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Improved instrumental learning in neodecorticate rats
Physiology & Behavior, Vol. 24, pp. 357-366. PergamonPress and BrainResearch Publ., 1980. Printedin the U.S.A.
Improved Instrumental Learning in Neodecorticate Rats D A V I D A. O A K L E Y 1'~
M R C Unit on N e u r a l M e c h a n i s m s o f Behaviour, 3 Malet Place, London, W C I E 7JG England R e c e i v e d 4 April 1979 OAKLEY, D. A. Improved instrumental learning in neodecorticate rats. PHYSIOL. BEHAV. 24(2) 357-366, 1980.--The first experiment describes the improvement in instrumental learned behaviour which can be achieved by pretraining in rats surgically deprived of neocortex. The pretraining consisted of allowing the animal to learn in gradual steps to attend to and manipulate a chain for a food reward which was delivered to a food tray some distance from the chain itself. Following this pretraining the neodecorticates were able to progress to operating the chain up to 60 times for a single reward and distributed their behaviour between the chain and the food tray in the same way as normal animals. Without pretraining neodecorticated rats have previously not shown such high levels of performance and have failed to separate the instrumental response and the reward directed components of their behaviour. In a second experiment the source of conflict between reward oriented behaviours and the instrumental response itself was removed by allowing the animal to make its instrumental responses to the food tray door. Again normal levels of performance were seen in the neodecorticated animal. It is concluded that neocortex is not a prerequisite for efficient instrumental learned performance even when a particular response must be repeated many times for a single reward. The possibility that the neodecorticate initially has difficulty in identifying or paying attention to the object to be manipulated in this type of situation and so, unless appropriately pretrained, fails to separate reward oriented behaviours from the instrumental response, is discussed. Neocortex Food reward
Decortication Attention
Rat Instrumental learning Operant conditioning Fixed ratio schedules Remedial training Manipulandum identification Response topography
CONTRARY to prior expectations [1, 17,28] instrumental learning has recently been demonstrated for food and other rewards in the absence of neocortex in cats [2], in rats [11, 16, 25] and in rabbits [14, 15, 23, 24], though when electric shock is used, neodecorticate learning in instrumental situations appears to be unstable [5] or absent [2, 3, 6, 16]. In instrumental learning situations which demand that the animal perform a particular response, such as pressing a bar or treadle, several times before receiving a single food reward neodecorticates are slow to learn, are inefficient and cease to work in the apparatus when the response demand exceeds between four and eight responses per reward [23, 24, 25]. It has previously been suggested that this is due to a failure on the part of the neodecorticate to identify the part of the apparatus to be manipulated (bar or treadle) and to distinguish it from the source of food reward [15, 24, 25]. This, it was argued, leads to inefficiency in neodecorticates because behaviours appropriate to collecting food reward intrude upon the instrumental bar or treadle pressing response. Consistent with an interpretation of this sort is the observation that neodecorticated rabbits which had received pretraining intended to increase their awareness or identification of a re-
sponse treadle, via a series of response reversals in a twotreadle apparatus, were subsequently able to work as efficiently as normal animals even when the response demands were as high as 60 treadle responses per food reward [15]. Prior experience of unrelated experimental procedures, such as Pavlovian nictitating membrane conditioning, which would not be expected to aid the neodecorticate in identifying the response treadle, did not have the same beneficial effect on subsequent treadle pressing performance [23]. EXPERIMENT 1 Previous studies using neodecorticate rats [25] have shown that neither prior experience of other instrumental learning situations nor of GO-NOGO learning to a houselight cue in the same apparatus was effective in improving subsequent performance in situations where a fixed number of responses is required of the animal per reinforcement (reward). Reward or reinforcement schedules of this sort are referred to as Fixed Ratio schedules. Where one response is required per reinforcement the schedule is a Fixed Ratio One (or FR1), where two responses are required per reinforce-
1Present address: Department of Psychology and Centre for Neuroscience, University College London, Gower Street, London WC 1E 6BT, England. 21 am grateful to Dr. Hannah Knuth for testing the animals and helping with the data analysis for Experiment 1, to Sarah Morgan for testing the animals in Experiment 2, to Mary Oakley for analysing the kymograph records, to Alison Hogg for preparing the histological material, to Mr. C. Cromarty for help in preparing the illustrations, and to Julie Steele for typing the manuscript.
C o p y r i g h t © 1980 B r a i n R e s e a r c h P u b l i c a t i o n s Inc.--0031-9384/80/020357-10502.00/0
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was anticipated that a procedure of" this son would ensure that the animal had correctly identified the manipulandum m isolation from contextual cues and would -dso servc~ it, enhance the distinction between the manipulandum and the food tray. If, as suggested, the neodecorticate's deficit on FR schedules is due to inadequate manipulandum identification, pretraining of this sort should reduce the likelihood that responses appropriate to retrieving food (food Hay responses) will intrude upon the instrumental response. This in turn should be reflected in normal levels of instrumental performance by the neodecorticates and a normal distribution of manipulandum oriented vs reward (food trayi oriented behaviors.
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• M E T H O D
Subjects and Surgery
Food tray Relay'~/
The subjects were four neodecorticate and four normal rats (male, Hooded Lister) with a mean body weight of 292•5 (SD _+ 14.2) g prior to surgery. The neodecortications were produced in two stages with 8-9 weeks between stages. Neodecortication was achieved by removing pia from the surface of the hemisphere, thereby devascularizing it and causing cortical necrosis [13, 16, 22]. The normal animals were sham operated and received two 5 mm dia. trephine holes over parietal cortex with 7-9 weeks between operations. All surgery was carried out under pentobarbitone sodium (Sagatal) anaesthesia and all animals had I 1-24 weeks of postoperative recovery. Table 1 summarizes interoperative and postoperative intervals, lesion size and order of lesioning for all subjects.
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FIG. I. The operant conditioning box. Above: View of end wall from inside the box. Below: Plan view. For clarity the wire mesh floor is indicated at bottom fight only. i-vii=changes in length and height of response bar during the early stages of bar press training (manipulandum identification pretraining). The chain was attached to the response bar in positions vi and vii but to simplify the figure is shown in position vii only.
ment the schedule is a Fixed Ratio Two (FR2), and so forth. The first experiment investigates whether pretraining designed to draw the animal's attention to the manipulandum (i.e., that part of the apparatus which is to be manipulated) results in the same improvement in instrumental FR performance in neodecorticated rats as that described for neodecorticated rabbits [15]. The pretraining procedure selected for this purpose was one in which the animal was required to identify and respond to a manipulandum which was moved progressively further from the vicinity of the food tray into which food reinforcement was delivered. It
The training box measured 18x24 cm with 17 cm high walls and was placed inside a sound attenuating chamber inside a soundproofed room at some distance from the electromechanical programming equipment• There was no illumination within the box. The manipulandum was a 6 mm dia. brass bar situated as shown in Fig. 1 on the side wall to the left of the food tray. The bar could be varied from 10 cm to 6.5 cm to 3 cm in length (i-iii in Fig. 1) and could also be raised, via a slot in the side wall, in 2.5 cm steps from its original position 5 cm above the grid floor of the box to a final position 15 cm above the box floor (iii-vii in Fig. 1). In positions vi and vii a 4 cm length of flexible chain consisting of 8 linked, chromium plated balls (3 mm dia.) was attached to the end of the 3 cm bar. The instrumental response was any behaviour by the animals which resulted in a downward movement of the manipulandum (approximately equivalent to 10 g on the 3 cm bar) sufficient to operate a switch contact. Each successful response was accompanied by a click from a nearby relay. The tray opening measured 6x4 cm. This aperature was fitted with a top-hung transparent door of 1.6 mm thick Perspex, which closed it except for a 4 mm gap at the bottom. Reinforcement consisted of Noyes food reward pellets (45 nag) dispensed automatically to the food tray• The delivery of reinforcement was signalled by the sound of the dispenser operating and the noise caused by the food pellet landing in the tray. The main recording system was a Gerbrands cumulative recorder at a paper speed of 5 ram/rain and a kymograph with a paper speed of 136 ram/rain, which was used alongside the cumulative recorder on some sessions to monitor responses to the bar, tray door movements, and delivery of reinforcement along a common timebase. A
NEOCORTEX AND L E A R N I N G
359
5D
28D FIG. 3. Coronal sections showing, in black, the tissue loss common to all four neodecorticates used in Experiment 1. The heavily dotted areas indicate tissue loss in at least one animal.
37D
42D
FIG. 2. Reconstructions of the brains of the four neodecorticated rats used in Experiment 1. Surface extent of the lesion is shown in black. The rhinal fissure is shown as a solid black or dashed white line running parallel to the ventral outline in the lateral views of each brain.
set of three counters recorded number of manipulandum movements, number of reinforcements, and tray door openings during each experimental session for each subject.
Feeding Schedule All animals were removed from ad lib feeding 2-3 days before tray feeding commenced and were given 10 g of Noyes pellets per day in the home cage. Once training had started all animals received sufficient standard diet (41B) after each session to stabilize their body weights at approximately 80% of their free-feeding values.
the tray door was progressively lowered to its fully closed position (tray door training). Bar press training continued under the FR1 schedule through the stages shown as ii to vii in Fig. 1 and as described in the apparatus section. This constituted manipulandum identification pretraining. Once an animal was operating the bar + chain in position vii, the FR value was raised in single steps to FR8 (8 responses per food pellet), in double responses steps between FR8 and FR20 and 2, 3, or 5 response steps thereafter to FR60 (60 responses per food pellet). The number of sessions given to each animal at each step and the size of the steps at higher FR values were determined by the stability of that animal's performance. Sessions lasted for approximately 30 min or until 60 reinforcements had been delivered, whichever was sooner.
Histology When testing was complete all animals received a lethal dose of pentobarbitone sodium anaesthetic followed by intracardiac perfusion with physiological saline and then 10% formol saline. Brains were removed, photographed, and embedded in paraffin wax. Coronal sections were cut at 15/~ thickness and every 17th section was stained with cresyl violet and mounted under glass. The lesions were drawn from the prepared sections onto a series of standard coronal sections and were then reconstructed individually onto an outline drawing of dorsal and lateral aspects of a normal rat brain. Estimates of lesion size were obtained by perimetry from the series of coronal sections.
Statistical Analyses Unless noted otherwise, between group statistical analysis was based on Mann-Whitney U tests [30] and within-group trends were evaluated using Page's L test [26].
Tray Feeding and Bar Press Training On the first day of tray feeding each animal was placed in the training box for 15 min with 60 Noyes pellets in the food tray and with the food tray door held open. This was followed by 4 daily sessions with the long (10 cm) bar in place in its lowest position (i in Fig. 1) on an FR1 schedule (one bar response per food reward pellet). During these four sessions
RESULTS
Histology Surface reconstructions of the brains of all five lesioned animals used in this experiment are shown in Fig. 2. Figure 3 is a set of nine standard coronal sections showing the area common to all lesions and their range. The small amount of
360
( )A K i •] TABLE 1 SHOWING INTEROPERATIVEINTERVALS, POSTOPERATIVEINTERVALS. LESION SIZES AND ORDER OF LESION1NGFOR ALL SUBJECTS lnteroperative* interval (weeks)
Posloperative+ interval {weeks)
%$ Lesion
Order of~ lesion
Neodecorticate 5D 28D 37D 42D
8 9 9 8
14 18 11 24
99.9 99.2 99.7 99.8
L-R L-R L-R R-L
Normal 18N 49N 5IN 53N
7 9 9 9
14 18 11 23
d
L-R L-R L-R L-R
*Interval in weeks between two stages of hemidecortication in the neodecorticates and between two sham operations in the normal group. tlnterval in weeks between the final operation and the first day of testing. ~:Lesion size expressed as a percentage of total neocortex removed. §Order in which left (L) and right (R) sided hemidecortication or sham operations were performed. neocortical sparing present in these brains (see Table 1) was predominantly anterior, adjacent to the rhinal fissure. Transitional cortex was invaded in all brains along the rhinal fissure, particularly caudally, and in midline regions. Postoperative degenerative changes had removed all cortical tissue below the devascularized surface of the hemisphere and in the majority of cases associated white matter, including the corpus callosum, had also disappeared (see Fig. 4). Ventricular expansion was evident in all lesioned brains resulting in lateral displacement of caudate/putamen. Hippocampus was less frequently displaced and neither set of structures showed signs of damage. No other evidence of subcortical changes was seen in the lesioned brains and no neocortical or other neural changes were found in the sham operated animals as a result of trephining.
Postoperative Recovery When training commenced all animals were selfmaintaining on laboratory diet and plain water. The neodecorticates were easy to handle and showed no obvious behavioural abnormalities when observed in their home cages, though grooming was sometimes less effectively performed than in normals. The stabilized ad lib body weights of the neodecorticate animals (347.8 + 19.9 g) and the normals (425.8 + 13.9 g) differed significantly immediately prior to the food deprivation procedures (N~=N2=4, U=0, p = ×0.014). This is consistent with earlier incidental observations of lower set-points for body weight in neodeeorticate rabbits [14, 15, 20, 21, 23] and with Braun's more formal observations in the neodecorticate rat [4]. FIG. 4. Dorsal and lateral views of a sample neodecorticate brain showing complete postoperative degeneration of devascularized neocortex and associated white matter. Ventricular expansion and integrity of hippocampus and other subcortical structures are evident in both views. The isolated strip of tissue in the dorsal midline region is transitional cortex, beneath which the corpus callosum has degenerated. The background in both parts of the figure is marked in 1 cm squares.
Bar Press Training All animals received 4 daily sessions with the long plain bar in the low position (stage 1) combined with tray door training. The transition from this condition to the short bar + chain in the high position (stages ii-vii) was completed in between 8 and 10 sessions in all animals except one
NEOCORTEX
AND LEARNING
361 TABLE 2
SHOWING MEAN ( _+ SD) OVERALL RESPONSE RATES AND RUNNING RESPONSE RATES IN RESPONSES PER MINUTE, AND POST-REINFORCEMENT PAUSE DURATIONS IN SECONDS FOR NORMAL AND NEODECORTICATE RATS UNDER FOUR FIXED RATIOS Within group* trend
FR 10
FR20
FR40
FR60
1) Overall response rate Normal Neodecorticate Between groupst
34.2 _+ 12.1 22.4 _ 4.3 p =0.029
51.5 ___ 12.9 24.7 _ 10.7 p =0.029
64.7 _+ 19.2 20.4 _ 4.4 p=0.014
75.9 _ 11.5 23.2 _+ 4.6 p =0.014
L = l l 6 , p<0.01 L=106, NS
2) Running response rate Normal Neodecorticate Between groupst
63.0 _ 23.7 46.2 + 12.1 NS
78.5 _+ 18.3 51.9 _+ 14.8 p =0.029
92.7 _+ 30.2 41.9 _+ 6.0 p=0.014
101.7 _+ 15.7 44.3 _+_ 7.6 p =0.014
L=l13, p<0.05 L=I01, NS
3) Post-reinforcement pause Normal Neodecorticate Between groupst
8.7 ± 3.8 13.7 ___ 6.2 NS
8.7 _+ 3.8 30.4 _+ 15.5 p=0.014
11.6 _+ 2.7 64.0 _+ 28.2 p=0.014
12.3 _+ 2.9 77.0 _+ 21.8 p =0.014
L = l 1 2 , p<0.05 L = l l 9 , p<0.01
These data are based on kymograph recordings. *L test, k=4, n = 4 in all cases. t U test Nl=N2=4 in all cases.
TABLE 3 SHOWING MEAN ( -+ SD) TRAY/REINFORCEMENT RATIOS IN NORMAL AND NEODECORTICATE RATS UNDER FIVE FIXED RATIOS
Normal Neodecorticate Between groupst
FR 1
FR 10
FR20
FR40
FR60
2.0 ___ 1.6 3.4 _ 2.3 NS
2.5 _+ 0.7 6.5 + 1.9 p=0.014
2.6 --_ 0.6 5.1 ± 1.4 p=0.014
2.9 _+ 0.7 5.1 _+ 1.5 NS
3.0 _+ 0.6 3.8 _+ 1.8 NS
Within group* t re nd L = 196 NS L=186 NS
These data are expressed as the number of food tray responses per reinforcement. *L test, k=5, n = 4 in all cases. t U test, NZ=N2=4 in all cases.
n e o d e c o r t i c a t e (28D) w h i c h r e q u i r e d 30 s e s s i o n s . R e s p o n s e r a t e s o n FR1 at t h e e n d o f this p e r i o d o f m a n i p u l a n d u m i d e n t i f i c a t i o n p r e t r a i n i n g w e r e n o t significantly different in the t w o g r o u p s ( N o r m a l s 8.7, S D --- 4.2 r e s p o n s e s p e r minute; N e o d e c o r t i c a t e s 5.0, ---2.5 r e s p o n s e s p e r minute). Raising t h e F i x e d R a t i o s c h e d u l e f r o m FR1 w i t h t h e b a r + c h a i n in p o s i t i o n vii to F R 6 0 r e q u i r e d 31.8 (SD ___ 8.2) s e s s i o n s in t h e n e o d e c o r t i c a t e s a n d 32.5 (-+7.0) s e s s i o n s in the n o r m a l a n i m a l s . T h e s e m e a n s are n o t significantly different. A s t h e r e i n f o r c e m e n t ratio w a s r a i s e d o n t h e b a r + c h a i n m a n i p u l a n d u m to FR60, b o t h n o r m a l s a n d n e o d e c o r t i c a t e s c o n t i n u e d to r e s p o n d b u t w i t h n o r m a l r e s p o n s e r a t e s b e c o m ing i n c r e a s i n g l y h i g h e r t h a n t h o s e o f t h e n e o d e c o r t i c a t e s f r o m F R 1 0 o n w a r d s (see overafi r e s p o n s e r a t e s in T a b l e 2). In n o r m a l s t h e i n c r e a s e in m a n i p u l a n d u m r e s p o n s e r a t e s as t h e F R v a l u e w a s r a i s e d w a s significant w h e r e a s t h e o v e r a l l r e s p o n s e r a t e s in t h e n e o d e c o r t i c a t e s s h o w e d n o significant i n c r e a s e o r d e c r e a s e as the F R v a l u e c h a n g e d . Overall res p o n s e r a t e s are relatively g r o s s i n d i c e s o f p e r f o r m a n c e , h o w e v e r , a n d so a n a n a l y s i s w a s m a d e of p o s t r e i n f o r c e m e n t
pause duration and running response rates. The postreinf o r c e m e n t p a u s e w a s d e f i n e d as the first b r e a k in regular r e s p o n d i n g following r e i n f o r c e m e n t a n d the r u n n i n g r e s p o n s e rate w a s c a l c u l a t e d as the rate of r e s p o n d i n g in the period between the postreinforcement pause and the next r e i n f o r c e m e n t . T h e d a t a o b t a i n e d for r u n n i n g r e s p o n s e r a t e s f o l l o w e d quite closely t h o s e a l r e a d y d e s c r i b e d for overall r e s p o n s e r a t e s e x c e p t t h a t t h e r e w a s n o significant d i f f e r e n c e in r u n n i n g r e s p o n s e rate b e t w e e n n o r m a l a n d n e o d e c o r t i c a t e g r o u p s at FR10 (see T a b l e 2). I n c r e a s i n g F R s are n o r m a l l y a c c o m p a n i e d b y a n i n c r e a s e in p o s t r e i n f o r c e m e n t p a u s e dur a t i o n [8] a n d significant t r e n d s in this d i r e c t i o n are e v i d e n t in b o t h g r o u p s , t h o u g h t h e t r e n d is s t r o n g e r in n e o d e c o r t i c a t e s t h a n in n o r m a l s (see T a b l e 2). A t all F R v a l u e s a b o v e F R 1 0 p o s t r e i n f o r c e m e n t p a u s e s w e r e significantly l o n g e r in n e o d e c o r t i c a t e s t h a n in n o r m a l s . S a m p l e c u m u l a t i v e r e c o r d s for all eight a n i m a l s at FR10, FR20, F R 4 0 a n d F R 6 0 are g i v e n in Fig. 5. T a b l e 3 s h o w s t h e efficiency o f tray r e l a t e d b e h a v i o u r for b o t h g r o u p s as n u m b e r o f t r a y e n t r i e s p e r r e i n f o r c e m e n t re-
362
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FR40
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lOminutes
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DECORTICAT E
(bar) response distributions in the two group~ arc ai~o vc markably similar, with a brief overshoot of responses im mediately after reinforcement R 1 followed by a perked oi io~ response probability, corresponding to the postfeinforcc ment pause, which is followed in turn by the response ~am leading to reinforcement at R2 (see Fig. 6). The steeper stope to the bar response run profile in the neodecorticates in Fig. 6 reflects the generally longer and more variable duration postreinforcement pauses in that group, especially at higher FRs.
/
/ /
NORMAL
FIG. 5. Sample cumulative records for all eight animals in Experiment 1 at FR10, FR20, FR40 and FR60. On these records a horizontal line indicates a pause in responding, vertical movements of the recording pen indicate repeated bar responding and the small diagonal marks show the point at which a food pellet reward was given. Cessation of responding commonly seen following delivery of food reward is the postreinforcement pause. These are particularly clear as long horizontal sections in the neodecorticate FR60 records. The almost vertical section of the record following the postreinforcement pause is the response run used in calculating the 'running' response rate. At each FR value the records, reading from left to right, were obtained from animals 5D, 28D, 37D, 42D, 18N, 49N, 51N and 53N, respectively.
ceived. The normal animals consistently produced lower mean tray/reinforcement ratios than neodecorticates but this difference was significant only at FR10 and FR20. The temporal distribution of both manipulandum and tray door responses in the interval between consecutive reinforcements is illustrated in Fig. 6, from which it is clear that the supernumerary tray responses in the neodecorticates were concentrated in the period immediately following reinforcement as are the tray responses of normal animals. Manipulandum
All neodecorticate and all normal animals successfidly completed the long, low bar to high bar + chain training sequence which was intended to serve as a form of manipulandum identification pretraining. In terms of the aims stated in the introduction this pretraining achieved its purpose and all animals went on to perform efficiently on FR60 schedules. These results thus confirm those previously reported for rabbits with manipulandum identification pretraining [15] and suggest that the pretraining effect is not speciesspecific. In addition to this general confirmation it is worth noting the following detailed similarities between the results obtained from the two species when pretrained animals are tested on FR schedules: (1) overall and local response rates were higher in the normal animals, especially at high FRs; (2) postreinforcement pauses increased in duration as FR values increased in both normals and nondecorticates: (3) the postreinforcement pauses were longer in neodecorticates than in normal animals: (4) tray/reinforcement ratios were slightly higher in the neodecorticates but not significantly so at the completion of FR training: (5) the distribution of tray responses and manipulandum responses in the interval between consecutive reinforcements were identical in normals and neodecorticates. Rats [251 and rabbits [231 without manipulandum identification pretraining, on the other hand, show an upper limit to their performance around FR4-10 and high levels of tray behaviour which persist throughout the interreinforcement period and give rise to enormous tray/reinforcement ratios. It would appear, therefore, that the bar + chain pretraining is effective in preventing both these effects and enables neodecorticate rats to perform as efficiently as normal animals on high Fixed Ratios insofar as response topography is concerned. The only substantial difference between normal and lesioned groups which was detected in this study was in the lower rate of maniputandum operation in the lesioned animals. This was due in part to longer postreinforcement pauses in this group but also to generally lower running response rates. EXPERIMENT 2 If the neodecorticate's inefficiency in bar and treadle pressing situations on FR schedules is due at least in part to a failure to separate manipulandum (bar or treadle) related behaviours from those associated with the food tray 115,24t, pretraining directed at enhancing manipulandum identification is only one of several possible ways of overcoming the lesioned animal's deficit. If, for example, the tray door itself were to be used as the manipulandum on a FR schedule any conflict between these two sets of behaviours should be eliminated and decorticate performance should be improved. This second experiment investigates FR performance in a naive neodecorticate rat using the food tray door as the manipulandum.
NEOCORTEX
AND LEARNING
363
NORMAL
DECORTICATE
2 >:
40 0
A
u,
55-2 set
-
24.9sec
-
-
FR 40
z B
1
FR 60
: FR.60 300
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-
R2
dl
R2
Rl
INTER-REINFORCEMENT
INTERVAL
FIG. 6. Distribution of food tray and bar+chain
manipulandum responses within the interreinforcement interval at FRIO, FR20, FR40 and FR60 in four neodecorticate and four normal rats in Experiment 1. Each set of histograms is based on 10 consecutive reinforcements at the stated FR value for each of the four animals in the group. The mean interval between consecutive reinforcements is shown in seconds beneath each pair of histograms. Rl =reinforcement. R2=subsequent reinforcement. These data are based on kymograph recordings.
METHOD
Subjects
The subjects were one normal and one neodecorticated male, Hooded Lister rat. The lesioned rat weighed 268 g
prior to surgery. Neodecortication stage as described in Experiment
was performed
in one
1 and 9 weeks were allowed for recovery. Neither animal had prior experience in any experimental apparatus.
)AKI . I
364
TABLE 4 MEAN RUNNING RESPONSE RAI'E IN RESPONSES PER MINUTE ( _~ SD) AND MEAN POST-REINFORCEMENT PAUSE DURATIONS IN SECONDS ( _+ SI)) FOR ONE NORMAL AND ONF NEODECORTICATE RAT UNDER FOUR FIXED RATIOS USING A FOOD TRAY DOOR MANIPULANDUM
1) Running response rate Normal Neodecorticate
FR 10
FR20
FR40
FR60
105.8 z 42.6 115.3 ~ 52.4
87.7 + 24.4 149.2 + 93.0
77.6 _+ 15.4 99.2 ± 15.2
70.1 ± 15.1 89.9 ± 10.7
7.2 ± 7.3 9.0 :t: 6.6
10.2 ± 10.9 7.2 + 4.6
16.2 _+ 16.3 9.6 ± 4.9
32.4 ± 33.1 16.2 + t8.3
2) Post-reinforcement pause Normal Neodecorticate
These data are based on the first 20 reinforcements of the final session at each FR value.
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t
1
tray d o o r was held completely open and was gradually closed on later sessions until, after 4 sessions, both rats were reliably pushing the tray door open to retrieve the pellets in the tray. An FR1 schedule was then introduced so that a response pulse was generated and a pellet delivered to the food tray each time the tray d o o r was opened and then closed. The ratio of d o o r m o v e m e n t s to reinforcements was then increased from F R I (one d o o r press per food reward pellet) to FR60 (60 d o o r presses per pellet) in both animals on the following schedule, in which the F R value is shown followed by the number o f daily sessions in brackets. F R I 112); FR2 (!); FR3 (1); F R 4 (18); FR5 (1); F R 6 (1); FR8 (1); F R I 0 (17); FR12 (1); FR15 (1); FR17 (1); FR20 (3); FR25 (I); FR30 (1); FR35 (1); FR40 (1); FR45 (1); FR50 (2); FR55 (1); FR60 (4). Up to FR8 each session consisted of 90 reinforcements and from FR10 onwards 60 reinforcements were given per session.
I
RESULTS
Histology Reconstruction of the brain of the neodecorticate showed that 89.9% of total n e o c o r t e x had been r e m o v e d , with the major neocortical sparings occurring laterally adjacent to the rhinal fissure. S o m e damage to retrosplenial areas of cingulate cortex was present in both hemispheres. No subcortical damage was seen.
f NORMAL I
1
1
1
I
t
I
I
;
I
I
1
I
I
I
I
I
I
I
I
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I
I
I
I
I
FIG. 7. Sample cumulative records for one normal and one neodecorticate rat with a tray door manipulandum in Experiment 2. The baseline for each half of the figure is marked in 1 min intervals.
Apparattts The apparatus was as described in E x p e r i m e n t 1 except that no response bar was present.
Tray Feeding and Door-Push Training Both animals were reduced to 85-90% of normal body weight by regular daily feeding. Preliminary training consisted of allowing the animal to eat 20 r e i n f o r c e m e n t pellets per daily session from the food tray. On the first session the
I
Fixed Ratio Training Both animals continued to operate the tray d o o r manipulandum reliably at all F R values and, as Fig. 7 shows, the cumulative records they p r o d u c e d w e r e remarkably similar. Both animals p r o d u c e d longer p o s t r e i n f o r c e m e n t pauses as the F R was increased to FR60 (Table 4). Mean running response rates, h o w e v e r , showed a t e n d e n c y to reduce in value in both animals as the F R increased (Table 4). Whilst it would be inappropriate to draw firm conclusions from data based on only two animals it is interesting to note that the neodecorticate in this experiment p r o d u c e d faster running response rates and shorter p o s t r e i n f o r c e m e n t pauses than the normal, which is the c o n v e r s e of the o u t c o m e in Experiment 1 using a bar + chain manipulandum. DISCUSSION On the basis of this one neodecorticate rat it would appear
NEOCORTEX AND L E A R N I N G
365
that normal levels of performance on FR schedules can be achieved without pretraining if the manipulandum is not separated from the source of food. The FR schedule itself does not therefore seem to be a problem for the neodecorticate rat. The results is generally consistent with the notion that the neodecorticate is impaired in its ability to identify and respond discretely to separate elements in its environment. G E N E R A L DISCUSSION The results of these two experiments are in general support of the view that neodecorticated mammals are not impaired in their ability to form learned associations in instrumental situations where some manipulandum, such as a movable bar or treadle, must be operated for food reward. Their difficulty seems to lie more in identifying and responding selectively to separate elements in their environment, in particular the manipulandum and the food tray. One consequence of this inability is the neodecorticate's tendency to interrupt its manipulandum responding with inappropriate food tray oriented behaviours. Under these conditions instrumental performance is inefficient and the behaviour breaks down if more than 4--8 manipulandum responses are required for each food reward. These deficits are still evident if the neodecorticates have had prior experience of Pavlovian nictitating membrane conditioning [23], of different instrumental responses [25] of GO-NO GO training to a houselight cue [25] and unsuccessful reversal training using the
same manipulandum [15]. When, on the other hand, pretraining which was designed to increase the neodecorticate's identification of a particular manipulandum was employed, subsequent instrumental performance was highly efficient, food tray responses were normally distributed and distinct from manipulandum responses and performance was sustained even if the response requirement was raised to 60 manipulandum responses for each food reward. Pretraining procedures having this remedial effect are successful reversal training on the same manipulandum [15] and training on a distinct and progressively more distant manipulandum (Experiment 1 of this study). Removing the conflict between the manipulandum and food tray behaviours similarly produced highly efficient and normal looking instrumental performance in a neodecorticate, in this case by making the manipulandum and the food tray components synergistic. (Experiment 2 of this study). Pavlovian conditioning has already been shown to be reliably mediated outside neocortex in the mammalian brain [18, 19, 20, 21, 22]. Insofar as the behavior described in neodecorticate rats in the present study can be attributed to instrumental learning and not to implicit Pavlovian processes such as those involved in autoshaping or signtracking [7, 9, 10, 12, 29], the present results are inconsistent with earlier beliefs that instrumental learning in mammals is dependent on neocortex [I, 2, 6, 23, 27, 28]. The question of the likely neurological substrate of Paviovian conditioning and instrumental learning in the light of recent neodecortication studies is considered in more detail elsewhere [17].
REFERENCES 1. Berlucchi, G. and H. A. Buchtei. Some trends in the neurological study of learning. In: Handbook of Psychobiology, edited by M. S. Gazzaniga and C. Blakemore. London: Academic Press, 1975, pp. 481-497. 2. Bjursten, L.-M., K. Norrsell and U. Norrsell. Behavioural repertory of cats without cerebral cortex from infancy. Expl Brain Res. 25: 115-130, 1976. 3. Bloch, S. and I. Lagarrigue. Cardiac and simple avoidance learning in neodecorticate rats. Physiol. Behav. 3: 305-308, 1968. 4. Braun, J. J. Neocortex and feeding behaviour in the rat. J. cornp, physiol. Psychol. 89: 507-522, 1975. 5. Bromiley, R. B. Conditioned responses in a dog after removal of neocortex. J. comp. physiol. Psychol. 41: 102-110, 1948. 6. DiCara, L. V., J. J. Braun and B. A. Pappas. Classical conditioning and instrumental learning of cardiac and gastrointestinal responses following removal of neocortex in the rat. J. comp. physiol. Psychol. 73: 208-216, 1970. 7. Dickinson, A. and N. J. Mackintosh. Classical conditioning in animals. Ann. Rev. Psychol. 29: 587-612, 1978. 8. Felton, M. and D. O. Lyon. The post-reinforcement pause. J. exp. Analysis Behav. 9: 131-134, 1966. 9. Hearst, E. Pavlovian conditioning and directed movements. In: The Psychology of Learning and Motivation. Vol. 9, edited by G. H. Bower. New York: Academic Press, 1975, pp. 215-262.
10. Hearst, E. and H. M. Jenkins. Sign-tracking: The StimulusreinJbrcer Relation and Directed Action. Austin, Texas: The Psychonomic Society, 1974. 11. Huston, J. P. and A. A. Borbrly. The thalamic rat: General behaviour, operant learning with rewarding hypothalamic stimulation, and effects of amphetamine. Physiol. Behav. 12: 433-448, 1974. 12. Jenkins, H. M. Sensitivity of different response systems to stimulus-reinforcer and response-reinforcer relations. In: Operant-Pavlovian Interaction, edited by H. Davis and H. M. B. Hurwitz. Hillsdale, New Jersey: Lawrence Erlbaum Associates, 1977, pp. 47-66. 13. Meyer, P. M. and D. R. Meyer. Neurosurgical procedures with special reference to aspiration lesions. In: Methods in Psychobiology. Vol. 1. edited by R. D. Myers. London: Academic Press, 1971, pp. 91-130. 14. Oakley, D. A. Instrumental learning in neodecorticate rabbits. Nature (New Biol.) 233: 185-187, 1971. 15. Oakley, D. A. Instrumental reversal learning and subsequent Fixed Ratio performance on simple and GO-NOGO schedules in neodecorticate rabbits. Physiol. Psychol. 7: 2%42, 1979a. 16. Oakley, D. A. Learning with food reward and shock avoidance in neodecorticate rats. Expl Neurol. 63: 627-642, 1979b.
17. Oakley, D. A. Cerebral cortex and adaptive behaviour. In: Brain. Behaviour and Ev~;lution, edited by D. A. Oakley and H. C. Plotkin. London: Methuen, 1979c, pp. 154-188. 18. Oakley, D. A. and I, S. Russell. Neocortical lesions and PavlovJan conditioning. Physiol. Behav. 8: 915-926, 1972. 19. Oakley, D. A. and 1. S. Russell. Differential and reversai conditioning in partially neodecorticate rabbits, l'hv~iol. Behav. 13: 221-230, 1974. 20. Oakley, D. A. and I. S. Russell. Role of cortex in Pavlovian discrimination learning. Physiol. Behav. 15:315-321, 1975. 21, Oakley, D. A. and I. S. Russell. Subcortical nature of Pavlovian differentiation in the rabbit. Physiol. Behav. 17: 947-954, 1976. 22, Oakley, D. A. and I. S. Russell. Subcortical storage of Pavlovian conditioning in the rabbit. Physiol. Beha r. 18:931-937, 1977. 23. Oakley, D. A. and I. S. Russell. Performance of neodecorticared rabbits in a free-operant situation. Physiol. Behav. 20: 157-170, 1978a. 24. Oakley, D. A. and 1. S. Russell. Manipulandum identification in operant behaviour in neodecorticate rabbits. Physical. Behav. 21: 943-950, 1978b.
25. Oakley, D. A. and 1. S. Russell. Instrumental learning on l'ixcd Ratio and GO-NOGO schedules in neodecor~icate rats. Br,;i, Res. 161: 356-360, 1979. 26. Page, E. B. Ordered hypotheses for multiple treatmems: ,~ significance test for linear ranks..I. Am. ~s~l~/,; ,~,', 58:216230, 1963. 27. Russell, I. S. Animal learning and memory. In: ..Lsi~(,(t~ ,!1 Learninx, and Memory, edited by D. Richter. London: Heinemann, 1966, pp. 121-171. 28. Russell, 1. S. Neurological basis of complex learning. Bt. W~.d. Bull. 27: 278-285, 1971. 29. Schwartz, B. and E. Gamzu. Pavlovian control of operant behavior. In: Handbook o f Operant Behavior, edited by W. K. Honig and J. E. R. Staddon. Englewood Cliffs, New Jersey: Prentice Hall, 1977, pp. 53-97. 30. Siegel, S. Nonparametric Statistic.Llbr the Behavioral Sctctt~ e~'. New York: McGraw-Hill, 1956.
Improved Instrumental Learning in Neodecorticate Rats D A V I D A. O A K L E Y 1'~
M R C Unit on N e u r a l M e c h a n i s m s o f Behaviour, 3 Malet Place, London, W C I E 7JG England R e c e i v e d 4 April 1979 OAKLEY, D. A. Improved instrumental learning in neodecorticate rats. PHYSIOL. BEHAV. 24(2) 357-366, 1980.--The first experiment describes the improvement in instrumental learned behaviour which can be achieved by pretraining in rats surgically deprived of neocortex. The pretraining consisted of allowing the animal to learn in gradual steps to attend to and manipulate a chain for a food reward which was delivered to a food tray some distance from the chain itself. Following this pretraining the neodecorticates were able to progress to operating the chain up to 60 times for a single reward and distributed their behaviour between the chain and the food tray in the same way as normal animals. Without pretraining neodecorticated rats have previously not shown such high levels of performance and have failed to separate the instrumental response and the reward directed components of their behaviour. In a second experiment the source of conflict between reward oriented behaviours and the instrumental response itself was removed by allowing the animal to make its instrumental responses to the food tray door. Again normal levels of performance were seen in the neodecorticated animal. It is concluded that neocortex is not a prerequisite for efficient instrumental learned performance even when a particular response must be repeated many times for a single reward. The possibility that the neodecorticate initially has difficulty in identifying or paying attention to the object to be manipulated in this type of situation and so, unless appropriately pretrained, fails to separate reward oriented behaviours from the instrumental response, is discussed. Neocortex Food reward
Decortication Attention
Rat Instrumental learning Operant conditioning Fixed ratio schedules Remedial training Manipulandum identification Response topography
CONTRARY to prior expectations [1, 17,28] instrumental learning has recently been demonstrated for food and other rewards in the absence of neocortex in cats [2], in rats [11, 16, 25] and in rabbits [14, 15, 23, 24], though when electric shock is used, neodecorticate learning in instrumental situations appears to be unstable [5] or absent [2, 3, 6, 16]. In instrumental learning situations which demand that the animal perform a particular response, such as pressing a bar or treadle, several times before receiving a single food reward neodecorticates are slow to learn, are inefficient and cease to work in the apparatus when the response demand exceeds between four and eight responses per reward [23, 24, 25]. It has previously been suggested that this is due to a failure on the part of the neodecorticate to identify the part of the apparatus to be manipulated (bar or treadle) and to distinguish it from the source of food reward [15, 24, 25]. This, it was argued, leads to inefficiency in neodecorticates because behaviours appropriate to collecting food reward intrude upon the instrumental bar or treadle pressing response. Consistent with an interpretation of this sort is the observation that neodecorticated rabbits which had received pretraining intended to increase their awareness or identification of a re-
sponse treadle, via a series of response reversals in a twotreadle apparatus, were subsequently able to work as efficiently as normal animals even when the response demands were as high as 60 treadle responses per food reward [15]. Prior experience of unrelated experimental procedures, such as Pavlovian nictitating membrane conditioning, which would not be expected to aid the neodecorticate in identifying the response treadle, did not have the same beneficial effect on subsequent treadle pressing performance [23]. EXPERIMENT 1 Previous studies using neodecorticate rats [25] have shown that neither prior experience of other instrumental learning situations nor of GO-NOGO learning to a houselight cue in the same apparatus was effective in improving subsequent performance in situations where a fixed number of responses is required of the animal per reinforcement (reward). Reward or reinforcement schedules of this sort are referred to as Fixed Ratio schedules. Where one response is required per reinforcement the schedule is a Fixed Ratio One (or FR1), where two responses are required per reinforce-
1Present address: Department of Psychology and Centre for Neuroscience, University College London, Gower Street, London WC 1E 6BT, England. 21 am grateful to Dr. Hannah Knuth for testing the animals and helping with the data analysis for Experiment 1, to Sarah Morgan for testing the animals in Experiment 2, to Mary Oakley for analysing the kymograph records, to Alison Hogg for preparing the histological material, to Mr. C. Cromarty for help in preparing the illustrations, and to Julie Steele for typing the manuscript.
C o p y r i g h t © 1980 B r a i n R e s e a r c h P u b l i c a t i o n s Inc.--0031-9384/80/020357-10502.00/0
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was anticipated that a procedure of" this son would ensure that the animal had correctly identified the manipulandum m isolation from contextual cues and would -dso servc~ it, enhance the distinction between the manipulandum and the food tray. If, as suggested, the neodecorticate's deficit on FR schedules is due to inadequate manipulandum identification, pretraining of this sort should reduce the likelihood that responses appropriate to retrieving food (food Hay responses) will intrude upon the instrumental response. This in turn should be reflected in normal levels of instrumental performance by the neodecorticates and a normal distribution of manipulandum oriented vs reward (food trayi oriented behaviors.
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• M E T H O D
Subjects and Surgery
Food tray Relay'~/
The subjects were four neodecorticate and four normal rats (male, Hooded Lister) with a mean body weight of 292•5 (SD _+ 14.2) g prior to surgery. The neodecortications were produced in two stages with 8-9 weeks between stages. Neodecortication was achieved by removing pia from the surface of the hemisphere, thereby devascularizing it and causing cortical necrosis [13, 16, 22]. The normal animals were sham operated and received two 5 mm dia. trephine holes over parietal cortex with 7-9 weeks between operations. All surgery was carried out under pentobarbitone sodium (Sagatal) anaesthesia and all animals had I 1-24 weeks of postoperative recovery. Table 1 summarizes interoperative and postoperative intervals, lesion size and order of lesioning for all subjects.
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FIG. I. The operant conditioning box. Above: View of end wall from inside the box. Below: Plan view. For clarity the wire mesh floor is indicated at bottom fight only. i-vii=changes in length and height of response bar during the early stages of bar press training (manipulandum identification pretraining). The chain was attached to the response bar in positions vi and vii but to simplify the figure is shown in position vii only.
ment the schedule is a Fixed Ratio Two (FR2), and so forth. The first experiment investigates whether pretraining designed to draw the animal's attention to the manipulandum (i.e., that part of the apparatus which is to be manipulated) results in the same improvement in instrumental FR performance in neodecorticated rats as that described for neodecorticated rabbits [15]. The pretraining procedure selected for this purpose was one in which the animal was required to identify and respond to a manipulandum which was moved progressively further from the vicinity of the food tray into which food reinforcement was delivered. It
The training box measured 18x24 cm with 17 cm high walls and was placed inside a sound attenuating chamber inside a soundproofed room at some distance from the electromechanical programming equipment• There was no illumination within the box. The manipulandum was a 6 mm dia. brass bar situated as shown in Fig. 1 on the side wall to the left of the food tray. The bar could be varied from 10 cm to 6.5 cm to 3 cm in length (i-iii in Fig. 1) and could also be raised, via a slot in the side wall, in 2.5 cm steps from its original position 5 cm above the grid floor of the box to a final position 15 cm above the box floor (iii-vii in Fig. 1). In positions vi and vii a 4 cm length of flexible chain consisting of 8 linked, chromium plated balls (3 mm dia.) was attached to the end of the 3 cm bar. The instrumental response was any behaviour by the animals which resulted in a downward movement of the manipulandum (approximately equivalent to 10 g on the 3 cm bar) sufficient to operate a switch contact. Each successful response was accompanied by a click from a nearby relay. The tray opening measured 6x4 cm. This aperature was fitted with a top-hung transparent door of 1.6 mm thick Perspex, which closed it except for a 4 mm gap at the bottom. Reinforcement consisted of Noyes food reward pellets (45 nag) dispensed automatically to the food tray• The delivery of reinforcement was signalled by the sound of the dispenser operating and the noise caused by the food pellet landing in the tray. The main recording system was a Gerbrands cumulative recorder at a paper speed of 5 ram/rain and a kymograph with a paper speed of 136 ram/rain, which was used alongside the cumulative recorder on some sessions to monitor responses to the bar, tray door movements, and delivery of reinforcement along a common timebase. A
NEOCORTEX AND L E A R N I N G
359
5D
28D FIG. 3. Coronal sections showing, in black, the tissue loss common to all four neodecorticates used in Experiment 1. The heavily dotted areas indicate tissue loss in at least one animal.
37D
42D
FIG. 2. Reconstructions of the brains of the four neodecorticated rats used in Experiment 1. Surface extent of the lesion is shown in black. The rhinal fissure is shown as a solid black or dashed white line running parallel to the ventral outline in the lateral views of each brain.
set of three counters recorded number of manipulandum movements, number of reinforcements, and tray door openings during each experimental session for each subject.
Feeding Schedule All animals were removed from ad lib feeding 2-3 days before tray feeding commenced and were given 10 g of Noyes pellets per day in the home cage. Once training had started all animals received sufficient standard diet (41B) after each session to stabilize their body weights at approximately 80% of their free-feeding values.
the tray door was progressively lowered to its fully closed position (tray door training). Bar press training continued under the FR1 schedule through the stages shown as ii to vii in Fig. 1 and as described in the apparatus section. This constituted manipulandum identification pretraining. Once an animal was operating the bar + chain in position vii, the FR value was raised in single steps to FR8 (8 responses per food pellet), in double responses steps between FR8 and FR20 and 2, 3, or 5 response steps thereafter to FR60 (60 responses per food pellet). The number of sessions given to each animal at each step and the size of the steps at higher FR values were determined by the stability of that animal's performance. Sessions lasted for approximately 30 min or until 60 reinforcements had been delivered, whichever was sooner.
Histology When testing was complete all animals received a lethal dose of pentobarbitone sodium anaesthetic followed by intracardiac perfusion with physiological saline and then 10% formol saline. Brains were removed, photographed, and embedded in paraffin wax. Coronal sections were cut at 15/~ thickness and every 17th section was stained with cresyl violet and mounted under glass. The lesions were drawn from the prepared sections onto a series of standard coronal sections and were then reconstructed individually onto an outline drawing of dorsal and lateral aspects of a normal rat brain. Estimates of lesion size were obtained by perimetry from the series of coronal sections.
Statistical Analyses Unless noted otherwise, between group statistical analysis was based on Mann-Whitney U tests [30] and within-group trends were evaluated using Page's L test [26].
Tray Feeding and Bar Press Training On the first day of tray feeding each animal was placed in the training box for 15 min with 60 Noyes pellets in the food tray and with the food tray door held open. This was followed by 4 daily sessions with the long (10 cm) bar in place in its lowest position (i in Fig. 1) on an FR1 schedule (one bar response per food reward pellet). During these four sessions
RESULTS
Histology Surface reconstructions of the brains of all five lesioned animals used in this experiment are shown in Fig. 2. Figure 3 is a set of nine standard coronal sections showing the area common to all lesions and their range. The small amount of
360
( )A K i •] TABLE 1 SHOWING INTEROPERATIVEINTERVALS, POSTOPERATIVEINTERVALS. LESION SIZES AND ORDER OF LESION1NGFOR ALL SUBJECTS lnteroperative* interval (weeks)
Posloperative+ interval {weeks)
%$ Lesion
Order of~ lesion
Neodecorticate 5D 28D 37D 42D
8 9 9 8
14 18 11 24
99.9 99.2 99.7 99.8
L-R L-R L-R R-L
Normal 18N 49N 5IN 53N
7 9 9 9
14 18 11 23
d
L-R L-R L-R L-R
*Interval in weeks between two stages of hemidecortication in the neodecorticates and between two sham operations in the normal group. tlnterval in weeks between the final operation and the first day of testing. ~:Lesion size expressed as a percentage of total neocortex removed. §Order in which left (L) and right (R) sided hemidecortication or sham operations were performed. neocortical sparing present in these brains (see Table 1) was predominantly anterior, adjacent to the rhinal fissure. Transitional cortex was invaded in all brains along the rhinal fissure, particularly caudally, and in midline regions. Postoperative degenerative changes had removed all cortical tissue below the devascularized surface of the hemisphere and in the majority of cases associated white matter, including the corpus callosum, had also disappeared (see Fig. 4). Ventricular expansion was evident in all lesioned brains resulting in lateral displacement of caudate/putamen. Hippocampus was less frequently displaced and neither set of structures showed signs of damage. No other evidence of subcortical changes was seen in the lesioned brains and no neocortical or other neural changes were found in the sham operated animals as a result of trephining.
Postoperative Recovery When training commenced all animals were selfmaintaining on laboratory diet and plain water. The neodecorticates were easy to handle and showed no obvious behavioural abnormalities when observed in their home cages, though grooming was sometimes less effectively performed than in normals. The stabilized ad lib body weights of the neodecorticate animals (347.8 + 19.9 g) and the normals (425.8 + 13.9 g) differed significantly immediately prior to the food deprivation procedures (N~=N2=4, U=0, p = ×0.014). This is consistent with earlier incidental observations of lower set-points for body weight in neodeeorticate rabbits [14, 15, 20, 21, 23] and with Braun's more formal observations in the neodecorticate rat [4]. FIG. 4. Dorsal and lateral views of a sample neodecorticate brain showing complete postoperative degeneration of devascularized neocortex and associated white matter. Ventricular expansion and integrity of hippocampus and other subcortical structures are evident in both views. The isolated strip of tissue in the dorsal midline region is transitional cortex, beneath which the corpus callosum has degenerated. The background in both parts of the figure is marked in 1 cm squares.
Bar Press Training All animals received 4 daily sessions with the long plain bar in the low position (stage 1) combined with tray door training. The transition from this condition to the short bar + chain in the high position (stages ii-vii) was completed in between 8 and 10 sessions in all animals except one
NEOCORTEX
AND LEARNING
361 TABLE 2
SHOWING MEAN ( _+ SD) OVERALL RESPONSE RATES AND RUNNING RESPONSE RATES IN RESPONSES PER MINUTE, AND POST-REINFORCEMENT PAUSE DURATIONS IN SECONDS FOR NORMAL AND NEODECORTICATE RATS UNDER FOUR FIXED RATIOS Within group* trend
FR 10
FR20
FR40
FR60
1) Overall response rate Normal Neodecorticate Between groupst
34.2 _+ 12.1 22.4 _ 4.3 p =0.029
51.5 ___ 12.9 24.7 _ 10.7 p =0.029
64.7 _+ 19.2 20.4 _ 4.4 p=0.014
75.9 _ 11.5 23.2 _+ 4.6 p =0.014
L = l l 6 , p<0.01 L=106, NS
2) Running response rate Normal Neodecorticate Between groupst
63.0 _ 23.7 46.2 + 12.1 NS
78.5 _+ 18.3 51.9 _+ 14.8 p =0.029
92.7 _+ 30.2 41.9 _+ 6.0 p=0.014
101.7 _+ 15.7 44.3 _+_ 7.6 p =0.014
L=l13, p<0.05 L=I01, NS
3) Post-reinforcement pause Normal Neodecorticate Between groupst
8.7 ± 3.8 13.7 ___ 6.2 NS
8.7 _+ 3.8 30.4 _+ 15.5 p=0.014
11.6 _+ 2.7 64.0 _+ 28.2 p=0.014
12.3 _+ 2.9 77.0 _+ 21.8 p =0.014
L = l 1 2 , p<0.05 L = l l 9 , p<0.01
These data are based on kymograph recordings. *L test, k=4, n = 4 in all cases. t U test Nl=N2=4 in all cases.
TABLE 3 SHOWING MEAN ( -+ SD) TRAY/REINFORCEMENT RATIOS IN NORMAL AND NEODECORTICATE RATS UNDER FIVE FIXED RATIOS
Normal Neodecorticate Between groupst
FR 1
FR 10
FR20
FR40
FR60
2.0 ___ 1.6 3.4 _ 2.3 NS
2.5 _+ 0.7 6.5 + 1.9 p=0.014
2.6 --_ 0.6 5.1 ± 1.4 p=0.014
2.9 _+ 0.7 5.1 _+ 1.5 NS
3.0 _+ 0.6 3.8 _+ 1.8 NS
Within group* t re nd L = 196 NS L=186 NS
These data are expressed as the number of food tray responses per reinforcement. *L test, k=5, n = 4 in all cases. t U test, NZ=N2=4 in all cases.
n e o d e c o r t i c a t e (28D) w h i c h r e q u i r e d 30 s e s s i o n s . R e s p o n s e r a t e s o n FR1 at t h e e n d o f this p e r i o d o f m a n i p u l a n d u m i d e n t i f i c a t i o n p r e t r a i n i n g w e r e n o t significantly different in the t w o g r o u p s ( N o r m a l s 8.7, S D --- 4.2 r e s p o n s e s p e r minute; N e o d e c o r t i c a t e s 5.0, ---2.5 r e s p o n s e s p e r minute). Raising t h e F i x e d R a t i o s c h e d u l e f r o m FR1 w i t h t h e b a r + c h a i n in p o s i t i o n vii to F R 6 0 r e q u i r e d 31.8 (SD ___ 8.2) s e s s i o n s in t h e n e o d e c o r t i c a t e s a n d 32.5 (-+7.0) s e s s i o n s in the n o r m a l a n i m a l s . T h e s e m e a n s are n o t significantly different. A s t h e r e i n f o r c e m e n t ratio w a s r a i s e d o n t h e b a r + c h a i n m a n i p u l a n d u m to FR60, b o t h n o r m a l s a n d n e o d e c o r t i c a t e s c o n t i n u e d to r e s p o n d b u t w i t h n o r m a l r e s p o n s e r a t e s b e c o m ing i n c r e a s i n g l y h i g h e r t h a n t h o s e o f t h e n e o d e c o r t i c a t e s f r o m F R 1 0 o n w a r d s (see overafi r e s p o n s e r a t e s in T a b l e 2). In n o r m a l s t h e i n c r e a s e in m a n i p u l a n d u m r e s p o n s e r a t e s as t h e F R v a l u e w a s r a i s e d w a s significant w h e r e a s t h e o v e r a l l r e s p o n s e r a t e s in t h e n e o d e c o r t i c a t e s s h o w e d n o significant i n c r e a s e o r d e c r e a s e as the F R v a l u e c h a n g e d . Overall res p o n s e r a t e s are relatively g r o s s i n d i c e s o f p e r f o r m a n c e , h o w e v e r , a n d so a n a n a l y s i s w a s m a d e of p o s t r e i n f o r c e m e n t
pause duration and running response rates. The postreinf o r c e m e n t p a u s e w a s d e f i n e d as the first b r e a k in regular r e s p o n d i n g following r e i n f o r c e m e n t a n d the r u n n i n g r e s p o n s e rate w a s c a l c u l a t e d as the rate of r e s p o n d i n g in the period between the postreinforcement pause and the next r e i n f o r c e m e n t . T h e d a t a o b t a i n e d for r u n n i n g r e s p o n s e r a t e s f o l l o w e d quite closely t h o s e a l r e a d y d e s c r i b e d for overall r e s p o n s e r a t e s e x c e p t t h a t t h e r e w a s n o significant d i f f e r e n c e in r u n n i n g r e s p o n s e rate b e t w e e n n o r m a l a n d n e o d e c o r t i c a t e g r o u p s at FR10 (see T a b l e 2). I n c r e a s i n g F R s are n o r m a l l y a c c o m p a n i e d b y a n i n c r e a s e in p o s t r e i n f o r c e m e n t p a u s e dur a t i o n [8] a n d significant t r e n d s in this d i r e c t i o n are e v i d e n t in b o t h g r o u p s , t h o u g h t h e t r e n d is s t r o n g e r in n e o d e c o r t i c a t e s t h a n in n o r m a l s (see T a b l e 2). A t all F R v a l u e s a b o v e F R 1 0 p o s t r e i n f o r c e m e n t p a u s e s w e r e significantly l o n g e r in n e o d e c o r t i c a t e s t h a n in n o r m a l s . S a m p l e c u m u l a t i v e r e c o r d s for all eight a n i m a l s at FR10, FR20, F R 4 0 a n d F R 6 0 are g i v e n in Fig. 5. T a b l e 3 s h o w s t h e efficiency o f tray r e l a t e d b e h a v i o u r for b o t h g r o u p s as n u m b e r o f t r a y e n t r i e s p e r r e i n f o r c e m e n t re-
362
~>A~.i i;'~
/ /::/
FR1
:/// /
l)l SC[ I SS ION
FR40
:l
g
/
lOminutes
f i i
DECORTICAT E
(bar) response distributions in the two group~ arc ai~o vc markably similar, with a brief overshoot of responses im mediately after reinforcement R 1 followed by a perked oi io~ response probability, corresponding to the postfeinforcc ment pause, which is followed in turn by the response ~am leading to reinforcement at R2 (see Fig. 6). The steeper stope to the bar response run profile in the neodecorticates in Fig. 6 reflects the generally longer and more variable duration postreinforcement pauses in that group, especially at higher FRs.
/
/ /
NORMAL
FIG. 5. Sample cumulative records for all eight animals in Experiment 1 at FR10, FR20, FR40 and FR60. On these records a horizontal line indicates a pause in responding, vertical movements of the recording pen indicate repeated bar responding and the small diagonal marks show the point at which a food pellet reward was given. Cessation of responding commonly seen following delivery of food reward is the postreinforcement pause. These are particularly clear as long horizontal sections in the neodecorticate FR60 records. The almost vertical section of the record following the postreinforcement pause is the response run used in calculating the 'running' response rate. At each FR value the records, reading from left to right, were obtained from animals 5D, 28D, 37D, 42D, 18N, 49N, 51N and 53N, respectively.
ceived. The normal animals consistently produced lower mean tray/reinforcement ratios than neodecorticates but this difference was significant only at FR10 and FR20. The temporal distribution of both manipulandum and tray door responses in the interval between consecutive reinforcements is illustrated in Fig. 6, from which it is clear that the supernumerary tray responses in the neodecorticates were concentrated in the period immediately following reinforcement as are the tray responses of normal animals. Manipulandum
All neodecorticate and all normal animals successfidly completed the long, low bar to high bar + chain training sequence which was intended to serve as a form of manipulandum identification pretraining. In terms of the aims stated in the introduction this pretraining achieved its purpose and all animals went on to perform efficiently on FR60 schedules. These results thus confirm those previously reported for rabbits with manipulandum identification pretraining [15] and suggest that the pretraining effect is not speciesspecific. In addition to this general confirmation it is worth noting the following detailed similarities between the results obtained from the two species when pretrained animals are tested on FR schedules: (1) overall and local response rates were higher in the normal animals, especially at high FRs; (2) postreinforcement pauses increased in duration as FR values increased in both normals and nondecorticates: (3) the postreinforcement pauses were longer in neodecorticates than in normal animals: (4) tray/reinforcement ratios were slightly higher in the neodecorticates but not significantly so at the completion of FR training: (5) the distribution of tray responses and manipulandum responses in the interval between consecutive reinforcements were identical in normals and neodecorticates. Rats [251 and rabbits [231 without manipulandum identification pretraining, on the other hand, show an upper limit to their performance around FR4-10 and high levels of tray behaviour which persist throughout the interreinforcement period and give rise to enormous tray/reinforcement ratios. It would appear, therefore, that the bar + chain pretraining is effective in preventing both these effects and enables neodecorticate rats to perform as efficiently as normal animals on high Fixed Ratios insofar as response topography is concerned. The only substantial difference between normal and lesioned groups which was detected in this study was in the lower rate of maniputandum operation in the lesioned animals. This was due in part to longer postreinforcement pauses in this group but also to generally lower running response rates. EXPERIMENT 2 If the neodecorticate's inefficiency in bar and treadle pressing situations on FR schedules is due at least in part to a failure to separate manipulandum (bar or treadle) related behaviours from those associated with the food tray 115,24t, pretraining directed at enhancing manipulandum identification is only one of several possible ways of overcoming the lesioned animal's deficit. If, for example, the tray door itself were to be used as the manipulandum on a FR schedule any conflict between these two sets of behaviours should be eliminated and decorticate performance should be improved. This second experiment investigates FR performance in a naive neodecorticate rat using the food tray door as the manipulandum.
NEOCORTEX
AND LEARNING
363
NORMAL
DECORTICATE
2 >:
40 0
A
u,
55-2 set
-
24.9sec
-
-
FR 40
z B
1
FR 60
: FR.60 300
I
-
R2
dl
R2
Rl
INTER-REINFORCEMENT
INTERVAL
FIG. 6. Distribution of food tray and bar+chain
manipulandum responses within the interreinforcement interval at FRIO, FR20, FR40 and FR60 in four neodecorticate and four normal rats in Experiment 1. Each set of histograms is based on 10 consecutive reinforcements at the stated FR value for each of the four animals in the group. The mean interval between consecutive reinforcements is shown in seconds beneath each pair of histograms. Rl =reinforcement. R2=subsequent reinforcement. These data are based on kymograph recordings.
METHOD
Subjects
The subjects were one normal and one neodecorticated male, Hooded Lister rat. The lesioned rat weighed 268 g
prior to surgery. Neodecortication stage as described in Experiment
was performed
in one
1 and 9 weeks were allowed for recovery. Neither animal had prior experience in any experimental apparatus.
)AKI . I
364
TABLE 4 MEAN RUNNING RESPONSE RAI'E IN RESPONSES PER MINUTE ( _~ SD) AND MEAN POST-REINFORCEMENT PAUSE DURATIONS IN SECONDS ( _+ SI)) FOR ONE NORMAL AND ONF NEODECORTICATE RAT UNDER FOUR FIXED RATIOS USING A FOOD TRAY DOOR MANIPULANDUM
1) Running response rate Normal Neodecorticate
FR 10
FR20
FR40
FR60
105.8 z 42.6 115.3 ~ 52.4
87.7 + 24.4 149.2 + 93.0
77.6 _+ 15.4 99.2 ± 15.2
70.1 ± 15.1 89.9 ± 10.7
7.2 ± 7.3 9.0 :t: 6.6
10.2 ± 10.9 7.2 + 4.6
16.2 _+ 16.3 9.6 ± 4.9
32.4 ± 33.1 16.2 + t8.3
2) Post-reinforcement pause Normal Neodecorticate
These data are based on the first 20 reinforcements of the final session at each FR value.
1
I
I
I
1
I
1
I
I
I
I
I
I
I
I
I
I
1
I
t
I
I
l
I
t
1
tray d o o r was held completely open and was gradually closed on later sessions until, after 4 sessions, both rats were reliably pushing the tray door open to retrieve the pellets in the tray. An FR1 schedule was then introduced so that a response pulse was generated and a pellet delivered to the food tray each time the tray d o o r was opened and then closed. The ratio of d o o r m o v e m e n t s to reinforcements was then increased from F R I (one d o o r press per food reward pellet) to FR60 (60 d o o r presses per pellet) in both animals on the following schedule, in which the F R value is shown followed by the number o f daily sessions in brackets. F R I 112); FR2 (!); FR3 (1); F R 4 (18); FR5 (1); F R 6 (1); FR8 (1); F R I 0 (17); FR12 (1); FR15 (1); FR17 (1); FR20 (3); FR25 (I); FR30 (1); FR35 (1); FR40 (1); FR45 (1); FR50 (2); FR55 (1); FR60 (4). Up to FR8 each session consisted of 90 reinforcements and from FR10 onwards 60 reinforcements were given per session.
I
RESULTS
Histology Reconstruction of the brain of the neodecorticate showed that 89.9% of total n e o c o r t e x had been r e m o v e d , with the major neocortical sparings occurring laterally adjacent to the rhinal fissure. S o m e damage to retrosplenial areas of cingulate cortex was present in both hemispheres. No subcortical damage was seen.
f NORMAL I
1
1
1
I
t
I
I
;
I
I
1
I
I
I
I
I
I
I
I
I
I
I
I
I
I
FIG. 7. Sample cumulative records for one normal and one neodecorticate rat with a tray door manipulandum in Experiment 2. The baseline for each half of the figure is marked in 1 min intervals.
Apparattts The apparatus was as described in E x p e r i m e n t 1 except that no response bar was present.
Tray Feeding and Door-Push Training Both animals were reduced to 85-90% of normal body weight by regular daily feeding. Preliminary training consisted of allowing the animal to eat 20 r e i n f o r c e m e n t pellets per daily session from the food tray. On the first session the
I
Fixed Ratio Training Both animals continued to operate the tray d o o r manipulandum reliably at all F R values and, as Fig. 7 shows, the cumulative records they p r o d u c e d w e r e remarkably similar. Both animals p r o d u c e d longer p o s t r e i n f o r c e m e n t pauses as the F R was increased to FR60 (Table 4). Mean running response rates, h o w e v e r , showed a t e n d e n c y to reduce in value in both animals as the F R increased (Table 4). Whilst it would be inappropriate to draw firm conclusions from data based on only two animals it is interesting to note that the neodecorticate in this experiment p r o d u c e d faster running response rates and shorter p o s t r e i n f o r c e m e n t pauses than the normal, which is the c o n v e r s e of the o u t c o m e in Experiment 1 using a bar + chain manipulandum. DISCUSSION On the basis of this one neodecorticate rat it would appear
NEOCORTEX AND L E A R N I N G
365
that normal levels of performance on FR schedules can be achieved without pretraining if the manipulandum is not separated from the source of food. The FR schedule itself does not therefore seem to be a problem for the neodecorticate rat. The results is generally consistent with the notion that the neodecorticate is impaired in its ability to identify and respond discretely to separate elements in its environment. G E N E R A L DISCUSSION The results of these two experiments are in general support of the view that neodecorticated mammals are not impaired in their ability to form learned associations in instrumental situations where some manipulandum, such as a movable bar or treadle, must be operated for food reward. Their difficulty seems to lie more in identifying and responding selectively to separate elements in their environment, in particular the manipulandum and the food tray. One consequence of this inability is the neodecorticate's tendency to interrupt its manipulandum responding with inappropriate food tray oriented behaviours. Under these conditions instrumental performance is inefficient and the behaviour breaks down if more than 4--8 manipulandum responses are required for each food reward. These deficits are still evident if the neodecorticates have had prior experience of Pavlovian nictitating membrane conditioning [23], of different instrumental responses [25] of GO-NO GO training to a houselight cue [25] and unsuccessful reversal training using the
same manipulandum [15]. When, on the other hand, pretraining which was designed to increase the neodecorticate's identification of a particular manipulandum was employed, subsequent instrumental performance was highly efficient, food tray responses were normally distributed and distinct from manipulandum responses and performance was sustained even if the response requirement was raised to 60 manipulandum responses for each food reward. Pretraining procedures having this remedial effect are successful reversal training on the same manipulandum [15] and training on a distinct and progressively more distant manipulandum (Experiment 1 of this study). Removing the conflict between the manipulandum and food tray behaviours similarly produced highly efficient and normal looking instrumental performance in a neodecorticate, in this case by making the manipulandum and the food tray components synergistic. (Experiment 2 of this study). Pavlovian conditioning has already been shown to be reliably mediated outside neocortex in the mammalian brain [18, 19, 20, 21, 22]. Insofar as the behavior described in neodecorticate rats in the present study can be attributed to instrumental learning and not to implicit Pavlovian processes such as those involved in autoshaping or signtracking [7, 9, 10, 12, 29], the present results are inconsistent with earlier beliefs that instrumental learning in mammals is dependent on neocortex [I, 2, 6, 23, 27, 28]. The question of the likely neurological substrate of Paviovian conditioning and instrumental learning in the light of recent neodecortication studies is considered in more detail elsewhere [17].
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