EXPERIMENTAL
NEUROLOGY
63, 627-642 (1979)
Learning with Food Reward and Shock Avoidance in Neodecorticate Rats DAVID A. OAKLEY' Medical
Research Council 3 Malet Place,
Unit on Neural Mechanisms of Behaviour, London, WClE 7JG, England
Received
October
II,
1978
Early investigators found instrumental learning to be weak or absent in surgically neodecorticated mammals whereas more recent studies demonstrated efficient performance by such animals in bar-pressing and other instrumental learning situations. One difference between the two sets of investigations is the use of shock avoidance in the former and food reward in the latter. The present study compared the effectiveness of shock avoidance and food reward in totally neodecorticated rats in a straight alleyway. All neodecorticated animals learned to run the alleyway for food reward as rapidly, or more rapidly, than normal animals whereas none of the operated animals acquired the same response under shock-avoidance conditions. This was true even if shock training followed successful acquisition of the alleyway response for food. A comparison of sensitivity to footshock in normal and neodecorticated animals revealed that the latter were slightly less sensitive than normal animals on a “flinch” threshold test, but no significant differences were seen on a “jump” threshold test. Varying shock parameters had no effect on avoidance acquisition performance. It would appear on these data that shock avoidance was not an effective training procedure in neodecorticated rats whereas food reward was highly effective. The disruptive effect of shock may have resulted from changes in the probability or intensity of species-specific defence reactions to aversive stimuli due to the removal of neocortical influences. The discrepancy between earlier and more recent observations on neodecorticate learning may thus have been due to the type of reinforcer used.
INTRODUCTION The behavioral literature on totally neodecorticated mammals is not large but, until recently, had been consistent in showing the severe 1 The author’s present address is Department of Psychology, University College London, Gower Street, London, WC 1E 6BT, England. I am grateful to Paul Wilkinson and Dr. Hannah Knuth for assistance in testing the animals, to Alison Hogg for preparing the histological material, to Dr. C. H. Yeo and Mr. C. Cromarty for help in preparing the illustrations, and to Marita McLaughlin for typing the manuscript. 627 0014-4886/79/030627-16$02.00/O Copyright 0 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
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impairment or even abolition of instrumental learning after surgical removal of all neocortical tissue. Acquisition of a leg flexion avoidance response in a neodecorticated dog was demonstrated only after some 700 trials, and even then consistent performance depended on testing the animal when it was not agitated (6). Similarly, a totally neodecorticated rat failed to produce an instrumental head-turning response to a visual stimulus signaling shock (2), and instrumental heart-rate and intestinal responses were not formed in curarized rats with at least 90% neodecortications within a normally effective training session (7). Recently, however, a series of studies reported not only the possibility of instrumental learning in neodecorticated rabbits (10, 18, 19) and rats (20) but showed that it may be of highly efficient form (11, 12). There are a number of procedural and other differences between the earlier, essentially negative, studies and the recent positive ones, but a major distinction centers on the type of reinforcement used. The earlier investigations (2,6, 7) utilized a shock avoidance paradigm whereas the more recent ones (10-12, 18-20) involved neodecorticated animals operating a variety of manipulanda for food reward. There are no direct comparisons of aversive and appetitive reinforcers in neodecorticated animals though in one study cats acquired a T-maze response for food but did (3) “striatal” not learn to escape shock in a shuttle box. Although they did not test their suggestion directly, Bloch and Bello (1) proposed, on the basis of earlier work with partially neodecorticated animals, that food may be a more effective reinforcer than shock avoidance, and Bromiley (6) noted the disruptive effects of shock on his decorticated dog. It may be, therefore, that the different outcomes in studies of instrumental learning in neodecorticated animals depends primarily on the nature of the reinforcer used. The present study compared directly the effectiveness of food reward and shock avoidance as reinforcers for neodecorticated rats in a simple straight alleyway. MATERIALS
AND METHODS
Subjects and Surgery. The subjects were seven neodecorticated and seven normal rats (male, Hooded Lister) with a mean body weight of 302.1 (SD 4 32.0) g prior to surgery. The neodecortications were produced in two stages in three animals, with 7 weeks between stages, and in one stage in the other four animals. Neodecortication was achieved by removing the pia from the surface of the hemisphere thereby devascularizing it and causing cortical necrosis (9, 18). The normal animals were sham operated and received two 5-mm diameter trephine holes over the parietal cortex with 7 weeks between operations in three animals and as a one-stage
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operation in the other four. All surgery was carried out under pentobarbital sodium (Sagatal) anesthesia, and all animals had 14 to 31 weeks of postoperative recovery. Normal and neodecorticated animals were trained in pairs matched for surgical and postoperative history (see footnote a to Table 1). Table 1 summarizes interoperative and postoperative intervals, lesion size, and order of lesion for all subjects. Apparatus. The apparatus is shown in plan view in Fig. 1 and consisted of a 30 x 25cm start box joined by a 60-cm-long, 16cm-wide alleyway to a goal box measuring 14 x 27-cm. The walls of the apparatus were 1%cm high throughout. The floor of the alleyway and start box consisted of a grid of lZmm-diameter stainless-steel rods spaced at 2.5cm intervals, and the goal box floor was of solid nonconducting material. All three sections of the apparatus had hinged lids of clear plastic. Exit from the start box was blocked with a spring-operated shutter door which could be released manually at the start of each trial. There was a 10 x lo-cm opening between start box and alleyway and between alleyway and goal box, both of which were closed by a freely-moving, transparent, top-hinged door of a nonretrace design. Start box exit latency and alleyway running times were recorded automatically. On a food reward trial a single Noyes reinforcement pellet (45 mg) was placed in a g-cm-diameter dish in the goal box. Electromechanically chopped DC shock (eight reversals per second) could be delivered from a 250-V constant current source via the steel bars forming the start box and alleyway floors. Shock Avoidance. On the first session of shock avoidance training for naive animals the rat was placed in the alleyway section of the apparatus with the goal box door held in a half-open position for four trials, then with the door one-quarter open for four trials, and then fully closed for four trials. On trials 12 through 16 the rat was placed in the start box with the start box door removed, and on the final four trials of the first session the apparatus was complete with all doors in place and in their normal closed positions. In all cases shock was delivered to the grid floor 5 s after the animal had been placed in the apparatus. On all subsequent sessions the rat was placed in the start box facing one side wall (short thick arrow in Fig. l), the shutter door was released, and shock was delivered to the grid floor 5 s later. All sessions consisted of 20 trials with an average intertrial interval of 60 s. At all stages of training the rat could avoid shock by entering the goal box in less than 5 s or could escape shock by entering at any time after shock onset. Any animal which had not entered the goal box within 100 s, however, was removed from the apparatus. When shock avoidance training followed food reinforced training in the same apparatus the preliminary response shaping described above was omitted. Food Reward. Prior to training with food reward all animals were
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1
Interoperative and Postoperative Intervals, Lesion Size, and Order, Use of Animal in a Shock Threshold Test, and Type of Shock for AU Subjects”
Rat No.
A.
16D 40D 69D 77D 78D B. 46D 73D A.
17N 63N 99N 102N 103N B. 60N 1OlN
Interoperative interval* (weeks)
I I I I 7 7 -
Postoperative intervaP
Percentage lesiond
Order of IesiotF
Used in threshold test’
Shock type”
1s 31 25 19 31 20 19
Neodecorticate 99.7 99.9 99.3 99.8 99.8 99.8 99.7
L-R L-R B B B R-L B
No Yes Yes No Yes No No
1, cont. 1, int. 0.5, cont. 1, cont. 1, int. 1, cont. 1, cont.
14 29 26 18 29 16 16
Normal -
L-R L-R B B B R-L B
No Yes Yes No Yes No No
1, cont. 1, int. 0.4, cont. 1, cont. 1, int. 1, cont. 1, cont.
(weeks)
a Neodecorticated and normal subjects were paired for testing in the order shown (i.e., 16D with 17N; 40D with 63N, etc.) and were matched for type (one- or two-stage) and order of lesion, duration of postoperative recovery, shock parameters during avoidance training, and involvement in shock threshold assessment. In the neodecorticate and normal groups, subgroup A was tested in the alleyway in the order shock-food-shock and subgroup B had food-shock (see text for details). * Interval in weeks between two stages of hemidecortication in the neodecorticated group and between two sham operations in the normal group. c Interval in weeks between the final operation and the first day of testing. d Lesion size expressed as a percentage of total neocortex removed. e Order in which left (L)- and right (R)-side hemidecortication or sham operations were performed. B-bilateral (one-stage) lesion. f Three neodecorticated and three normal animals were used in shock threshold tests as indicated. B Shock used in avoidance training in milliamperes. Cont. - continuous, int.-intermittent (0.5 s on, 2.0 s off).
deprived the goal standard repeated
of food overnight and were fed 20 to 30 reinforcement pellets in box on the next day. They were allowed a limited amount of diet on being replaced in their home cage, and the procedure was for several days with appropriate changes in the daily diet until
NEOCORTEX GOAL BOX
food dish
ALLEY
START BOX
WAY
top-hung (transparent) I 0
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centimetres I 10
doors door I
I
20
30
FIG. 1. Plan of alleyway. The heavy arrows in the start box and alleyway indicate, respectively, the position in which the animal was placed in the apparatus and the direction of alleyway running.
they were eating reliably in the goal box. The shaping of naive animals to pass through the transparent doors was conducted as described above for shock avoidance training except that rather more trials were needed for each step due to the generally lower levels of motivation achieved by food deprivation in comparison to shock avoidance and escape. A single reinforcement pellet was present in the goal box on shaping trials. Animals which had already learned to run the apparatus to escape or avoid shock were given the goal box feeding experience but did not require door shaping training. Procedures during food reward training were exactly as described for shock avoidance except that no shock was delivered and a food reward pellet was present in the goal box on each trial. All trials on which the animal entered the goal box in less than 100 s were reinforced. Shock-Food-Shock Training. For five neodecorticate and five normal animals (subgroups A in Table l), training commenced with 10 sessions of shock avoidance, followed by 10 sessions offood reward training, and then a final 10 sessions of shock avoidance, during which the food deprivation schedule initiated for the second 10 sessions was maintained though food was no longer given in the goal box. Shock parameters following the S-s avoidance period of no shock were varied across animals (see Table 1). Two normal and two neodecorticated rats were trained with 1-mA continuous shock in the two avoidance phases of the experiment; for two normal and two decorticated animals the shock was of I-mA intensity and intermittently delivered as a 500-ms square wave pulse every 2 s; one normal and one neodecorticated rat were trained using continuous shock at an intensity which matched their “flinch” thresholds, as described later. Food-Shock Training. Two neodecorticated and two normal rats (subgroups B in Table 1) were first given 10 sessions of food reward training.
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Preliminary goal box feeding and alleyway door shaping trials were completed before the first session of food reward training, in contrast to shock avoidance training where any shaping required was conducted as part of the first session. Food reward training was followed by 10 sessions of shock-avoidance training, again with the food deprivation schedule maintained. The shock for all four animals was 1-mA and continuous. Shock Threshold Tests. Sensitivity to footshock in normal and neodecorticated rats was assessed following a procedure described by Lints and Harvey (8). Each animal was exposed to l-s pulses of chopped, constant current, DC shock of O.l-, 0.2-, 0.3-, 0.4-, OS-, 0.75, and 1.O-mA intensity through a shock grid forming the floor of a 30 x 25 x 18-cm high enclosure in alternating ascending then descending series, each pulse of shock occurring at approximately 20-s intervals. Four ascending and four descending series were presented on each of 2 consecutive days. The animal’s reactivity to the onset of shock was characterized by two observers as “no response,” “ flinch” (startle or crouch, rear paws not leaving the floor), or “jump” (both rear paws leave grid floor). The threshold level for flinch and jump responses was defined as the lowest shock value at which the animal exhibited the response on at least 50% of the presentations. Eight normal and six neodecorticated animals took part in these tests, and all had at least 22 weeks of postoperative recovery prior to testing. Three of each group were animals which later served as subjects in the present experiments (see Table 1) and the remainder were naive animals drawn from a stock of sham-operated and neodecorticated rats which had received their operations as part of the same series as those in
FIG. 2. Reconstructions Surface dashed
of the brains of the neodecorticated rats used in alleyway training. extent of the lesions is shown in black. The rhinal fissure is shown as a solid black or white line running parallel to the ventral outline in the lateral views of each brain.
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FIG. 3. Coronal sections showing, in black, the tissue loss common to all seven neodecorticated rats. The heavily dotted areas indicate tissue loss in at least one animal.
the present studies and were of matched lesion sizes. The flinch thresholds obtained for the neodecorticated rat 69D (0.5 mA) and the normal rat 99N (0.4 mA) were used as the shock levels during their avoidance training. Histology. When testing was complete the animals were given a lethal dose of pentobarbital sodium followed by intracardiac perfusion with physiological saline and then a 10% formol-saline solution. Brains were removed, drawn, photographed, and embedded in paraffin wax. Coronal sections were cut at 15qm thickness, and every 17th section was stained with cresyl violet and mounted under glass. The lesions were drawn from the prepared sections on a series of standard coronal sections and were then reconstructed individually on 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. All between-groups statistical analysis was based on one-tailed Mann-Whitney U-tests (23) and within-group trends were evaluated using Page’s L-test (21). RESULTS Histology. Surface reconstructions of the brains of all seven animals with lesions used in alleyway training are shown in Fig. 2. Figure 3 is a set of nine
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standard coronal sections showing the area common to all lesions and their range. The small amount of neocortical sparing present in these brains 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 all cases the majority of associated white matter, including the corpus callosum, had also disappeared (see Figs. 4 and 5). Ventricular expansion was evident in all brains with lesions and had resulted in most in the lateral displacement of the caudate-putamen. The hippocampus was less frequently displaced, and no sign of direct subcortical damage was seen in any brain. No neocortical or other neural changes were found in the sham-operated animals as a result of trephining. Postoperative Recovery. All seven neodecorticated rats used in the alleyway study were self-maintained on laboratory diet and plain water at the time the experiments commenced. They were alert and showed no obvious behavioral abnormalities when observed in their home cages or when allowed to explore work surfaces in the testing rooms. Shock Avoidance and Food Reward Training. Mean running times over 40-trial (two sessions) blocks for the five normal and five neodecorticate rats in subgroup A (shock-food-shock) and the two normals and two neodecorticated animals in subgroup B (food-shock) are shown in Fig. 6. Running time was counted from the opening of the shutter door to the time the animal entered the goal box. On the first shock avoidance training session with naive animals, full running times were available only for the final four trials when the animals ran the complete apparatus; the first 40-trials (two sessions) block shown for subgroups A in Fig. 6 consequently contained data from only 24 trials. Preliminary analyses revealed no differences due to varying shock parameters in either normal or neodecorticate animals or to the effects of one- vs. two-stage lesions, and so all the data are presented here as group means. All normal animals in both subgroups acquired a shock avoidance response and ran the apparatus reliably in less than 5 s. None of the neodecorticate rats, on the other hand, showed any sign of avoidance acquisition even when shock avoidance training commenced after successful acquisition of the response for food reward. All the neodecorticate rats produced long-latency shock escape responses but did not improve even this behavior during any lo-session period of training. In fact the only significant trend shown by neodecorticate rats during shock avoidance sessions was a deterioration in escape times seen in Fig. 6 in subgroup B (k = 5, N = 2, L = 103, P ~0.05). With food-motivated acquisition, after shock avoidance training, in subgroups A the normal rats were initially running the apparatus faster than the neodecorticated
NEOCORTEX
AND LEARNING
d
635
. lcm.
FIG. 4. Lateral and dorsal views of a neodecorticate rat brain from the present study, showing the complete postoperative degeneration of devascularized neocortex and associated white matter. Ventricular expansion and integrity of hippocampus and other subcortical structures are evident in all three views.
(N1 = N2 = 5, U = 0, P = 0.004). With continued food-reward training, however, the normal rats increased their running times (k = 5, N = 5, L = 25 1, P < 0.01) while the neodecorticated rats decreased theirs (k =5, N = 5, L = 260, P < 0.01) so that at the end of food-reward training the neodecorticated rats were not only entering the goal box in less than 5 s but had significantly shorter running times than normal rats (N’ = N* = 5, U = 3, P = 0.028). When food-rewarded training was initiated with naive animals in subgroup B, running times decreased significantly during the five blocks of 40 sessions in both normal (k = 5, N = 2, L = 104, P < 0.05) and in neodecorticated rats (k = 5, N = 2, L = 107, P < 0.01) again to yield mean running times less than 5 s in the neodecorticated group on the final 40-trial block. If it had experienced shock on previous trials, the neodecorticate rat’s response to being placed in the apparatus consisted primarily of freezing, followed soon after the onset of shock by attempts to jump out of the top of the apparatus, to burrow through the grid bars, or to escape via the corners of the start box either at floor or ceiling level. On the majority of trials the
636
DAVID A. OAKLEY
FIG. 5. Sample coronal sections of a neodecorticated rat brain. A-section at the level of the optic chiasm and decussation of the anterior commissure, showing the intact septum and marked bilateral displacement of the caudate-putamen due to expansion of the lateral ventricles. B-section at midthalamic level, showing intact hippocampus and lateral displacement of amygdaloid complex. In both sections neocortex is completely absent dorsal to the rhinal fissure. The island of tissue at the top of each section is midline transitional cortex, beneath which the corpus callosum has degenerated.
neodecorticated rats eventually exited abruptly from the start box via the transparent door, traversed the alley at speed, and entered the goal box within the 100-s time limit. Normal rats under shock avoidance conditions executed a rapid left turn on being placed in the start and ran immediately through the two sets of doors to enter the goal box before shock delivery. With food reward both the normal and the neodecorticated rats developed a simple turn to the left to exit from the start box. Start-box exit latencies and alleyway running times on the final 20-trial session in each of the three stages of training in subgroups A are shown in Fig. 7. Start-box exit latency was defined as the time (in seconds) between the experimenter opening the shutter door and the animal moving through the start box door into the alleyway. Alleyway running time was the time (in seconds) from the animal’s entry into the alleyway to its entry into the goal box. The neodecorticated animals were significantly slower in exiting from the start box than normal animals in both the first and the second attempt at
NEOCORTEX
B
AND
LEARNING
637
* .
avoidance training (N’ = N2 = 5, U = 0, P = 0.004 in both cases) but were not significantly different from normal animals in terms of alleyway running times during shock avoidance training. Figure 7 also shows that neodecorticated rats have both shorter start-box latencies and shorter running times for food reward compared to normal animals, though only the latter difference is significant (N’ = N* = 5, U = 3, P = 0.028). A picture similar to that depicted in Fig. 7 emerged from subgroups B for food then shock avoidance training. As the neodecorticated animals were traversing the apparatus in less than 5 s during the final sessions of food-motivated acquisition, the introduction of the shock avoidance contingency resulted in several avoidance responses on the initial trials. However, as food was no longer present in the goal box, the animals reduced their running speeds and when the first shock was encountered the neodeocorticated rats’ performance deteriorated immediately to become the inefficient escape behavior already described. During the shock avoidance training period the usually docile and tractable neodecorticated rats became difficult to transfer from their home cages into the apparatus, adopted exaggerated defensive postures when approached, and became generally hyperreactive. This type of reactivity was not seen with food-motivated training. In general the neodecorticated rats responded more rapidly than normal animals to food
638
DAVID A. OAKLEY SHOCK
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FIG. 6. Mean running times for normal and neodecorticate rats in subgroups A (above) and B (below) for shock avoidance and food reward in the alleyway apparatus. The horizontal dotted lines indicate the 5-s limit for avoidance under the shock condition.
deprivation schedules and in subgroup B when trained de LWVO with food reward the neodecorticated rats required only two and four shaping sessions, respectively, to learn to run the full apparatus and negotiate both doors. The normal rats required 6 and 11 sessions to reach the same level of performance. These shaping sessions were not counted in the 10 sessions of food retiard training shown in Fig. 6. Preliminary training with shock SHOCK
FOOD
SHOCK
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FIG. 7. Mean start-box exit latencies and alleyway running times on the final 20 sessions of training in the three phases of the experiment for normal and neodecorticate rats in subgroup A. * The difference between the two groups was statistically significant, P < 0.05.
NEOCORTEX
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AND LEARNING TABLE
2
Mean ? SD Minimum Shock Intensities (in Milliamperes) at Which Flinch and Jump Responses Were Recorded on 50% of Shock Presentations for Normal and Neodecorticate Rats Shock sensitivity thresholds (in mA)
Normal (N = 8) Neodecorticate (N = 6)
Flinch
Jump
0.33 t 0.07 0.48 2 0.14
0.69 5 0.11 0.75 2 0.14
was less variable and both normal and neodecorticate rats learned to operate both sets of doors within a single session as described earlier. Shock Sensitivity Thresholds. Results of the flinch and jump threshold tests are summarized in Table 2. The flinch threshold was significantly higher in neodecorticate than in normal rats (N’ = 6, N2 = 8, U = 8, P = 0.021) whereas there was no significant difference between the two groups on the jump threshold. DISCUSSION In its simplest terms the outcome of this study was to demonstrate that neodecorticated rats failed to acquire shock avoidance responses when required to exit from a start box and run down a straight alleyway but were able to produce the appropriate running response in the same apparatus when food reward was used. This is consistent with the idea that previous failures to demonstrate instrumental learning were due to the use of shock avoidance paradigms. The neodecorticate rats in the present study were generally more efficient than normal animals in food reward conditions and were capable of reaching the goal box within the 5-s time limit for avoidance responses. There would thus seem to be no reason to assume an impairment in instrumental learning ability per se as a result of neodecortication. Nor is there any basis for assuming a sensory or motor deficit to account for performance failures in shock avoidance conditions in this apparatus. This is especially evident in those cases where shock avoidance training was initiated after the animal had already acquired short-latency running responses for food reward. It would appear then, that the presence of shock serves directly to disrupt instrumental performance in the neodecorticated rat, particularly start-box exit responses. One possibility is that neodecortication renders the animal hypersensitive to this type of stimulus so that its normally disturbing effect is grossly exaggerated. Ameliorating the aversiveness of
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shock by making it intermittent or reducing it to a flinch threshold level, however, did not lessen its disruptive influence. Also the threshold tests revealed slightly less sensitivity in the animals with lesions on the flinch test, and their gross reaction to shock, as measured by jump thresholds, was not significantly different from normal animals. A second possibility is that the type of response to shock or the persistence with which such responses are displayed may be changed by removal of the neocortex. The suggestion that exaggerated “freezing” may disrupt performance in instrumental situations in neodecorticate (1) and striatal preparations (3) has been made before and is supported in the present studies insofar as freezing seemed to take precedence over any other form of behavior in the start box during the 5-s avoidance period before shock onset. In the presence of shock, however, freezing was less common than digging, jumping, and other forms of, in this case ineffective, escape behavior. It is interesting though that when a flight response was initiated and the animal left the start box, the neodecorticated animal’s performance in reaching the goal box was as efficient as that of a normal animal. The possibly disruptive effect of species-specific defence reactions in avoidance situations has been extensively discussed (4), and it is generally recognized that they are a potent source of “misbehavior” (5). Neodecortication may impair the rats’ ability to suppress inappropriate species-specific defence reactions, creating in the neodecorticate rat essentially a new species in which the biological constraints on learning have to be investigated anew. It should be possible to devise instrumental shock avoidance situations in which the neodecorticated animal’s species-specific defence reactions are compatible with instrumental performance and so abolish the avoidance learning deficit. On the basis of the present observations, for example, requiring the animal to remain immobile to avoid shock, or to jump out of an enclosure to escape shock, should be relatively easy responses for the neodecorticate rat to acquire. Bromiley’s (6) partial success in training aleg flexion response to avoid foot shock in a neodecorticate dog may, on this analysis, be because the flexion response was already part of the species-specific defence reaction to footshock. Certainly shock is a perfectly adequate unconditional stimulus for neodecorticate animals in Pavlovian conditioning situations and leads to virtually normal acquisition of conditional responses (7, 13) and is compatible with rather better than normal differentiation performance (14- 17). The original conflict of data from which this study arose concerned the question whether neodecorticated mammals could or could not learn under an instrumental paradigm. Early studies using shock avoidance implied that they could not, whereas later work with food reward found good evidence of instrumental learning in the absence of neocortex. The
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resolution of this conflict would appear to be that the neodecorticate rat, in common with the normal rat, finds some responses in some situations easy to learn and others difficult. On the basis of the somewhat limited data so far collected it seems that the neodecorticate rat finds alleyway running for food easy to acquire (this study): bar pressing for food less easy (12,20) and some responses, such as heart-rate changes, gastrointestinal changes, head movements, and alleyway running to avoid shock, difficult or even impossible [(2, 7) and the present study]. It is interesting to note that the order of difficulty given in this list is not the same as that which would be obtained for the normal rat. The overall conclusion must be that, despite earlier doubts (22), normal levels of performance are possible in neodecorticated mammals in some operationally defined instrumental learning situations. REFERENCES 1. BLOCH, S., AND M. BELLO. 1974. Differential instrumental learning with food reward after extensive neocortical lesions in rats. Actu. Neurobiol. Exp. 34: 603-613. 2. BLOCH, S., AND I. LAGARRIGUE. 1968. Cardiac and simple avoidance learning in neodecorticate rats. Physiol. Behav. 3: 305-308. 3. BJURSTEN, L.-M., K. NORRSELL, AND U. NORRSELL. 1976. Behavioural repertory ofcats without cerebral cortex from infancy. Exp. Bruin Res. 25: 115-130. 4. BOLLES, R. C. 1970. Species-specific defense reactions and avoidance learning. Psycho/. Rev.
77: 32-48.
5. BRELAND, K., AND M. BRELAND. 1961. The misbehavioroforganisms.Am. Psychol. 16: 681-684. 6. BROMILEY, R. B. 1948. Conditioned responses in a dog after removal of neocortex. J. Comp. Physiol. Psychol. 41: 102-110. 7. DICARA, L. V., J. J. BRAUN, AND B. A. PAPPAS. 1970. Classical conditioning and instrumental learning of cardiac and gastrointestinal responses following removal of neocortex in the rat. J. Comp. Physiol. Psycho/. 73: 208-216. 8. LINTS, C. E.. AND J. A. HARVEY. 1969. Altered sensitivity to footshock and decreased brain content of serotonin following brain lesions in the rat. J. Comp. Physiol. Psychol. 67: 23-31. 9. MEYER, P. M., AND D. R. MEYER. 1971. Neurosurgical procedures with special reference to aspiration lesions. Pages 91- 130 in R. D. MYERS, Ed., Methods in Psychobiology: Laborafory Techniques in Neuropsychoiogy and Neurobiology. Academic Press, London/New York. 10. OAKLEY, D. A., 1971. Instrumental learning in neodecorticate rabbits. Nature (NW Biol.) 233: 185- 187. 11. OAKLEY, D. A. 1979. Instrumental reversal learning and subsequent Fixed Ratio performance on simple and GO-NOGO schedules in neodecorticate rabbits. Physiol. Psychol.. in press. 12. OAKLEY, D. A. 1979. Performance on high Fixed Ratio schedules in neodecorticate rats. J. Comp. Physiol. Psychol., in press. 13. OAKLEY, D. A., AND I. S. RUSSELL. 1972. Neocortical lesions and Pavlovian conditioning. Physiol. Behav. 8: 915-926.
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14. OAKLEY, D. A., AND I. S. RUSSELL. 1974. Differential and reversal conditioning in partially neodecorticate rabbits. Physiol. Behav. 13: 221-230. 15. OAKLEY, D. A., AND I. S. RUSSELL. 1975. Role of cortex in Pavlovian discrimination learning. Physiol. Behav. 15: 315-321. 16. OAKLEY, D. A., AND I. S. RUSSELL. 1976. Subcortical nature of Pavlovian differentiation in the rabbit. Physiol. Behav. 17: 947-954. 17. OAKLEY, D. A., AND I. S. RUSSELL. 1977. Subcortical storage of Pavlovian conditioning in the rabbit. Physiol. Behav. 18: 931-937. 18. OAKLEY, D. A., AND I. S. RUSSELL. 1978. Performance of neodecorticated rabbits in a free-operant situation. Physiol. Behav. 20: 157- 170. 19. OAKLEY, D. A., AND I. S. RUSSELL. 1978. Manipulandum identification in operant behaviour in neodecorticate rabbits. Physiol. Behav. 21 (6). 20. OAKLEY, D. A., AND I. S. RUSSELL. 1979. Instrumental learning on Fixed Ratio and GO-NOGO schedules in neodecorticate rats. Brain Res. 162. 21. PAGE, E. B. 1963. Ordered hypotheses for multiple treatments: a significance test for linear ranks. J. Am. Statist. Assoc. 58: 216-230. 22. RUSSELL, I. S. 1971. Neurological basis of complex learning. Br. Med. Bull. 27: 278-285. 23. SIEGEL, S. 1956. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York.
NEUROLOGY
63, 627-642 (1979)
Learning with Food Reward and Shock Avoidance in Neodecorticate Rats DAVID A. OAKLEY' Medical
Research Council 3 Malet Place,
Unit on Neural Mechanisms of Behaviour, London, WClE 7JG, England
Received
October
II,
1978
Early investigators found instrumental learning to be weak or absent in surgically neodecorticated mammals whereas more recent studies demonstrated efficient performance by such animals in bar-pressing and other instrumental learning situations. One difference between the two sets of investigations is the use of shock avoidance in the former and food reward in the latter. The present study compared the effectiveness of shock avoidance and food reward in totally neodecorticated rats in a straight alleyway. All neodecorticated animals learned to run the alleyway for food reward as rapidly, or more rapidly, than normal animals whereas none of the operated animals acquired the same response under shock-avoidance conditions. This was true even if shock training followed successful acquisition of the alleyway response for food. A comparison of sensitivity to footshock in normal and neodecorticated animals revealed that the latter were slightly less sensitive than normal animals on a “flinch” threshold test, but no significant differences were seen on a “jump” threshold test. Varying shock parameters had no effect on avoidance acquisition performance. It would appear on these data that shock avoidance was not an effective training procedure in neodecorticated rats whereas food reward was highly effective. The disruptive effect of shock may have resulted from changes in the probability or intensity of species-specific defence reactions to aversive stimuli due to the removal of neocortical influences. The discrepancy between earlier and more recent observations on neodecorticate learning may thus have been due to the type of reinforcer used.
INTRODUCTION The behavioral literature on totally neodecorticated mammals is not large but, until recently, had been consistent in showing the severe 1 The author’s present address is Department of Psychology, University College London, Gower Street, London, WC 1E 6BT, England. I am grateful to Paul Wilkinson and Dr. Hannah Knuth for assistance in testing the animals, to Alison Hogg for preparing the histological material, to Dr. C. H. Yeo and Mr. C. Cromarty for help in preparing the illustrations, and to Marita McLaughlin for typing the manuscript. 627 0014-4886/79/030627-16$02.00/O Copyright 0 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
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impairment or even abolition of instrumental learning after surgical removal of all neocortical tissue. Acquisition of a leg flexion avoidance response in a neodecorticated dog was demonstrated only after some 700 trials, and even then consistent performance depended on testing the animal when it was not agitated (6). Similarly, a totally neodecorticated rat failed to produce an instrumental head-turning response to a visual stimulus signaling shock (2), and instrumental heart-rate and intestinal responses were not formed in curarized rats with at least 90% neodecortications within a normally effective training session (7). Recently, however, a series of studies reported not only the possibility of instrumental learning in neodecorticated rabbits (10, 18, 19) and rats (20) but showed that it may be of highly efficient form (11, 12). There are a number of procedural and other differences between the earlier, essentially negative, studies and the recent positive ones, but a major distinction centers on the type of reinforcement used. The earlier investigations (2,6, 7) utilized a shock avoidance paradigm whereas the more recent ones (10-12, 18-20) involved neodecorticated animals operating a variety of manipulanda for food reward. There are no direct comparisons of aversive and appetitive reinforcers in neodecorticated animals though in one study cats acquired a T-maze response for food but did (3) “striatal” not learn to escape shock in a shuttle box. Although they did not test their suggestion directly, Bloch and Bello (1) proposed, on the basis of earlier work with partially neodecorticated animals, that food may be a more effective reinforcer than shock avoidance, and Bromiley (6) noted the disruptive effects of shock on his decorticated dog. It may be, therefore, that the different outcomes in studies of instrumental learning in neodecorticated animals depends primarily on the nature of the reinforcer used. The present study compared directly the effectiveness of food reward and shock avoidance as reinforcers for neodecorticated rats in a simple straight alleyway. MATERIALS
AND METHODS
Subjects and Surgery. The subjects were seven neodecorticated and seven normal rats (male, Hooded Lister) with a mean body weight of 302.1 (SD 4 32.0) g prior to surgery. The neodecortications were produced in two stages in three animals, with 7 weeks between stages, and in one stage in the other four animals. Neodecortication was achieved by removing the pia from the surface of the hemisphere thereby devascularizing it and causing cortical necrosis (9, 18). The normal animals were sham operated and received two 5-mm diameter trephine holes over the parietal cortex with 7 weeks between operations in three animals and as a one-stage
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629
operation in the other four. All surgery was carried out under pentobarbital sodium (Sagatal) anesthesia, and all animals had 14 to 31 weeks of postoperative recovery. Normal and neodecorticated animals were trained in pairs matched for surgical and postoperative history (see footnote a to Table 1). Table 1 summarizes interoperative and postoperative intervals, lesion size, and order of lesion for all subjects. Apparatus. The apparatus is shown in plan view in Fig. 1 and consisted of a 30 x 25cm start box joined by a 60-cm-long, 16cm-wide alleyway to a goal box measuring 14 x 27-cm. The walls of the apparatus were 1%cm high throughout. The floor of the alleyway and start box consisted of a grid of lZmm-diameter stainless-steel rods spaced at 2.5cm intervals, and the goal box floor was of solid nonconducting material. All three sections of the apparatus had hinged lids of clear plastic. Exit from the start box was blocked with a spring-operated shutter door which could be released manually at the start of each trial. There was a 10 x lo-cm opening between start box and alleyway and between alleyway and goal box, both of which were closed by a freely-moving, transparent, top-hinged door of a nonretrace design. Start box exit latency and alleyway running times were recorded automatically. On a food reward trial a single Noyes reinforcement pellet (45 mg) was placed in a g-cm-diameter dish in the goal box. Electromechanically chopped DC shock (eight reversals per second) could be delivered from a 250-V constant current source via the steel bars forming the start box and alleyway floors. Shock Avoidance. On the first session of shock avoidance training for naive animals the rat was placed in the alleyway section of the apparatus with the goal box door held in a half-open position for four trials, then with the door one-quarter open for four trials, and then fully closed for four trials. On trials 12 through 16 the rat was placed in the start box with the start box door removed, and on the final four trials of the first session the apparatus was complete with all doors in place and in their normal closed positions. In all cases shock was delivered to the grid floor 5 s after the animal had been placed in the apparatus. On all subsequent sessions the rat was placed in the start box facing one side wall (short thick arrow in Fig. l), the shutter door was released, and shock was delivered to the grid floor 5 s later. All sessions consisted of 20 trials with an average intertrial interval of 60 s. At all stages of training the rat could avoid shock by entering the goal box in less than 5 s or could escape shock by entering at any time after shock onset. Any animal which had not entered the goal box within 100 s, however, was removed from the apparatus. When shock avoidance training followed food reinforced training in the same apparatus the preliminary response shaping described above was omitted. Food Reward. Prior to training with food reward all animals were
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1
Interoperative and Postoperative Intervals, Lesion Size, and Order, Use of Animal in a Shock Threshold Test, and Type of Shock for AU Subjects”
Rat No.
A.
16D 40D 69D 77D 78D B. 46D 73D A.
17N 63N 99N 102N 103N B. 60N 1OlN
Interoperative interval* (weeks)
I I I I 7 7 -
Postoperative intervaP
Percentage lesiond
Order of IesiotF
Used in threshold test’
Shock type”
1s 31 25 19 31 20 19
Neodecorticate 99.7 99.9 99.3 99.8 99.8 99.8 99.7
L-R L-R B B B R-L B
No Yes Yes No Yes No No
1, cont. 1, int. 0.5, cont. 1, cont. 1, int. 1, cont. 1, cont.
14 29 26 18 29 16 16
Normal -
L-R L-R B B B R-L B
No Yes Yes No Yes No No
1, cont. 1, int. 0.4, cont. 1, cont. 1, int. 1, cont. 1, cont.
(weeks)
a Neodecorticated and normal subjects were paired for testing in the order shown (i.e., 16D with 17N; 40D with 63N, etc.) and were matched for type (one- or two-stage) and order of lesion, duration of postoperative recovery, shock parameters during avoidance training, and involvement in shock threshold assessment. In the neodecorticate and normal groups, subgroup A was tested in the alleyway in the order shock-food-shock and subgroup B had food-shock (see text for details). * Interval in weeks between two stages of hemidecortication in the neodecorticated group and between two sham operations in the normal group. c Interval in weeks between the final operation and the first day of testing. d Lesion size expressed as a percentage of total neocortex removed. e Order in which left (L)- and right (R)-side hemidecortication or sham operations were performed. B-bilateral (one-stage) lesion. f Three neodecorticated and three normal animals were used in shock threshold tests as indicated. B Shock used in avoidance training in milliamperes. Cont. - continuous, int.-intermittent (0.5 s on, 2.0 s off).
deprived the goal standard repeated
of food overnight and were fed 20 to 30 reinforcement pellets in box on the next day. They were allowed a limited amount of diet on being replaced in their home cage, and the procedure was for several days with appropriate changes in the daily diet until
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food dish
ALLEY
START BOX
WAY
top-hung (transparent) I 0
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centimetres I 10
doors door I
I
20
30
FIG. 1. Plan of alleyway. The heavy arrows in the start box and alleyway indicate, respectively, the position in which the animal was placed in the apparatus and the direction of alleyway running.
they were eating reliably in the goal box. The shaping of naive animals to pass through the transparent doors was conducted as described above for shock avoidance training except that rather more trials were needed for each step due to the generally lower levels of motivation achieved by food deprivation in comparison to shock avoidance and escape. A single reinforcement pellet was present in the goal box on shaping trials. Animals which had already learned to run the apparatus to escape or avoid shock were given the goal box feeding experience but did not require door shaping training. Procedures during food reward training were exactly as described for shock avoidance except that no shock was delivered and a food reward pellet was present in the goal box on each trial. All trials on which the animal entered the goal box in less than 100 s were reinforced. Shock-Food-Shock Training. For five neodecorticate and five normal animals (subgroups A in Table l), training commenced with 10 sessions of shock avoidance, followed by 10 sessions offood reward training, and then a final 10 sessions of shock avoidance, during which the food deprivation schedule initiated for the second 10 sessions was maintained though food was no longer given in the goal box. Shock parameters following the S-s avoidance period of no shock were varied across animals (see Table 1). Two normal and two neodecorticated rats were trained with 1-mA continuous shock in the two avoidance phases of the experiment; for two normal and two decorticated animals the shock was of I-mA intensity and intermittently delivered as a 500-ms square wave pulse every 2 s; one normal and one neodecorticated rat were trained using continuous shock at an intensity which matched their “flinch” thresholds, as described later. Food-Shock Training. Two neodecorticated and two normal rats (subgroups B in Table 1) were first given 10 sessions of food reward training.
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Preliminary goal box feeding and alleyway door shaping trials were completed before the first session of food reward training, in contrast to shock avoidance training where any shaping required was conducted as part of the first session. Food reward training was followed by 10 sessions of shock-avoidance training, again with the food deprivation schedule maintained. The shock for all four animals was 1-mA and continuous. Shock Threshold Tests. Sensitivity to footshock in normal and neodecorticated rats was assessed following a procedure described by Lints and Harvey (8). Each animal was exposed to l-s pulses of chopped, constant current, DC shock of O.l-, 0.2-, 0.3-, 0.4-, OS-, 0.75, and 1.O-mA intensity through a shock grid forming the floor of a 30 x 25 x 18-cm high enclosure in alternating ascending then descending series, each pulse of shock occurring at approximately 20-s intervals. Four ascending and four descending series were presented on each of 2 consecutive days. The animal’s reactivity to the onset of shock was characterized by two observers as “no response,” “ flinch” (startle or crouch, rear paws not leaving the floor), or “jump” (both rear paws leave grid floor). The threshold level for flinch and jump responses was defined as the lowest shock value at which the animal exhibited the response on at least 50% of the presentations. Eight normal and six neodecorticated animals took part in these tests, and all had at least 22 weeks of postoperative recovery prior to testing. Three of each group were animals which later served as subjects in the present experiments (see Table 1) and the remainder were naive animals drawn from a stock of sham-operated and neodecorticated rats which had received their operations as part of the same series as those in
FIG. 2. Reconstructions Surface dashed
of the brains of the neodecorticated rats used in alleyway training. extent of the lesions is shown in black. The rhinal fissure is shown as a solid black or white line running parallel to the ventral outline in the lateral views of each brain.
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FIG. 3. Coronal sections showing, in black, the tissue loss common to all seven neodecorticated rats. The heavily dotted areas indicate tissue loss in at least one animal.
the present studies and were of matched lesion sizes. The flinch thresholds obtained for the neodecorticated rat 69D (0.5 mA) and the normal rat 99N (0.4 mA) were used as the shock levels during their avoidance training. Histology. When testing was complete the animals were given a lethal dose of pentobarbital sodium followed by intracardiac perfusion with physiological saline and then a 10% formol-saline solution. Brains were removed, drawn, photographed, and embedded in paraffin wax. Coronal sections were cut at 15qm thickness, and every 17th section was stained with cresyl violet and mounted under glass. The lesions were drawn from the prepared sections on a series of standard coronal sections and were then reconstructed individually on 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. All between-groups statistical analysis was based on one-tailed Mann-Whitney U-tests (23) and within-group trends were evaluated using Page’s L-test (21). RESULTS Histology. Surface reconstructions of the brains of all seven animals with lesions used in alleyway training are shown in Fig. 2. Figure 3 is a set of nine
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standard coronal sections showing the area common to all lesions and their range. The small amount of neocortical sparing present in these brains 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 all cases the majority of associated white matter, including the corpus callosum, had also disappeared (see Figs. 4 and 5). Ventricular expansion was evident in all brains with lesions and had resulted in most in the lateral displacement of the caudate-putamen. The hippocampus was less frequently displaced, and no sign of direct subcortical damage was seen in any brain. No neocortical or other neural changes were found in the sham-operated animals as a result of trephining. Postoperative Recovery. All seven neodecorticated rats used in the alleyway study were self-maintained on laboratory diet and plain water at the time the experiments commenced. They were alert and showed no obvious behavioral abnormalities when observed in their home cages or when allowed to explore work surfaces in the testing rooms. Shock Avoidance and Food Reward Training. Mean running times over 40-trial (two sessions) blocks for the five normal and five neodecorticate rats in subgroup A (shock-food-shock) and the two normals and two neodecorticated animals in subgroup B (food-shock) are shown in Fig. 6. Running time was counted from the opening of the shutter door to the time the animal entered the goal box. On the first shock avoidance training session with naive animals, full running times were available only for the final four trials when the animals ran the complete apparatus; the first 40-trials (two sessions) block shown for subgroups A in Fig. 6 consequently contained data from only 24 trials. Preliminary analyses revealed no differences due to varying shock parameters in either normal or neodecorticate animals or to the effects of one- vs. two-stage lesions, and so all the data are presented here as group means. All normal animals in both subgroups acquired a shock avoidance response and ran the apparatus reliably in less than 5 s. None of the neodecorticate rats, on the other hand, showed any sign of avoidance acquisition even when shock avoidance training commenced after successful acquisition of the response for food reward. All the neodecorticate rats produced long-latency shock escape responses but did not improve even this behavior during any lo-session period of training. In fact the only significant trend shown by neodecorticate rats during shock avoidance sessions was a deterioration in escape times seen in Fig. 6 in subgroup B (k = 5, N = 2, L = 103, P ~0.05). With food-motivated acquisition, after shock avoidance training, in subgroups A the normal rats were initially running the apparatus faster than the neodecorticated
NEOCORTEX
AND LEARNING
d
635
. lcm.
FIG. 4. Lateral and dorsal views of a neodecorticate rat brain from the present study, showing the complete postoperative degeneration of devascularized neocortex and associated white matter. Ventricular expansion and integrity of hippocampus and other subcortical structures are evident in all three views.
(N1 = N2 = 5, U = 0, P = 0.004). With continued food-reward training, however, the normal rats increased their running times (k = 5, N = 5, L = 25 1, P < 0.01) while the neodecorticated rats decreased theirs (k =5, N = 5, L = 260, P < 0.01) so that at the end of food-reward training the neodecorticated rats were not only entering the goal box in less than 5 s but had significantly shorter running times than normal rats (N’ = N* = 5, U = 3, P = 0.028). When food-rewarded training was initiated with naive animals in subgroup B, running times decreased significantly during the five blocks of 40 sessions in both normal (k = 5, N = 2, L = 104, P < 0.05) and in neodecorticated rats (k = 5, N = 2, L = 107, P < 0.01) again to yield mean running times less than 5 s in the neodecorticated group on the final 40-trial block. If it had experienced shock on previous trials, the neodecorticate rat’s response to being placed in the apparatus consisted primarily of freezing, followed soon after the onset of shock by attempts to jump out of the top of the apparatus, to burrow through the grid bars, or to escape via the corners of the start box either at floor or ceiling level. On the majority of trials the
636
DAVID A. OAKLEY
FIG. 5. Sample coronal sections of a neodecorticated rat brain. A-section at the level of the optic chiasm and decussation of the anterior commissure, showing the intact septum and marked bilateral displacement of the caudate-putamen due to expansion of the lateral ventricles. B-section at midthalamic level, showing intact hippocampus and lateral displacement of amygdaloid complex. In both sections neocortex is completely absent dorsal to the rhinal fissure. The island of tissue at the top of each section is midline transitional cortex, beneath which the corpus callosum has degenerated.
neodecorticated rats eventually exited abruptly from the start box via the transparent door, traversed the alley at speed, and entered the goal box within the 100-s time limit. Normal rats under shock avoidance conditions executed a rapid left turn on being placed in the start and ran immediately through the two sets of doors to enter the goal box before shock delivery. With food reward both the normal and the neodecorticated rats developed a simple turn to the left to exit from the start box. Start-box exit latencies and alleyway running times on the final 20-trial session in each of the three stages of training in subgroups A are shown in Fig. 7. Start-box exit latency was defined as the time (in seconds) between the experimenter opening the shutter door and the animal moving through the start box door into the alleyway. Alleyway running time was the time (in seconds) from the animal’s entry into the alleyway to its entry into the goal box. The neodecorticated animals were significantly slower in exiting from the start box than normal animals in both the first and the second attempt at
NEOCORTEX
B
AND
LEARNING
637
* .
avoidance training (N’ = N2 = 5, U = 0, P = 0.004 in both cases) but were not significantly different from normal animals in terms of alleyway running times during shock avoidance training. Figure 7 also shows that neodecorticated rats have both shorter start-box latencies and shorter running times for food reward compared to normal animals, though only the latter difference is significant (N’ = N* = 5, U = 3, P = 0.028). A picture similar to that depicted in Fig. 7 emerged from subgroups B for food then shock avoidance training. As the neodecorticated animals were traversing the apparatus in less than 5 s during the final sessions of food-motivated acquisition, the introduction of the shock avoidance contingency resulted in several avoidance responses on the initial trials. However, as food was no longer present in the goal box, the animals reduced their running speeds and when the first shock was encountered the neodeocorticated rats’ performance deteriorated immediately to become the inefficient escape behavior already described. During the shock avoidance training period the usually docile and tractable neodecorticated rats became difficult to transfer from their home cages into the apparatus, adopted exaggerated defensive postures when approached, and became generally hyperreactive. This type of reactivity was not seen with food-motivated training. In general the neodecorticated rats responded more rapidly than normal animals to food
638
DAVID A. OAKLEY SHOCK
FOOD
SHOCK 60-
A 4
\
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‘O Y F 60
.:
1
2
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3
4
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.
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30. e-aDECORTlCATE -NORMAL o-’
2
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3
4 ‘.k-o\---:,,:
4
5
1
40
-*
2
3
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TRIAL
.
5
1
2
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BLOCKS
FIG. 6. Mean running times for normal and neodecorticate rats in subgroups A (above) and B (below) for shock avoidance and food reward in the alleyway apparatus. The horizontal dotted lines indicate the 5-s limit for avoidance under the shock condition.
deprivation schedules and in subgroup B when trained de LWVO with food reward the neodecorticated rats required only two and four shaping sessions, respectively, to learn to run the full apparatus and negotiate both doors. The normal rats required 6 and 11 sessions to reach the same level of performance. These shaping sessions were not counted in the 10 sessions of food retiard training shown in Fig. 6. Preliminary training with shock SHOCK
FOOD
SHOCK
40
“0 6 Y m
20
2 -L w I ,r
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FIG. 7. Mean start-box exit latencies and alleyway running times on the final 20 sessions of training in the three phases of the experiment for normal and neodecorticate rats in subgroup A. * The difference between the two groups was statistically significant, P < 0.05.
NEOCORTEX
639
AND LEARNING TABLE
2
Mean ? SD Minimum Shock Intensities (in Milliamperes) at Which Flinch and Jump Responses Were Recorded on 50% of Shock Presentations for Normal and Neodecorticate Rats Shock sensitivity thresholds (in mA)
Normal (N = 8) Neodecorticate (N = 6)
Flinch
Jump
0.33 t 0.07 0.48 2 0.14
0.69 5 0.11 0.75 2 0.14
was less variable and both normal and neodecorticate rats learned to operate both sets of doors within a single session as described earlier. Shock Sensitivity Thresholds. Results of the flinch and jump threshold tests are summarized in Table 2. The flinch threshold was significantly higher in neodecorticate than in normal rats (N’ = 6, N2 = 8, U = 8, P = 0.021) whereas there was no significant difference between the two groups on the jump threshold. DISCUSSION In its simplest terms the outcome of this study was to demonstrate that neodecorticated rats failed to acquire shock avoidance responses when required to exit from a start box and run down a straight alleyway but were able to produce the appropriate running response in the same apparatus when food reward was used. This is consistent with the idea that previous failures to demonstrate instrumental learning were due to the use of shock avoidance paradigms. The neodecorticate rats in the present study were generally more efficient than normal animals in food reward conditions and were capable of reaching the goal box within the 5-s time limit for avoidance responses. There would thus seem to be no reason to assume an impairment in instrumental learning ability per se as a result of neodecortication. Nor is there any basis for assuming a sensory or motor deficit to account for performance failures in shock avoidance conditions in this apparatus. This is especially evident in those cases where shock avoidance training was initiated after the animal had already acquired short-latency running responses for food reward. It would appear then, that the presence of shock serves directly to disrupt instrumental performance in the neodecorticated rat, particularly start-box exit responses. One possibility is that neodecortication renders the animal hypersensitive to this type of stimulus so that its normally disturbing effect is grossly exaggerated. Ameliorating the aversiveness of
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shock by making it intermittent or reducing it to a flinch threshold level, however, did not lessen its disruptive influence. Also the threshold tests revealed slightly less sensitivity in the animals with lesions on the flinch test, and their gross reaction to shock, as measured by jump thresholds, was not significantly different from normal animals. A second possibility is that the type of response to shock or the persistence with which such responses are displayed may be changed by removal of the neocortex. The suggestion that exaggerated “freezing” may disrupt performance in instrumental situations in neodecorticate (1) and striatal preparations (3) has been made before and is supported in the present studies insofar as freezing seemed to take precedence over any other form of behavior in the start box during the 5-s avoidance period before shock onset. In the presence of shock, however, freezing was less common than digging, jumping, and other forms of, in this case ineffective, escape behavior. It is interesting though that when a flight response was initiated and the animal left the start box, the neodecorticated animal’s performance in reaching the goal box was as efficient as that of a normal animal. The possibly disruptive effect of species-specific defence reactions in avoidance situations has been extensively discussed (4), and it is generally recognized that they are a potent source of “misbehavior” (5). Neodecortication may impair the rats’ ability to suppress inappropriate species-specific defence reactions, creating in the neodecorticate rat essentially a new species in which the biological constraints on learning have to be investigated anew. It should be possible to devise instrumental shock avoidance situations in which the neodecorticated animal’s species-specific defence reactions are compatible with instrumental performance and so abolish the avoidance learning deficit. On the basis of the present observations, for example, requiring the animal to remain immobile to avoid shock, or to jump out of an enclosure to escape shock, should be relatively easy responses for the neodecorticate rat to acquire. Bromiley’s (6) partial success in training aleg flexion response to avoid foot shock in a neodecorticate dog may, on this analysis, be because the flexion response was already part of the species-specific defence reaction to footshock. Certainly shock is a perfectly adequate unconditional stimulus for neodecorticate animals in Pavlovian conditioning situations and leads to virtually normal acquisition of conditional responses (7, 13) and is compatible with rather better than normal differentiation performance (14- 17). The original conflict of data from which this study arose concerned the question whether neodecorticated mammals could or could not learn under an instrumental paradigm. Early studies using shock avoidance implied that they could not, whereas later work with food reward found good evidence of instrumental learning in the absence of neocortex. The
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resolution of this conflict would appear to be that the neodecorticate rat, in common with the normal rat, finds some responses in some situations easy to learn and others difficult. On the basis of the somewhat limited data so far collected it seems that the neodecorticate rat finds alleyway running for food easy to acquire (this study): bar pressing for food less easy (12,20) and some responses, such as heart-rate changes, gastrointestinal changes, head movements, and alleyway running to avoid shock, difficult or even impossible [(2, 7) and the present study]. It is interesting to note that the order of difficulty given in this list is not the same as that which would be obtained for the normal rat. The overall conclusion must be that, despite earlier doubts (22), normal levels of performance are possible in neodecorticated mammals in some operationally defined instrumental learning situations. REFERENCES 1. BLOCH, S., AND M. BELLO. 1974. Differential instrumental learning with food reward after extensive neocortical lesions in rats. Actu. Neurobiol. Exp. 34: 603-613. 2. BLOCH, S., AND I. LAGARRIGUE. 1968. Cardiac and simple avoidance learning in neodecorticate rats. Physiol. Behav. 3: 305-308. 3. BJURSTEN, L.-M., K. NORRSELL, AND U. NORRSELL. 1976. Behavioural repertory ofcats without cerebral cortex from infancy. Exp. Bruin Res. 25: 115-130. 4. BOLLES, R. C. 1970. Species-specific defense reactions and avoidance learning. Psycho/. Rev.
77: 32-48.
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