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Long-term memory deficits for habituation of predatory behavior in the forebrain ablated goldfish (Carassius auratus)
EXPERIMENTAL
NEUROLOGY
36, 288-294 (1972)
Long-Term
Memory
Deficits
for
Predatory
Behavior
in the
Forebrain
Goldfish
(Carassius
V. S.
HARMAN University
PEEKE
of California,
1 AND San
Habituation
of
Ablated
auratus) SHIRLEY
Francisco.
C.
California
PEEKE 94122
AND JOHN State
S.
Uniz~ersity,
WILLISTON
San
Received
Fvawisco,
April
Calijomia
21, 1972
Forebrain-ablated, sham-operated, and normal goldfish were presented with 40 live brine shrimp confined in a clear plastic tube for 10 min on each of 5 successive days. The predatory responses (bites) directed at the brine shrimp waned similarly for all groups on day 1, indicating no deficit in inhibition or in shortterm memory. The normal and sham-operated groups showed complete savings of the previous day’s experience on subsequent days, indicating good memory for the first day’s habituation. The forebrainless fish showed essentially no savings between days, suggesting a deficit in long-term memory. The experimental paradigm makes it difficult to interpret the results according to nonspecific arousal or inhibitory explanations. Introduction
The function of the teleostian telencephalon is shrouded in interpretations which are apparently contradictory or at least not easily reconciled. Overmier and his collaborators (3-5, 9) have studied the forebrainless goldfish in active and passive avoidance situations and have concluded that loss of inhibitory function with forebrain ablation was responsible for deficits in both kinds of avoidance. Aronson and Kaplan (l), in a detailed summary of data from their own as well as other investigators’ laboratories, have concluded that the forebrain is essentially a nonspecific activating system: “Qualitative changes in behavior after forebrain removal are related to changes in arousal, and the similarity of these changes to those following lesions of the limbic system in mammals is noted. On the basis of the arousal hypothesis, we predict that the more complex the learning 1 This Training
research was supported Grant .5-Tl-MH 7082.
by Research
288 Copyright 0 1972 by Academic Press, Inc. All rights of reproduction in any form reserved.
Grants
MH
18636
and
MH
19978
and
MEMORY
DEFICITS
239
paradigm, the greater will be the effect of forebrain ablation” (p. 121). Savage (12j, on the basis of his work and a review of the literature, have postulated that the fmlction of the forebrain may be to “. . . intensify, prolong, or focus the effects of reinforcement, and in this way could greatly facilitate the progress of learning.” In summary, investigators have ascribed to the forebrain inhibitory functions, arousal functions, and reinforcement registration. Memory deficits found in many studies have been ascribed to one or the other of the more general functions listed. The teleostian forebrain is generally considered to be the derivative of the evolutionary forerunner of the mammalian limbic system and striatum. Nonspecific functions have been ascribed to both the limbic system and corpus striatum in mammals providing apparent agreement with the postulated nonspecific functions of the fish forebrain. However, disruption of limbic system function in mammals has been shown to interfere with the formation of memory [e.g., 7 (amygdala and hippocampus in cats) ; 2 (hippocampus in rats) ; 8 (amygdala in rats) 1. Similarly, disruption of striatal function (caudate-putamen ) interferes with memory formation in rats in a variety of tasks (6, 10, 14). Thompson (13) found similar results with caudate stimulation in monkeys. This body of evidence suggests the possibility that the forebrain in fish might have very specific functions related to long-term memory in addition to or rather than the postulated nonspecific function. The present experiment was designed to test the hypothesis that forebrain ablation in the goldfish would have detrimental effects on memory which would be separable from more general, nonspecific functions. We chose a paradigm that wo~dcl allow some assessment of the general capacities of arousal to stimuli and inhibition within a simple learning paradigm, repeated over days to allow assessment of memory for previous day’s experience. It has been demonstrated previously that goldfish (and also the Paradise Macropodus operccllavis) will attempt to catch small live crustaceans which are contained in a glass tube placed in the goldfish’s aquarium. This response, being unreinforced by success, will wane over a IO-min period, and this habituation persists and accumulates over days ( 11). Specifically, in the present study, the rate and permanence of this habituation to live, visible, but uncapturable prey was studied and comparisons drawn between normal. sham-operated, and forebrain-ablated goldfish. Comparisons were made within and between consecutive days. The hypothesis of a significant long-term memory function for the forebrain would be supported by findings that neither the initial response to the stimuli was different between forebrainless and control groups (i.e., no difference in arousal) nor the rate of decrement within the first session (i.e., no difference in inhibition),
290 but a between-days the least savings.
PEEKE,
PEEXE,
AND
recovery differential
WILLISTOPi
with the forebrainless
fish showing
Method
Sixty goldfish (Carussim auvafrts) 5-8 cm in length were selected for assignment to one of three groups: forebrain ablated, sham, or normal. After histological verification of complete ablation or noninjurious sham treatment, the numbers were : normals 20 ; sham operates 14 : and forebrainless 14. Surgical P9ocedures. Forebrain removal surgery was performed under urethane anesthesia administered in the water of a separate vessel. After disequilibrium and cessation of spontaneous motor activity, the goldfish was placed in a body holder supplied with a mouth tube through which fluid from the vessel flowed into the mouth and over the gill membranes. A scalpel cut was made through the skull in the shape of a T with the stem of the T oriented nasally. The scalpel blade severed the brain at the rear of the telencephalon and the severed lobes were aspirated through a drawn glass pipette. Fish were placed in a group tank and were watched for “normal” recovery. Fish demonstrating circling or other locomotor abnormalities were rejected. Sham-operated fish were similarly anesthetized, the T incision made, then placed in a group recovery tank. Experimental Procedures. Each fish was placed in a separate 30 X 30 X 60 cm aquarium and allowed to acclimatize to the new environment for 7 days. Each tank was provided with an outside air-driven filter, sand and gravel to cover the bottom, and was illuminated with a 100-W bulb on a 14 hr light-on cycle suspended 38 cm above the tank. Each tank had a 96 mm Petri dish in the front left corner in which a daily ration of tuhifex worms was placed. The placement in the Petri dish prevented the worms from escaping into the gravel substrate and then becoming a source of uncontrolled feeding. The daily ration was small enough to be consumed in less than a minute. Fish were fed in the evening (7 PM) and the esperimental observations were made between 11 AM and noon. During the acclimatization period a clear plastic waterfilled tube. S6 mm in diameter and long enough to protrude above the waterline. was placed in the center of the right half of the aquarium on each of the days. This tube was to be used to contain the prey in the experiment and responses to the tube alone, whether of approach or avoidance, had to be habituated before the experiment proper. The experiment proper consisted of placing the clear plastic tube filled with 40 live brine shrimp (,49te&u salina) in the aquarium at the spot where the tube was placed during acclimatization for 10 min each day. The number of bites directed at the brine shrimp was recorded through a hand console with buttons which registered each responsein one of five
MEMORY
291
DEFICITS
2-min bin counters. This procedure was repeated each day for 5 successive days. Histology. At the end of the experiment, all fish from the sham- and forebrain-operated groups as well as several normals were killed in urethane for histological examination. The top of the skull was removed to permit the diffusion of the fixative into the brain, and the head placed in a jar of 10% formalin for several weeks. The brains were then carefully removed from the heads, embedded in paraffin, and sectioned at 10 p. These serial sections were stained with either hematoxylin-eosin or thionine and examined for extent of the lesion and the possibility of additional damage to other parts of the brain. All forebrain-operated fish reported in this study had total loss of the telencephalon and did not sustain damage to either the mesencephalon or optic nerves or tracts. Results
The results are presented in Fig. 1. Initial level of response on day 1 is similar for all three groups, the rate of decrement over the 10 min is smaller for all groups. There is no trend toward a significant difference between the groups.2 On day 2 there is complete savings for both the control (C) and sham (S) groups, which do not differ from one another. The forebrainless (F) group is reliably more responsive than the sham 2 Between groups comparisons analysis of variance. Probability vidual group comparisons.
evaluated with levels greater
the Kruska l- Wallis nonparametric than .05 were not followed by indi-
H A-d
I
FIG.
during
7.
MINUTES 3 DAYS
FOREBRAINLESS SHAM OPERATES NORMALS
4
5
1. Predatory responses (bites) directed at visible but unavailable-brine a lo-min exposure period repeated on 5 successive days.
shrimp
292
PEEKE,
PEEKE,
AND
WILLISTON
and the normal group (p < .OS). This same pattern (P < .05>3 of results is repeated on each successive day. The control groups show a consistent low level of response, whereas the forebrainless group is reliably more responsive showing no savings from the previous day (day 3 F vs. C. p < .OOl : F vs. S, p < .OOl. Day 4 F vs. C, p < .OOl ; F vs. S, p < .OOl. Day 5 F vs. C, p < .OOl; F vs. S, p < .OOl). On days 3-5 the forebrainless group is significantly more responsive than either control group (p < .OOl) in all cases. In no case was there any trend toward a difference between the two control groups. The form of the daily response curves for the forebrainless group on days 1, 3-5 are very similar, each showing a within-days decrement of much the same magnitude. The curve for day 2 is not so clearly similar, but rather presents a picture of a depressed initial responding. Whether this represents some important phenomenon or is the result of sampling variability is not clear. A sign test between the total number of responses made on day 1 versus the number made on day 2 shows that there is a significant decline in responding (p < .Ol). Additional tests between day 1 and subsequent days show that days 4 and 5 are also reliably lower than day 1 (p < .03 for both days). This would indicate that some carry-over does occur between days, but of a magnitude much less than in control groups. This finding, however, does not detract from the basic findings, i.e., that forebrain-ablated goldfish are more responsive on all 4 of the last 4 days of the experiment, and that such responsivity is not the product of anesthesia and cranial insult, but rather of the ablation of the forebrain. The decline between days 1 and 2 in the two control groups reflects the behavior of all the fish in the groups. group
Discussion
The results of this experiment support the contention that the forebrainless goldfish is left with an impaired memory (storage or retrieval or both) mechanism insofar as forebrainless fish were only minimally able to profit from the habituation experience of the previous days. Control fish showed complete savings indicative of efficient memory. That such results were not due to more general, nonspecific functions as has been suggested by other investigators seems indicated in that differential effects on arousal due to forebrain ablation would have shown themselves on the initial levels of responding to stimuli on the first day. There were no differences nor trends toward differences on the initial level of response on day 1. Furthermore, proponents of the arousal hypothesis, predicting large effects of forebrain ablation only on more complex learning paradigms, would find it difficult 3 Probability levels using Mann-Whitney
less than U tests.
.05 were
followed
by
individual
group
comparisons
MEMORY
DEFICITS
293
to explain such large effects as we found on as simple a paradigm as habituation. Differential effects on a general inhibitory capacity due to forebrain ablation should have been revealed by different rates of habituation on day 1. There were no such differences. The interpretation of these results in terms of impairment of memory function should not be construed to mean that the forebrain is necessarily either the storage location of the engram or, if that were the case, the only storage location. It is consistent with the present results to hypothesize that the forebrain structures, either separately or in concert, exert tonic or modulaing influences on the consolidation of memory, and that the engram is stored in some older structure(s). A similar interpretation has been suggested for caudate-putamen function in regard to memory formation processes in rats ( 10). The results also suggest a dissociation of function between short- and long-term memory. Short-term memory is apparently intact in the forebrainless fish, as they are capable of showing habituation within the daily sessions. However, although the normal fish are apparently able to convert this short-term store into a more permanent long-term engram, the forebrainless fish cannot (or does so to a greatly diminished degree), showing essentially naivete between daily sessions. References
1. ARONSON, L. R., and H. KAPLAN. 1968. Function of the teleostean forebrain, pp, 107-125. Zlt “The Central Nervous System and Fish Behavior.” University of Chicago Press, Chicago. 2. BRUNNER, R. L.. R. R. Rossr, R. M. STUTZ, and T. G. ROTH. 1970. Memory loss following posttrial electrical stimulation of the hippocampus. Psychon. Sri. 18: 159-160. 3. CURNOW.
P. F., and J. B. OVERWER. 1968. Failure to show associative loss as the source of avoidance deficits following forebrain ablation in goldfish. --l>crrzl
Cow. 4. FRANK,
L4P-4
Proc.
76th
289-290.
A. H., N. B. FLOOD, and J. B. OVERMEIR. 1972. Reversal learning in fore. brain ablated and olfactory tract sectioned teleost, Carassizcs aurafus. Psyrhor~
Sci. 28: 149-150. 5. HAINSWORTH, F.
6. 7. 8. 9.
10.
R., J. B. OVERMEIR, and C. T. SNOWDON. 1967. Specific and permanent deficits in instrumental avoidance responding following forebrain ablation in the goldfish. J. Cornp. Physiol. Psychol. 83 : 111-116. HERZ, M. J., and H. V. S. PEEKE. 1971. Impairment of extinction with caudate nucleus stimulation. Brairt Res. 33 : 519-522. KESNER, R. P., and R. W. DOTY. 1968. Amnesia produced in cats by local seizure activity initiated from the amygdala. Exp. Aieuvol. 21 : 58-68. MCINTYRE, D. C. 1970. Differential amnesic effect of cortical vs. amygdaloid elicited convulsions in rats. Physiol. Bchav. 5 : 747-753. OVERMEIR, J. B., and N. B. FLOOD. 1969. Passive avoidance in forebrain ablated teleost fish, Carassius aurafus. Physiol. Behav. 4 : 791-794. PEEKE, H. V. S., and M. J. HERZ. 1971. Caudate nucleus stimulation retroactively impairs complex maze learning in the rat. Scimce 173 : 80-82.
294 II.
PEEKE,
PEEKE,
AND
WILLISTON
PEEKE, H. V. S., and S. C. PEEKE. 1972. Habituation, reinforcement, and recovery of predatory responses in two species of fish (Carassim nrtrntzrs and Macropodtts opercularis) . dnim. Behav. (in press). 12. SAVAGE, G. E. 1968. Function of the forebrain in the memory system of the fish, pp. 127-138. In “The Central Nervous System and Fish Behavior.” D. Ingle [Ed.]. University of Chicago Press, Chicago. 13. THOMPSON, R. 1958. The effect of intercranial stimulation on memory in cats. J. Cotrrp. Phgsiol. Ps~chol. 51: 421426. 14. WYERS, E. J., H. V. S. PEEKE, J. S. WILLISTON, and M. J. HERZ. 1968. Retroactive impairment of passive avoidance learning by stimulation of the caudate nucleus. Erb. Newol. 22 : 39-366.
NEUROLOGY
36, 288-294 (1972)
Long-Term
Memory
Deficits
for
Predatory
Behavior
in the
Forebrain
Goldfish
(Carassius
V. S.
HARMAN University
PEEKE
of California,
1 AND San
Habituation
of
Ablated
auratus) SHIRLEY
Francisco.
C.
California
PEEKE 94122
AND JOHN State
S.
Uniz~ersity,
WILLISTON
San
Received
Fvawisco,
April
Calijomia
21, 1972
Forebrain-ablated, sham-operated, and normal goldfish were presented with 40 live brine shrimp confined in a clear plastic tube for 10 min on each of 5 successive days. The predatory responses (bites) directed at the brine shrimp waned similarly for all groups on day 1, indicating no deficit in inhibition or in shortterm memory. The normal and sham-operated groups showed complete savings of the previous day’s experience on subsequent days, indicating good memory for the first day’s habituation. The forebrainless fish showed essentially no savings between days, suggesting a deficit in long-term memory. The experimental paradigm makes it difficult to interpret the results according to nonspecific arousal or inhibitory explanations. Introduction
The function of the teleostian telencephalon is shrouded in interpretations which are apparently contradictory or at least not easily reconciled. Overmier and his collaborators (3-5, 9) have studied the forebrainless goldfish in active and passive avoidance situations and have concluded that loss of inhibitory function with forebrain ablation was responsible for deficits in both kinds of avoidance. Aronson and Kaplan (l), in a detailed summary of data from their own as well as other investigators’ laboratories, have concluded that the forebrain is essentially a nonspecific activating system: “Qualitative changes in behavior after forebrain removal are related to changes in arousal, and the similarity of these changes to those following lesions of the limbic system in mammals is noted. On the basis of the arousal hypothesis, we predict that the more complex the learning 1 This Training
research was supported Grant .5-Tl-MH 7082.
by Research
288 Copyright 0 1972 by Academic Press, Inc. All rights of reproduction in any form reserved.
Grants
MH
18636
and
MH
19978
and
MEMORY
DEFICITS
239
paradigm, the greater will be the effect of forebrain ablation” (p. 121). Savage (12j, on the basis of his work and a review of the literature, have postulated that the fmlction of the forebrain may be to “. . . intensify, prolong, or focus the effects of reinforcement, and in this way could greatly facilitate the progress of learning.” In summary, investigators have ascribed to the forebrain inhibitory functions, arousal functions, and reinforcement registration. Memory deficits found in many studies have been ascribed to one or the other of the more general functions listed. The teleostian forebrain is generally considered to be the derivative of the evolutionary forerunner of the mammalian limbic system and striatum. Nonspecific functions have been ascribed to both the limbic system and corpus striatum in mammals providing apparent agreement with the postulated nonspecific functions of the fish forebrain. However, disruption of limbic system function in mammals has been shown to interfere with the formation of memory [e.g., 7 (amygdala and hippocampus in cats) ; 2 (hippocampus in rats) ; 8 (amygdala in rats) 1. Similarly, disruption of striatal function (caudate-putamen ) interferes with memory formation in rats in a variety of tasks (6, 10, 14). Thompson (13) found similar results with caudate stimulation in monkeys. This body of evidence suggests the possibility that the forebrain in fish might have very specific functions related to long-term memory in addition to or rather than the postulated nonspecific function. The present experiment was designed to test the hypothesis that forebrain ablation in the goldfish would have detrimental effects on memory which would be separable from more general, nonspecific functions. We chose a paradigm that wo~dcl allow some assessment of the general capacities of arousal to stimuli and inhibition within a simple learning paradigm, repeated over days to allow assessment of memory for previous day’s experience. It has been demonstrated previously that goldfish (and also the Paradise Macropodus operccllavis) will attempt to catch small live crustaceans which are contained in a glass tube placed in the goldfish’s aquarium. This response, being unreinforced by success, will wane over a IO-min period, and this habituation persists and accumulates over days ( 11). Specifically, in the present study, the rate and permanence of this habituation to live, visible, but uncapturable prey was studied and comparisons drawn between normal. sham-operated, and forebrain-ablated goldfish. Comparisons were made within and between consecutive days. The hypothesis of a significant long-term memory function for the forebrain would be supported by findings that neither the initial response to the stimuli was different between forebrainless and control groups (i.e., no difference in arousal) nor the rate of decrement within the first session (i.e., no difference in inhibition),
290 but a between-days the least savings.
PEEKE,
PEEXE,
AND
recovery differential
WILLISTOPi
with the forebrainless
fish showing
Method
Sixty goldfish (Carussim auvafrts) 5-8 cm in length were selected for assignment to one of three groups: forebrain ablated, sham, or normal. After histological verification of complete ablation or noninjurious sham treatment, the numbers were : normals 20 ; sham operates 14 : and forebrainless 14. Surgical P9ocedures. Forebrain removal surgery was performed under urethane anesthesia administered in the water of a separate vessel. After disequilibrium and cessation of spontaneous motor activity, the goldfish was placed in a body holder supplied with a mouth tube through which fluid from the vessel flowed into the mouth and over the gill membranes. A scalpel cut was made through the skull in the shape of a T with the stem of the T oriented nasally. The scalpel blade severed the brain at the rear of the telencephalon and the severed lobes were aspirated through a drawn glass pipette. Fish were placed in a group tank and were watched for “normal” recovery. Fish demonstrating circling or other locomotor abnormalities were rejected. Sham-operated fish were similarly anesthetized, the T incision made, then placed in a group recovery tank. Experimental Procedures. Each fish was placed in a separate 30 X 30 X 60 cm aquarium and allowed to acclimatize to the new environment for 7 days. Each tank was provided with an outside air-driven filter, sand and gravel to cover the bottom, and was illuminated with a 100-W bulb on a 14 hr light-on cycle suspended 38 cm above the tank. Each tank had a 96 mm Petri dish in the front left corner in which a daily ration of tuhifex worms was placed. The placement in the Petri dish prevented the worms from escaping into the gravel substrate and then becoming a source of uncontrolled feeding. The daily ration was small enough to be consumed in less than a minute. Fish were fed in the evening (7 PM) and the esperimental observations were made between 11 AM and noon. During the acclimatization period a clear plastic waterfilled tube. S6 mm in diameter and long enough to protrude above the waterline. was placed in the center of the right half of the aquarium on each of the days. This tube was to be used to contain the prey in the experiment and responses to the tube alone, whether of approach or avoidance, had to be habituated before the experiment proper. The experiment proper consisted of placing the clear plastic tube filled with 40 live brine shrimp (,49te&u salina) in the aquarium at the spot where the tube was placed during acclimatization for 10 min each day. The number of bites directed at the brine shrimp was recorded through a hand console with buttons which registered each responsein one of five
MEMORY
291
DEFICITS
2-min bin counters. This procedure was repeated each day for 5 successive days. Histology. At the end of the experiment, all fish from the sham- and forebrain-operated groups as well as several normals were killed in urethane for histological examination. The top of the skull was removed to permit the diffusion of the fixative into the brain, and the head placed in a jar of 10% formalin for several weeks. The brains were then carefully removed from the heads, embedded in paraffin, and sectioned at 10 p. These serial sections were stained with either hematoxylin-eosin or thionine and examined for extent of the lesion and the possibility of additional damage to other parts of the brain. All forebrain-operated fish reported in this study had total loss of the telencephalon and did not sustain damage to either the mesencephalon or optic nerves or tracts. Results
The results are presented in Fig. 1. Initial level of response on day 1 is similar for all three groups, the rate of decrement over the 10 min is smaller for all groups. There is no trend toward a significant difference between the groups.2 On day 2 there is complete savings for both the control (C) and sham (S) groups, which do not differ from one another. The forebrainless (F) group is reliably more responsive than the sham 2 Between groups comparisons analysis of variance. Probability vidual group comparisons.
evaluated with levels greater
the Kruska l- Wallis nonparametric than .05 were not followed by indi-
H A-d
I
FIG.
during
7.
MINUTES 3 DAYS
FOREBRAINLESS SHAM OPERATES NORMALS
4
5
1. Predatory responses (bites) directed at visible but unavailable-brine a lo-min exposure period repeated on 5 successive days.
shrimp
292
PEEKE,
PEEKE,
AND
WILLISTON
and the normal group (p < .OS). This same pattern (P < .05>3 of results is repeated on each successive day. The control groups show a consistent low level of response, whereas the forebrainless group is reliably more responsive showing no savings from the previous day (day 3 F vs. C. p < .OOl : F vs. S, p < .OOl. Day 4 F vs. C, p < .OOl ; F vs. S, p < .OOl. Day 5 F vs. C, p < .OOl; F vs. S, p < .OOl). On days 3-5 the forebrainless group is significantly more responsive than either control group (p < .OOl) in all cases. In no case was there any trend toward a difference between the two control groups. The form of the daily response curves for the forebrainless group on days 1, 3-5 are very similar, each showing a within-days decrement of much the same magnitude. The curve for day 2 is not so clearly similar, but rather presents a picture of a depressed initial responding. Whether this represents some important phenomenon or is the result of sampling variability is not clear. A sign test between the total number of responses made on day 1 versus the number made on day 2 shows that there is a significant decline in responding (p < .Ol). Additional tests between day 1 and subsequent days show that days 4 and 5 are also reliably lower than day 1 (p < .03 for both days). This would indicate that some carry-over does occur between days, but of a magnitude much less than in control groups. This finding, however, does not detract from the basic findings, i.e., that forebrain-ablated goldfish are more responsive on all 4 of the last 4 days of the experiment, and that such responsivity is not the product of anesthesia and cranial insult, but rather of the ablation of the forebrain. The decline between days 1 and 2 in the two control groups reflects the behavior of all the fish in the groups. group
Discussion
The results of this experiment support the contention that the forebrainless goldfish is left with an impaired memory (storage or retrieval or both) mechanism insofar as forebrainless fish were only minimally able to profit from the habituation experience of the previous days. Control fish showed complete savings indicative of efficient memory. That such results were not due to more general, nonspecific functions as has been suggested by other investigators seems indicated in that differential effects on arousal due to forebrain ablation would have shown themselves on the initial levels of responding to stimuli on the first day. There were no differences nor trends toward differences on the initial level of response on day 1. Furthermore, proponents of the arousal hypothesis, predicting large effects of forebrain ablation only on more complex learning paradigms, would find it difficult 3 Probability levels using Mann-Whitney
less than U tests.
.05 were
followed
by
individual
group
comparisons
MEMORY
DEFICITS
293
to explain such large effects as we found on as simple a paradigm as habituation. Differential effects on a general inhibitory capacity due to forebrain ablation should have been revealed by different rates of habituation on day 1. There were no such differences. The interpretation of these results in terms of impairment of memory function should not be construed to mean that the forebrain is necessarily either the storage location of the engram or, if that were the case, the only storage location. It is consistent with the present results to hypothesize that the forebrain structures, either separately or in concert, exert tonic or modulaing influences on the consolidation of memory, and that the engram is stored in some older structure(s). A similar interpretation has been suggested for caudate-putamen function in regard to memory formation processes in rats ( 10). The results also suggest a dissociation of function between short- and long-term memory. Short-term memory is apparently intact in the forebrainless fish, as they are capable of showing habituation within the daily sessions. However, although the normal fish are apparently able to convert this short-term store into a more permanent long-term engram, the forebrainless fish cannot (or does so to a greatly diminished degree), showing essentially naivete between daily sessions. References
1. ARONSON, L. R., and H. KAPLAN. 1968. Function of the teleostean forebrain, pp, 107-125. Zlt “The Central Nervous System and Fish Behavior.” University of Chicago Press, Chicago. 2. BRUNNER, R. L.. R. R. Rossr, R. M. STUTZ, and T. G. ROTH. 1970. Memory loss following posttrial electrical stimulation of the hippocampus. Psychon. Sri. 18: 159-160. 3. CURNOW.
P. F., and J. B. OVERWER. 1968. Failure to show associative loss as the source of avoidance deficits following forebrain ablation in goldfish. --l>crrzl
Cow. 4. FRANK,
L4P-4
Proc.
76th
289-290.
A. H., N. B. FLOOD, and J. B. OVERMEIR. 1972. Reversal learning in fore. brain ablated and olfactory tract sectioned teleost, Carassizcs aurafus. Psyrhor~
Sci. 28: 149-150. 5. HAINSWORTH, F.
6. 7. 8. 9.
10.
R., J. B. OVERMEIR, and C. T. SNOWDON. 1967. Specific and permanent deficits in instrumental avoidance responding following forebrain ablation in the goldfish. J. Cornp. Physiol. Psychol. 83 : 111-116. HERZ, M. J., and H. V. S. PEEKE. 1971. Impairment of extinction with caudate nucleus stimulation. Brairt Res. 33 : 519-522. KESNER, R. P., and R. W. DOTY. 1968. Amnesia produced in cats by local seizure activity initiated from the amygdala. Exp. Aieuvol. 21 : 58-68. MCINTYRE, D. C. 1970. Differential amnesic effect of cortical vs. amygdaloid elicited convulsions in rats. Physiol. Bchav. 5 : 747-753. OVERMEIR, J. B., and N. B. FLOOD. 1969. Passive avoidance in forebrain ablated teleost fish, Carassius aurafus. Physiol. Behav. 4 : 791-794. PEEKE, H. V. S., and M. J. HERZ. 1971. Caudate nucleus stimulation retroactively impairs complex maze learning in the rat. Scimce 173 : 80-82.
294 II.
PEEKE,
PEEKE,
AND
WILLISTON
PEEKE, H. V. S., and S. C. PEEKE. 1972. Habituation, reinforcement, and recovery of predatory responses in two species of fish (Carassim nrtrntzrs and Macropodtts opercularis) . dnim. Behav. (in press). 12. SAVAGE, G. E. 1968. Function of the forebrain in the memory system of the fish, pp. 127-138. In “The Central Nervous System and Fish Behavior.” D. Ingle [Ed.]. University of Chicago Press, Chicago. 13. THOMPSON, R. 1958. The effect of intercranial stimulation on memory in cats. J. Cotrrp. Phgsiol. Ps~chol. 51: 421426. 14. WYERS, E. J., H. V. S. PEEKE, J. S. WILLISTON, and M. J. HERZ. 1968. Retroactive impairment of passive avoidance learning by stimulation of the caudate nucleus. Erb. Newol. 22 : 39-366.