'S level 9, and not to the size of the lesion. He also comments that the anterior lesion, in rats and humans, does not appear to be important for the efficient solution of simple problems which are not too unfamiliar. This finding of his, is of particular relevance to the present results since in another study to be reported elsewhere [14], we found that both discrimination and reversal learning using the same stimuli and apparatus as in this experiment correlated significantly with performance on the shortened form of the H e b b Williams Maze test suggested by LAVERY and BELANGER [19]. In the recent study reported by GROSS et al. [4] it is of interest that when presenting the results comparing the performance of the control group with the group with bilateral anterior lesions, the histograms show that the lesion group were slightly superior. BOURKE[6] explains his result that frontal lesions produce a deficit in learning a position habit reversal, but not a brightness discrimination reversal, by suggesting that the deficit is only apparent on more difficult problems. On this view, position habit learning is the more difficult problem because it is not solved by external cues and hence shows the deficit whereas the brightness discrimination does not. However, in the present experiment, the task was visual pattern discrimination which, measured in terms of trials required to reach criterion, is certainly a more difficult task for rats than either position or brightness discrimination and therefore presumably according to BOURKE'S line of argument, the frontal group should show a deficit on reversal learning, but they do not. However, if as BOURKEalso suggests spatial habits are likely to be impaired in frontals, then presumably they would be less likely than the controls to entertain or use position habits in the course of learning and this is in line with the finding of fewer position habits amongst frontals than controls. Certainly BOURKE'S general conclusion that "the ability to learn the reversal of any given task does not appear to be necessarily associated with the integrity of the frontal cortex" is supported by our own results. All this, however, is still dodging the most striking aspect of the results, namely, the superior performance of the frontal group, a superiority which is evident over a nine-month
period and only seems to wash out as 'learning to learn' draws the two groups together. How can we explain this ? Several possibilities come to mind. The first, already mentioned in presenting the results, is that there is a deficit in short-term retention, or at least a deficit in recovery of information from what is stored in a short-term store. As we have already indicated this possibility is not supported by a more detailed analysis of the results (see above). The second possibility is that there is no real superiority in rate of learning, but that it only appears so because the mean trials to criterion of the control group is artificially inflated by strong position habits made in the middle of learning each reversal. Again, a closer inspection of rate of learning of individual animals and of different parts of the course of learning fails to support this explanation. Next we may refer back to the suggestions put forward by KRECHEVSKY [20] who concluded that "cortical destruction results in (a) diminishing the number o ~ 'hypotheses' an animal can bring with him to a novel problem
82
M . A . JEgvtis
situation; (b) decreasing the complexity of such 'hypotheses' as are available, and (c) decreasing the plasticity or adaptability of these remaining, relatively simply 'hypotheses'. According to this formulation, we could propose that our control animals are throughout entertaining both more 'hypotheses' and more complex 'hypotheses' so that the number of hypotheses they must search through and try out is greater than the experimental group and they therefore take longer to hit upon the correct hypothesis and hence they learn more slowly. Moreover, following from KRECHEVSKY'Spoint (c) we may suppose that at the start of each reversal because of the frontal groups reduced 'plasticity' they consider relatively 'simple' hypotheses, whereas the controls must again search through a wider repertoire. There is one corollary of this line of argument, namely that although the control group must search through more hypotheses, presumably some will land on the correct one quickly and others only after a long time, and the net result will be a greater variance in the scores of the control group than of the experimental group. When we compute the variances for ['or each group on R0 to R8 we find that three of the variance ratios are significant, using an F test and in the direction expected (Table 4). However, the reversal R 5 with the greatest Table 4. A c o m p a r i s o n of the wtriances of the trials to criterion scores of the frontal a n d control g r o u p s R0
Ri
R2
R3
R4
R5
R6
R7
R8
Frontal g r o u p (N :10) Control group ( N - - I0)
188
10,739
5006
I 1,357
4450
3872
2916
4010
2200
957
6143
8623
14,966
15,507
8912
1988
4284
6719
F ratio
5.1
1.7
1.7
1.3
3.5
2.3
1.5
1- 1
3. I
Significance
0.01
N.S.
N.S.
N.S.
0.05
N.S.
N.S.
N.S.
0.05
difference between groups on trials to criterion (Table l) does not show a significant variance ratio and it thus seems that in fact, a significant difference in variance does not correlate in the expected manner with the differences in scores to criterion in Table I. In short, this explanantion is not supported by the data either. Another possible explanation could suggest with some reason that the task of successively reversing the sign of the positive and negative stimuli eight times would produce considerable frustration in the rats and it could then be argued that the frontal lesions constituted a form of lobotomy having a similar effect to that reported by GONZALEZ and Ross [21], who showed that the administration of chlorpromazine resulted in a relative improvement in reversal performance. The plausibility of an explanation in these terms is strengthened by the results of the study of STREB and SMITH [22]. In their experiment rats were first conditioned to display anxiety in a grill box. it was discovered that the experimental group who had been subjected to frontal lobotomy subsequently displayed fewer of the responses indicative of anxiety than the sham operated controls. They conclude that the common notion that lobotomy tends to abolish anxiety thus receives considerable support. If the response of rats to a situation where every time they have mastered a discrimination learning task the sign of the stimuli is promptly reversed is that it produces anxiety and frustration, then it could well be that the frontal group in our experiment performed better because their anxiety and frustration were both reduced and thus minimised as interfering factors within the course el" learning.
SOME PARADOXICAL EFFECTS OF BILATERAL LESIONS IN THE FRONTAL CORTEX IN RATS
83
A similar hypothesis has been proposed by STAMM [23] in a recent study in which he was able to compare the response to frustration of normal monkeys with that of a group with ablations to the prefrontal cortex. Following AMSEL'S [24] suggestion, he conceptualises frustration as an implicit reaction elicited by non-reward after a number of prior rewards. Thus, in the normal animal, the withholding of a reward after training which leads to the expectation of rewards, results in a frustrative behaviour. In STAMM'S experiment [23] monkeys were first trained on a D R L schedule with a short delay setting so that they obtained a high ratio of rewarded responses. The delay setting was then suddenly lengthened and frustrated responses were elicited following lever presses which had previously been rewarded. In such a situation STAMM found that the monkeys with pre-frontal cortical ablations exhibited lower rates of frustrative responses than the controls. Their behaviour was thus less disrupted and their overall performance was consequently superior to the controls. Such an explanation as that proposed above suggests that it is only in situations where there is clear reversal of stimulus signs and not simply change to a new stimulus that frustration and anxiety will be generated to such an extent as to impair the performance of normal animals as compared with that of fi'ontals. The latter being less prone to frustration will, in fact, perform more efficiently. Applying this to DABROWSKA'S set-up referred to earlier, we see that there the main variable being manipulated was the integration of chains of motor responses, and not frustration, hence the difference between our results and his. SUMMARY The effects of bilateral lesions in the lrontal cortex in rats upon learning a visual discrimination task and then successively reversing the sign of the positive and negative stimuli eight times have been studied. It had been expected that the frontal group would show slower initial and reversal learning than the control group. Instead, the frontal group consistently required fewer trials to reach criterion than the control group. The possibility that this may have been due to an initial sampling error which had resulted in the frontal group being brighter than the control group was discounted by selecting matched subgroups on the initial discrimination. These matched sub-groups still showed the superiority of the frontal group on the successive reversals. A number of possible explanations are advanced, the most plausible being that the effect of frontal lesions is to reduce anxiety and frustration which is otherwise generated in a task in which every time the animal reaches criterion the signs of the stimuli are promptly reversed. This being so, the frontals are less hindered in their learning than the controls whose efficiency is impaired by the anxiety and frustration arising from the successive reversal learning task. Such an explanation finds support from a study by GONZALEZ and Ross [21] with rats and from a recent experiment by STAr,Ira [23] with monkeys. Acknowledgement--The author wishes to acknowledge the help received from several discussions with Dr. ALANCOWEYof the Cambridge Psychological Laboratory in interpreting the results reported here.
REFERENCES 1. RAJALAKSHMI, R . a n d JEEVES, M. A. J. genet. Psychol. 106, 149, 1965.
2. RAJALAKSHMI,R. and JEEVES,M. A. Anita. Behav. 13, 203, 1965.
3. WARREN, J. M. and AKERT, K. (Editors) The Frontal Granular Cortex and Behaviour, McGraw-Hill, New York, 1964. 4. GROSS,C. G., CHOROVER,S. L. and COHEN,S. M. Neuropsychologia 3, 53, 1965. 5. THOMPSON,R. Science, N. ]I. 129, 1223, 1959.
84 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24.
M.A..IFEvtS BOURKE, W. T. J. comp. physiol. Psycho/. 47, 277, 1954. LANDSELL, H. C. J. comp. physiol. Psycho/. 46, 461, 1953. MAHER, B. A. J. comp. physiol. P,wchol. 48, 102, 1955. HUNTER, W. S. and HALL, B. E. J. comp. physio/. Psychol. 32, 253, 1941. LOUCKS, R. B. J. cornp. Neurol. 53, 511, 1931. STELLAR, E., MORGAN, C. T. and YAROSH, M. J. comp. physiol. Psycho/. 34, 107, 1942. JEEVES, M. A. and NORTH, A. L. J. exp. Psycho/. 52, 90, 1956. GELLERMAN,L. W. J. genet. Psychol. 42, 207, 1933. RAJALAKSHMI,R. and JEEVES, M. A. Can. J. P.wchol. (in press). SI'ERLING, S. E. P.tvchol. Bull. 63, 281, 1965. ERLEBACHER,A. J. exp. Psychol. 66, 84, 1963. DABROWSKA,J. Acta Biol. Exper. (Warsaw) 24, (1), 19, 1964. DABROWSKA,J. Acta. Biol. Exper. (Warsaw) 24, (2), 99, 1964. LAVERY,3. J. and BELANGER, D. Can. J. Psychol. 14, 220, 1960. KRECHEVSKY, 1. J. comp. physiol. Psycho/. 19, 425, 1935. GONZALEZ, R. C. and Ross, S. J. comp. physiol. PsychoL 54, 645, 1961. STRER, J, M. and SrvnTZE, K. J. comp. physiol. P.wchoL 48, 126, 1955. STAMM,J. S. Acta Biol. E.vper. (Warsaw) 24 (1), 27. 1964. AMSEL,A. Psycho/. Bull. 55, 102, 1958. R~sum6--Des rats pr6sentant des 16sions bilat6rales du cortex frontal furent entra~n6s ia choisir entre des dessins consistant en bandes horizontales et verticales noires et blanches. La pr6f6rence 6tablie pendant la discrimination initiale fut ensuite renvers6e jusqu'~_ huit fois; c'est-a-dire que si les bandes verticales 6talent positives lors du Renversement R0, les bandes horizontales 1'6taient en Renversement R~, les bandes verticales en Renversement R2, et ainsi de suite. I1 s'est avdr6 que, Iors de la discrimination initiale et pendant chacun des huit renversements successifs, les sujets avec ldsions frontales eurent besoin de moins d'essais pour atteindre le critbre qu'un groupe de contr61e soumis ~_ une op6ration simulde. Des analyses d6tailldes des rdsultats obtenus ont permis de confronter plusieurs explications possibles des diffdrences observ6es. On en conclut que celle qui convient le mieux aux rdsultats actuels, ainsi qu"a ceux d'autres 6tudes comparables, est que l'effet des ldsions frontales consiste ~'t r6duire l'angoisse et l'irritation qui risquent d'etre provoqudes par une fftche dans laquelle, chaque lois que le sujet parvient au crit~re ~?l la suite de telle s6rie de stimuli, les signes de ces stimuli sont aussit6t invers6s.
Zusammenfassung--Ratten, die vorne am O rosshirn operiert worden waren, wurden abgerichtet, zeischen zwei M ustern von horizontalen und vertikalen Schwarzweissstreifen zu unterscheiden. Der Vorzug, welcher wfihrend der ersten Versuchsreihe gegrtindet wurde, wurde dann insgesamt achtmal ins Gegenteil verkehrt, das heisst, wenn bei der Umkehrung R0, die vertikalen Streifen positiv waren, waren bei der Umkehrung Rj die horizontalen die positiven, bei R~ wiedes die vertikalen positiv, u.s.w. Sowohl bei der ersten Lernperiode als auch bei den darauffolgenden Umkehrungen ergab es sich, dass die operierten Ratten weniger Versuche brauchten, um das gestellte Ziel zu erreichen, als die Ratten der Kontrollgruppe welche bloss scheinoperiert waren. Genaue Auswertungen der Resultate erm6glichte einen Vergleich zwischen verschiedenen annehmbaren Erkl/irungen der wahrgenommenen Unterschiede. Die Erkl'arung, die unseren Resultaten und auch anderen, verwandten Studien--am besten zu passen seheint ist diese: die Wirkung der Grosshirnoperation /iussert sich als eine Verringerung der Angst und Frustration, die normalerweise jedesmal hervortreten, wenn ein Versuchstier das gew~inschte Ziel erreicht habend, pl6tzlich seine Zielsetzung ins Gegenteil verkehrt sieht.