Journal of Comparative an, 1975, Vol. 89, No. 5, 489-497
Biological Psychology
Passive Avoidance Behavior in Rats After Electroconvulsive Shock : Facilitative Effect of Response Retardation Susan J. Sara, Michele David-Remacle, and Danielle Lefevre Center for Experimental and Comparative Psychology, University of Louvain, Pellenberg, Belgium Rats were trained in a one-trial passive avoidance task and then were submitted to electroconvulsive shock (ECS) or to sham ECS. Twenty-four hours later they were tested for retention,with the door opened either immediately or 30 sec after the beginning of the test. Rats initially forced to avoid for 30 sec continued to avoid for the entire test, but the others had the usual low step-through latencies seen withECS-treated animals. Activity measures for those animals stepping through differentiated groups having received footshock from those not having footshock and ECS. A retest 5-10 min later showed "recovery" in the amnestic animals and continued avoidance behavior for those that avoided on the first test. Results are taken as evidence that ECS effects are not on memory storage but on the capacity of the animal to organize information effectively and quickly in order to produce ah adaptive response.
Recovery from the amnestic effects of subthreshold engram to provide a viable such various agents as electroconvulsive memory capable of mediating behavior shock (ECS; Miller & Springer, 1972a, (Gherkin, 1972). Such a view predicts that 1972b; Quartermain, McEwen, & Azmitia, increasing the dose of the amnestic agent 1970, 1972; Sara, 1973a), hypoxia, (Sara, will decrease the probability of reco\ery of 1973b), hypothermia (Riccio & Stikes, memory. Experimental evidence does not, 1969), or cycloheximidc (Quartermain et al., however, always support this prediction 1972) is now well established. However, (Miller & Springer, 1972b; Quartermain controversy persists as to the significance et al., 1972, Exp. 5). of this recovery phenomenon for the conThe question of whether the reminder solidation hypothesis (Kesner & Connor, treatment provides new information has 1974). If amnestic agents produce a memory been addressed by several experiments. deficit by disruption of a time-dependent Most reactivation treatments use a nontrace fixation process, as the consolidation contingent footshock as a reminder for the hypothesis holds (McGaugh & Herz, 1972), footshock reinforcement given during trainthen the effects must necessarily be perma- ing. Springer and Miller (1972) have sucnent (see Lewis, 1969). To explain recovery ceeded in reinstating memory by a dissimiwithin a consolidation framework, it must lar stressful event, but this would likewise be supposed that the amnestic agent was serve to induce a reactive physiological inadequate and that a partial trace was state similar to the training state and could formed in spite of the treatment. Recovery be construed as being new relevant informaoccurs because reminder treatments give tion in the same way that noncontingent new information that sums with the existing footshock could. Quartermain et al. (1972) and Sara (1973a, 1973b) have underlined This research was supported by "Fonds pour la the importance of the training environment Recherche Fondamentale Collective" of Belgium and by a grant from Union Chimie Beige (U.C.B.). in reinstating memory. In these experiments, The authors wish to thank C. Giurgea for advice the animal steps through during the reand svipport. minder test and is removed from the shock Requests for reprints should be sent to Susan J. chamber, having received no shock. It has Sara, Centre de Psychologie Experimental et Compare'e, University de Louvain, Pellenberg, been argued that the motor act of stepping through (and/or the shock chamber) itself Belgium. 489
490
S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
has secondary reinforcing properties after association with footshock and therefore the animal receives response contingent secondary reinforcement during the reminder test—a new item of information. The present experiment is an attempt to reinstate memory after ECS without exposing the animal to either the primary footshock or secondary (shock chamber) reinforcement. EXPERIMENT 1 Method Subjects. The subjects were 42 male Wistar rats supplied by a commercial breeder. They weighed 200-250 g at the time of the experiment, were housed in groups of 6-8 in plastic breeding cages, and had free access to food and water. The cages were located in the laboratory with a normal day/ night cycle. The animals were habituated to this environment for 1 wk before the experiment. Apparatus. The training cage consisted of a two-compartment apparatus; the large compartment, measuring 37 X 28 X 14 cm, was constructed of gray plastic material, with a gravel floor similar to that of the living cage. This large compartment was illuminated from overhead by a 100-W bulb. The small compartment was made of aluminum, measuring 10 X 10 X 10 cm. The floor was constructed of metal rods 1 cm apart. A 6 X 6 cm door with guillotine closing separated the two compartments; a shock could be delivered through the floor and cage walls of the small compartment by means of a 180-V shock generator, through a Foringer scrambler. The output current was limited by a variable series resistance; shock intensity was 1 mA for 2 sec, controlled by an automatic Sedco timing device. The ECS was delivered by means of transtemporal electrodes from a 1,200-V transformer, 50-mA shock of .35-sec duration via a 10-kQ series resistance. The delay between footshock offset and ECS onset was 8 sec, controlled by a Sedco timing device that triggered an auditory signal to the experimenter. Experimental plan and procedure. Treatment of all animals during the training was identical. The rat was placed in the large compartment with the door leading to the small compartment closed. After 20 sec, the guillotine door was raised and the latency to step through was noted. When the animal had all four paws in the small compartment, the door was lowered and a 2-sec inescapable footshock was administered. The rat was immediately removed from the shock compartment. Each animal was restrained and electrodes were applied to the temporal area just behind the eyes. The electrodes were wet with saline solution mixed with red ink in order to verify that the electrodes had been correctly placed. Twenty-two animals received ECS and 20 sham ECS (no current).
Twenty-four hours later the rats were tested individually by placing them in the large compartment facing away from the closed door. For 11 ECS and 10 sham-ECS animals, the door was opened immediately. For the remaining 11 ECS and 10 sham-ECS animals, there was a 30-sec delay in opening the door. Thus, these animals were forced to "avoid" the small compartment formore than 30 sec at the beginning of the testing period. In this way four groups were generated: sham ECS and ECS, tested with the door immediately open (Groups ECSop and NECSop), and sham ECS and ECS, tested with the door closed for 30 sec (Groups NECScl and ECScl). The step-through latency after the door was opened was recorded for each rat. The testing period 24 hr after training lasted for 3 min after the door was opened.
Results and Discussion In both NECS groups all 10 animals avoided for the full 180-sec testing period. Ten animals stepped through and one avoided in the ECSop condition, and six stepped through and five avoided in Group ECScl. The difference between those two groups is significant (Fisher exact probability, p = .032). It should be noted, however, that the effect is only partial, since five of the ECScl stepped through, but no animals in either NECS group stepped through. Furthermore, the difference between the ECScl group and the NECScl group is significant (Fisher, p = .023). The results suggest that, although the position of the door at the beginning of the testing period is of no consequence for the animals that were trained but not convulsed, it is an important factor in the avoidance performance of those animals that are convulsed after footshock. If the step-through response is prevented for at least 30 sec (Group ECScl), there is a significantly greater tendency to avoid the shock compartment when compared with the ECS group whose step-through response is not delayed (Group ECSop). EXPERIMENT 2 It is possible that the position of the door of the shock compartment at testing could cause higher latencies in any group that would otherwise be expected to have low latencies, whether these low latencies are due to ECS treatment or absence of footshock reinforcement at training. This ex-
PASSIVE AVOIDANCE BEHAVIOR AFTER ECS
491
periment compares the effect of a 30-sec matically with the footshock and that triggered delay on an ECS group with the effect on an auditory signal to the experimenter 8 sec after termination. All animals were kept intwo other groups expected to have low test footshock dividually in small plastic cages for 15 min after latencies because of no footshock. The treatment and were then returned to the home motor activity in the shock chamber after a cage. Before testing, the groups were subdivided step-through response was monitored, and to permit two testing conditions for each training the total time spent in the shock chamber treatment. Half the animals were tested with the door open immediately and half with a 30-sec during a 60-sec period was recorded for each delay in door opening. If the rat avoided for 60 group. The purpose of these measures was sec, it was removed and assigned a score of 60. For to provide additional behavioral indices those animals stepping through, the latency was that might reveal memory of training foot- noted and the test was continued for 60 sec after the step-through response in order to have the shock, even for these animals that failed same duration of measurement of activity for each to produce the avoidance response. rat. If, indeed, the avoidance behavior of Animals were retested with the door in the open Group FS-ECScl is mediated by an orga- position (5-10 min after the first retention test); nized memory, the expression of this memory this second test lasted 180 sec. should be possible when tested with the door Results open. So all animals were retested 5-10 min after the first retention test. A slippage test (Conover, 1971) was performed on the initial step-through latencies, Method and there were no differences among the Subjects. Eighty-one male Wistar rats were ob- eight groups. The median latencies before tained from the same commercial breeder as in and after training for each group can be Experiment 1. They weighed 145-190 g at the time of the experiment. The housing, lighting, and ha- seen in Hgure 1. The influence of the posibituation period were the same as in Experiment 1. tion of the door on the step-through test Apparatus. The training cage used in Experi- latency was evaluated by calculating the ment 1 was modified so that the start compartment difference between initial step-through and and door remained the same, but the shock com- posttraining latency for each animal. Table partment was enlarged to 37 X 28 X 14 cm. This chamber was equipped with four pairs of photo- 1 lists the frequencies of positive and negaelectric cells to measure horizontal and vertical tive changes, for each treatment group activity. Two pairs of cells were located 10 cm under each door condition. The only case and 20 cm from the wall with the door, two pairs in which the door position has a significant at 3 cm from the floor, and the other two at a height of 8 cm. The cells were connected to a effect on training-to-test latency differences Sedco counter, which was controlled by a timer was in Group 1'S-ECS (Fisher exact probato register activity for 60 sec from the step- bility test, p = .025). through response. Further analysis of the step-through laThe floor of the shock chamber was composed tencies was made by Mann-Whitney U of 30 rods 1 cm apart. The shock generator and ECS apparatus were the same as in Experiment 1. tests. (All tests in this experiment are twoExperimental plan and procedure. Animals were tailed). The door-open and the door-closed divided into four groups: FS-ECS, FS-sham ECS conditions were compared in each treatment (FS-NECS), no FS-ECS (NFS-ECS), and a group group; the only difference was between that received neither footshock nor ECS (NFSNEC8). The groups of animals were housed to- FS-ECSop and FS-ECScl (U = 22, p < .02). In all other groups the position of the gether and treated in a quasi random order. The rat was placed in the start compartment in door did not influence step-through latencies. the corner opposite the opening to the shock chamThe NFS-ECS animals entered and stayed ber, facing the wall. After 20 sec, the door was in the shock compartment under both door raised and the latency to step through was recorded. When the animal had four paws in the conditions, and FS-NECS animals consistshock chamber, the door was lowered and a 3-sec, ently avoided the shock compartment. 1-mA footshock was administered. The animal Similar comparisons were made between was immediately removed and received KCS or FS-ECSop and FS-NECSop groups, and the sham ECS. The time between the termination of footshock and ECS was controlled as in Experi- difference was significant (U = 18.5, p < ment 1 by a timing device that was activated auto- .02), indicating that ECS effectively pro-
492
S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
60-
50
40
! 30-
7 7
m 5> 10-
NFS BECSoj,
NFS
NECScL
FS ECS»p
"bi
NFS
ECS il
FIGURE 1. Median step-through latency before training (dotted bars), at test 24 hr later (white bars), and at retest 7 min after initial test (striped bars). (Note that Group FS-ECSop failed to avoid on Test 1, but showed avoidance response on subsequent test; FS-ECScl avoids at both tests. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door; cl = closed door.)
duced a deficit in avoidance performance. However, there was no difference between FS-ECScl and FS-NECScl, indicating that the 30-sec delay in the start compartment was sufficient to prevent the amnestic behavior. As noted above, those animals that received NFS and ECS entered and remained in the shock compartment at retest in both the open and the closed door position ; there were no differences between these groups and their respective NFS-NECS groups, indicating no effect of ECS alone. The FS-ECSop group did not differ from the NFS-ECSop group, in step-through latency, but the difference between FS-ECScl and NFS-ECScl was significant (U = 16.5, p < .02). The percentage of animals stepping through and the mean horizontal and vertical activity measures can be seen in Table 2. Only those rats entering the shock chamber were considered in calculating the mean. All rats that stepped through spent the entire 60-sec period in the shock chamber, so the activity measure is for the same temporal duration for each rat. A t test for the horizontal movements between Groups FS-ECSop and NFS-ECSop showed the
difference to be significant, t(l7) = 3.480, p < .01. The difference between vertical measures was not quite significant, t(!7) = 2.145, p > .05. There were no differences between NFS-NECSop and NPS-ECSop or between NFS-NECScl and NtS-ECScl, assuring that the activity difference found between 1'S-ECSop and NTS-ECSop groups was likely due to the influence of the "memory" for footshock, even though this memory was not expressed in adaptive passive avoidance behavior. The median step-through latencies for each group at retest can be seen in Figure 1. The maximum possible latency at retest was 180 sec, but since there were no medians between 60 and 180, all maximum median latencies are shown in Figure 1 as 60+ in order to simplify the presentation of the data. The avoidance behavior of Group FS-ECScl carried over to the door-open position, thus confirming that the avoidance seen on Test 1 was due to an activation of the memory for footshock and the organization of an appropriate response during the preliminary 30-sec door-closed period. This memory mediated avoidance behavior on Test 2. Avoidance in Group FS-ECSop,
PASSIVE AVOIDANCE BEHAVIOR AFTER ECS TABLE 1 FREQUENCIES OF POSITIVE AND NEGATIVE CHANGES IN STEP-THROUGH LATENCIES IN EXPERIMENT 2 NFS-NECS
NFS-ECS
FS-ECS"
FS-NECS
Open Closed Open Closed Open* Closed' Open Closed
+ —
1 7
3
7
3 7
6
4
4 8
9 1
10 1
10 0
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock. * p = .025, Fisher exact probability test, significantly different from each other. The p is derived from the distribution of the four values.
which manifested the usual amnestic behavior after ECS on Test 1, tended to increase on Test 2. The difference in stepthrough latencies between this group and Group I1 S-ECScl on Test 2 was not significant, although it was on the first test. Furthermore, the difference between Group FS-ECSop and its nonfootshock control, NFS-ECSop, on Test 2 was significant (Mann-Whitney U test, two-tailed, U = 29, p < .05), whereas there was no difference on Test 1. In other words, animals having footshock and ECS and tested with the door open had step-through latencies similar to those of a group that did not receive footshock, when first tested; on a subsequent test this group showed a recovery of the memory (as measured by step-through latency), whereas the groups that had never received footshock continued to step through. The performance of all other groups did not change from Test 1 to Test 2. EXPERIMENT 3 Adams and Calhoun (1972) have observed that in spontaneous recovery from lick-suppression amnesia after ECS, animals have low response latencies, but after a few licks they stop drinking and freeze. A similar observation has been made in this laboratory for memory of bar-press suppression. Similarly, it would be of interest to know whether the difference in activity levels during the 60-sec test were evenly distributed over the period or, if there was no initial difference, whether a greater de-
493
crease in activity in the FS-ECSop group occurred as memory for footshock was reinstated. If there was no difference during the first 30-sec period, the difference appearing only after a delay, this would further confirm the hypothesis that memory retrieval activities need time and that in Experiments 1 and 2 the 30-sec "forced avoidance" provided the time for these processes to occur, thereby enabling the animal to produce the appropriate response. This experiment replicates Experiment 2, but in addition, activity after step through is monitored and recorded in 30-sec blocks. Method Subjects. The subjects were 55 male Wistar rats, weighing 150-190 g, supplied by the same breeder and fed and housed as in Experiments 1 and 2. Apparatus. The apparatus was the same as in the previous experiments except that the counter was connected to a print-out mechanism, set to print activity results every 30 sec. Procedure. Training, ECS, and testing were exactly as in Experiment 2. Since interest in this experiment centered on activity after step through, only those groups that normally would be expected to step through were included, with the exception of Group FS-ECScl. Experiment 2 showed that this group could be used as a control for avoidance learning. The first test was of 60sec duration. Animals not stepping through after 60 sec at retest were assigned a score of 60+ as before. Test 2 was continued for 180 sec to ensure that a rat's avoidance persisted; the total time spent in each compartment was also recorded. TABLE 2 MEAN ACTIVITY LEVELS IN SHOCK COMPARTMENT FOE ALL GROUPS IN EXPERIMENT 2 Group
% step through
NFS-NECSop NFS-NECScl NFS-ECSop NFS-ECScl FS-ECSop FS-ECScl FS-NECS op FS-NECScl
100 100 90 100 83 30 18 0.0
Horizontal
17
Vertical
5.4
16.6
4
19.3* 14.5 11.7* 10.5 0.0 0.0
3.6 2.9 1.7 .25 0.0 0.0
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door; cl = closed door. * .05 > p > .02, t test, significantly different from each other.
494
S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
ffl
1 Q
771
71
LLI
=
0 ECS Of.
PIOUKE 2. Median step-through latencies before training (dotted bars), at test 24 hr later (white bars), and at retest 5 min after initial test (striped bars). (Abbreviations for identification of groups: FS = footshock; ECS = electroconvulsive shock; op = open door; ol = closed door; NFS = no footshock.)
Results Training, test, and retest latencies can be seen in Figure 2. Total mean activity level during the two contiguous 30-sec periods of the first test can be seen in Table 3. First and second 30-sec totals for Groups NFS-ECSop and FS-ECSop- are shown in Table 4. As in Experiment 2, there was no difference in vertical movement. The position of the door alone at test had no effect on subsequent activity in the shock compartment, as there was no significant difference between NFS-ECSop and NFSECScl or between FS-ECSop and FS-ECScl. The activity of the animals that stepped through in Group FS-ECScl was very low, but this was not analyzed further, since only 31 % of the animals in the group entered the shock chamber. When FS-ECSop is compared with its control, NFS-ECSop, the difference is significant, p > .02, thus confirming the results of Experiment 2. When the results are viewed in terms of activity in the first 30 sec and the last 30 sec, the difference between FSECSop and NFS-ECSop is significant (.05 > p > .02) for the second 30 sec. For the
first 30 sec, there is a difference that did not reach the level of significance (.10 > p > .05). Perhaps activity measured in still smaller blocks of time would reveal no differences between groups during the first few seconds of the exposure to the shock chamber. Such evidence would further support the contention that cues associated with the response (Adams & Calhoun, 1972) as well as the environment in general can initiate or facilitate retrieval and organization of an avoidance or suppression response. Examination of the data from the retest 5 min after initial retention test confirms the results of Experiment 2— that there is a tendency to recovery from ECS for those animals (FS-ECSop) that behaved amnestically on the first test. As in Experiment 2, there was no longer a difference in stepthrough latencies between FS-ECSop and FS-ECScl (U = 73, p > .05), whereas this difference had been significant at Test 1; the difference in latencies between FSECSop and NFS-ECSop was now significant ([/ = 50, p < .02), whereas there had been no difference on Test 1 for these two groups. It should be noted that on a retest trial that lasted 180 sec, the total time spent in each chamber was a more appropriate index of memory than step-through latency. Animals that are recovering memory on this trial tended to move from shock chamber to safe chamber, a behavior not usually observed in nonfootshocked animals (see also Sara, 1973a, 1973b). Therefore, MannTABLE 3 MEAN ACTIVITY LEVELS IN SHOCK COMPARTMENT IN EXPERIMENT 3 Group
% step through
Horizontal
Vertical
NFS-ECSop NFS-ECScl FS-ECSop FS-ECScl
100 100
26* 26 14*
10.2 8.8
75 31
7.5
7.2 7.8
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door; cl = closed door. — * .05 > p > .02, i test, significantly different from each other.
PASSIVE-AVOIDANCE BEHAVIOR AFTER ECS
Whitney comparisons were made on the total time spent in the shock chamber during a 3-min test for all animals of the NFS groups (n = 26) and the FS groups (ra = 16) that had failed to avoid on the first test. The difference was highly significant (U = 101.5, 2 = 2.75, p = .003). DISCUSSION The principal result of these experiments is that the presence or absence of amnestic behavior after passive avoidance behavior and ECS is directly dependent upon conditions of testing. It is evident that the failure to avoid of Group FS-ECSop cannot be due to consolidation failure since Group I'SECScl, receiving exactly the same training and ECS treatment, did not exhibit this amnestic behavior when the step-through response was prevented for 30 sec. Furthermore, this adaptive behavior cannot be attributed to new information about response contingencies since no step-through response is made and the animal is exposed to neither shock chamber before the expression of avoidance behavior. The results support the point of view that memory traces survive ECS but in a primitive form, which must be integrated into existing functional systems (see Sara & Lefevre, 1973). This memory elaboration (Lewis, 1969) or integration probably takes place at least partially after learning, and the amnestic treatment prevents this activity. But the organization of the traces can take place at a time after learning if triggered by an appropriate stimulus (see Lewis & Nicolas, 1973; Sara, 1973a, 1973b). Retrieval activity could involve such a treatment of existing information. Presumably, animals that did not elaborate the training experience after learning because of ECS would need more time at the moment of retrieval in order to use this information to produce the appropriate response (avoidance). The 30-sec doorclosed period provides this retrieval time. Retest The fact that the FS-ECScl group continued to avoid on a second test (Experiment 2), with the door open, further supports the interpretation that dynamic memory
495
TABLE 4 MEAN 30-SEC HORIZONTAL ACTIVITY IN EXPERIMENT 4 Group
0-30 sec
31-60 sec
NFS -ECS op FS-ECSop
16.8
9.3* 4.3*
10.0
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door. * .05 > p > .02, two-tailed t test, significantly different from each other.
organization is involved and avoidance is not simply an effect of the door-open position or step-through latency per se. It should be noted that the amnestic group, FSECSop, had a greater tendency to avoid on Test 2 than on Test 1, indicating an increasing capacity to organize the appropriate avoidance response after exposure to the shock chamber. This phenomenon has been reported in other experiments (Quartermain et al., 1972; Sara, 1973a, 1973b) in which either one or several exposures led to increased avoidance. In the present study, the phenomenon is not as robust as was observed in the Sara (1973b) experiment, in which 90 % of the amnestic animals avoided on a second test, 4-5 min after the first. The difference could be due to slight changes in training procedure or to the small difference in the interval between tests. It has been recently demonstrated that retention of passive avoidance is biphasic (Zerbolio, 1971) and that the ECS efficacy depends on the dynamic state of the memory after training. There seems to be a critical period for giving ECS to produce amnesia (Robustelli, Geller, & Jarvik, 1973). A similar biphasic function of retrieval activity could be operative after reinstatement treatments, which could account for the differences between the two experiments. This is currently being investigated in this laboratory. Activity level That Group FS-ECSop has an activity level in the shock chamber significantly lower than that of the other groups that stepped through supports the contention that memory deficit after ECS is not due to-
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S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
consolidation failure. It is evident that this (1973), of Adams and Calhoun (1972), and lower activity level must be mediated by a of the present experiments support the idea memory for footshock. This result can be that the integrativc activity triggered by viewed as similar to those studies that show the very testing of the animal is time deheart beat responses or defecation (Hine & pendent and that the expression of memory Paolino, 1970) after FS-ECS when the for animals that have been submitted to skeletal responses (failure to avoid) indicate amnestic treatments after learning may reamnesia. The fact that these animals pro- quire more prolonged period of such activity. duced an appropriate skeletal response on furthermore, those animals that did not subsequent tests (Experiment 2; Quarter- produce the avoidance response at the first main et al., 1972; Sara, 1973a, 1973b) after test were nevertheless distinguishable from having received no footshock indicates that nonfootshocked animals by their activity the autonomic response was not simply a in the shock compartment. These same anipartial subthrcshold memory (Gherkin, mals tended to avoid if retested 5 min after 1972; Kesner & Connor, 1974) but an un- the initial test. All of these factors tend to organized memory. The information stored support the hypothesis that ECS affects the was sufficient to mediate an appropriate capacity to use acquired information to orgaresponse without further input. Lower ac- nize an appropriate response within a limited tivity levels were probably due to freezing time period. Given enough time, the animal, behavior on the part of the IS-ECSop without any further information, is capable group. This tendency to freeze would pro- of responding adaptively. vide an explanation as to the reason the rats, A revised version of the consolidation once memory for footshock is reinstated, theory, allowing for incomplete memory nevertheless did not immediately cross the storage (Kesner & Conner, 1974), would not safe compartment. However, it remains to be seem to be adequate to deal with the data seen if a good retention group (FS-NECS) presented in this experiment. would produce this active avoidance reREFERENCES sponse when tested by being placed in the shock compartment. Adams, H., & Calhoun, K. Indices of memory Lewis and Nicolas (1973) have recently recovery following electroconvulsive shock. Physiology and Behavior, 1972, 9, 783-787. reported results that further emphasize the A. Retrograde amnesia in the chick: importance of the kind of measure of reten- Gherkin, Resistance to the reminder effect. Physiology tion used after amnestic treatments. In that and Behavior, 1972, 8, 949-955. experiment a memory deficit for active Conover, W. J. Practical nonparametric statistics. New York: Wiley, 1971. avoidance, as measured by relearning, was not evidenced in terms of number of trials to Hine, B., & Paolino, R. Retrograde amnesia: Production of skeletal but not cardiac response relearn. However, the ECS group did not gradient by electroconvulsive shock. Science, avoid on the first test trial, but the NECS 1970, 169, 1224-1226. group did. The performance of the ECS Kesner, R., & Connor, H. Cue-dependent recovery from ECS-induced amnesia: Evidence for time group was indistinguishable from the NECS dependence. Physiological Psychology, 1974, #, group on Subsequent trials. This result sup123-125. ports the contention that the ECS deficit Lewis, D. Sources of experimental amnesia. Psycannot be due to storage failure and that the chological Review, 1969, 76, 461-472. first trial with footshock acts as a reminder Lewis, D., & Nicolas, T. Amnesia for active avoidance. Physiology and Behavior, 1973, 11, 821-825. to bring the memory to expression. Lewis McGaugh, J. L., & Herz, M. J. Memory consolidaargued that this footshock trial cannot be tion. San Francisco: Albion, 1972. considered part of acquisition, as Gherkin Miller, R. R., & Springer, A. D. Induced recovery of memory in rats following electroconvulsive would suggest, because of the dramatic shock. Physiology and Behavior, 1972, 8, 645-651. change in behavior fr0m>/Trial 1 to Trial 2 (a) of relearning, something that was not seen in Miller, R. R., & Springer, A. D. Recovery from acquisition. amnesia following transcorneal electroconvulThus, the results of Lewis and Nicolas sive shock, Psychonomic Science, 1972, 28, 7-9. (b)
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Miller, R. R., & Springer, A. D. Amnesia, consoli- Sara, S. J. Progressive development of avoidance dation, and retrieval. Psychological Review, response after training ECS, and repeated testing. Bulletin of Psychonomic Society, 1973, 8, 1973, 50,69-79. 134-136. (a) Quartermain, D., MoEwen, B., & Azmitia, E. Amnesia produced by electroconvulsive shock or Sara, S. J. Recovery from hypoxia and ECS induced amnesia after a single exposure to the cycloheximide: Conditions for recovery. Science, training environment. Physiology and Behavior, 1970, 169, 683-686. 1973, 9, 85-89. (b) Quartermain, D., McEwen, B., & Azmitia, E. Recovery of memory following amnesia in the rat Sara, S. J., & Lefevre, D. Reexamination of role of familiarization in retrograde amnesia in the and mouse. Journal of Comparative and Physiorat. Journal of Comparative and Physiological logical Psychology, 1972, 79, 360-379. Psychology, 1973, 84, 361-364. Riccio, D. C., & Stikes, E. R. Persistent butmodifiable retrograde amnesia produced by hypo- Springer, A., & Miller, R. Retrieval failure induced by electroconvulsive shock: Reversal thermia. Physiology and Behavior, 1969, 4, 649with dissimilar training and recovery agents. 652. Science, 1972, Iff, 628-630. Robustelli, F., Geller, A., & Jarvik, M. Biphasicity of the time-response curve and amnesic Zerbolio, D. J. Retrograde amnesia: The first post-trial hour. Communications in Behavioral effect of electroconvulsive shock in passive Biology, 1971, 6, 25-29. avoidance conditioning. Animal Learning & Behavior, 1973, 1, 251-253. (Received July 15, 1974)
Biological Psychology
Passive Avoidance Behavior in Rats After Electroconvulsive Shock : Facilitative Effect of Response Retardation Susan J. Sara, Michele David-Remacle, and Danielle Lefevre Center for Experimental and Comparative Psychology, University of Louvain, Pellenberg, Belgium Rats were trained in a one-trial passive avoidance task and then were submitted to electroconvulsive shock (ECS) or to sham ECS. Twenty-four hours later they were tested for retention,with the door opened either immediately or 30 sec after the beginning of the test. Rats initially forced to avoid for 30 sec continued to avoid for the entire test, but the others had the usual low step-through latencies seen withECS-treated animals. Activity measures for those animals stepping through differentiated groups having received footshock from those not having footshock and ECS. A retest 5-10 min later showed "recovery" in the amnestic animals and continued avoidance behavior for those that avoided on the first test. Results are taken as evidence that ECS effects are not on memory storage but on the capacity of the animal to organize information effectively and quickly in order to produce ah adaptive response.
Recovery from the amnestic effects of subthreshold engram to provide a viable such various agents as electroconvulsive memory capable of mediating behavior shock (ECS; Miller & Springer, 1972a, (Gherkin, 1972). Such a view predicts that 1972b; Quartermain, McEwen, & Azmitia, increasing the dose of the amnestic agent 1970, 1972; Sara, 1973a), hypoxia, (Sara, will decrease the probability of reco\ery of 1973b), hypothermia (Riccio & Stikes, memory. Experimental evidence does not, 1969), or cycloheximidc (Quartermain et al., however, always support this prediction 1972) is now well established. However, (Miller & Springer, 1972b; Quartermain controversy persists as to the significance et al., 1972, Exp. 5). of this recovery phenomenon for the conThe question of whether the reminder solidation hypothesis (Kesner & Connor, treatment provides new information has 1974). If amnestic agents produce a memory been addressed by several experiments. deficit by disruption of a time-dependent Most reactivation treatments use a nontrace fixation process, as the consolidation contingent footshock as a reminder for the hypothesis holds (McGaugh & Herz, 1972), footshock reinforcement given during trainthen the effects must necessarily be perma- ing. Springer and Miller (1972) have sucnent (see Lewis, 1969). To explain recovery ceeded in reinstating memory by a dissimiwithin a consolidation framework, it must lar stressful event, but this would likewise be supposed that the amnestic agent was serve to induce a reactive physiological inadequate and that a partial trace was state similar to the training state and could formed in spite of the treatment. Recovery be construed as being new relevant informaoccurs because reminder treatments give tion in the same way that noncontingent new information that sums with the existing footshock could. Quartermain et al. (1972) and Sara (1973a, 1973b) have underlined This research was supported by "Fonds pour la the importance of the training environment Recherche Fondamentale Collective" of Belgium and by a grant from Union Chimie Beige (U.C.B.). in reinstating memory. In these experiments, The authors wish to thank C. Giurgea for advice the animal steps through during the reand svipport. minder test and is removed from the shock Requests for reprints should be sent to Susan J. chamber, having received no shock. It has Sara, Centre de Psychologie Experimental et Compare'e, University de Louvain, Pellenberg, been argued that the motor act of stepping through (and/or the shock chamber) itself Belgium. 489
490
S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
has secondary reinforcing properties after association with footshock and therefore the animal receives response contingent secondary reinforcement during the reminder test—a new item of information. The present experiment is an attempt to reinstate memory after ECS without exposing the animal to either the primary footshock or secondary (shock chamber) reinforcement. EXPERIMENT 1 Method Subjects. The subjects were 42 male Wistar rats supplied by a commercial breeder. They weighed 200-250 g at the time of the experiment, were housed in groups of 6-8 in plastic breeding cages, and had free access to food and water. The cages were located in the laboratory with a normal day/ night cycle. The animals were habituated to this environment for 1 wk before the experiment. Apparatus. The training cage consisted of a two-compartment apparatus; the large compartment, measuring 37 X 28 X 14 cm, was constructed of gray plastic material, with a gravel floor similar to that of the living cage. This large compartment was illuminated from overhead by a 100-W bulb. The small compartment was made of aluminum, measuring 10 X 10 X 10 cm. The floor was constructed of metal rods 1 cm apart. A 6 X 6 cm door with guillotine closing separated the two compartments; a shock could be delivered through the floor and cage walls of the small compartment by means of a 180-V shock generator, through a Foringer scrambler. The output current was limited by a variable series resistance; shock intensity was 1 mA for 2 sec, controlled by an automatic Sedco timing device. The ECS was delivered by means of transtemporal electrodes from a 1,200-V transformer, 50-mA shock of .35-sec duration via a 10-kQ series resistance. The delay between footshock offset and ECS onset was 8 sec, controlled by a Sedco timing device that triggered an auditory signal to the experimenter. Experimental plan and procedure. Treatment of all animals during the training was identical. The rat was placed in the large compartment with the door leading to the small compartment closed. After 20 sec, the guillotine door was raised and the latency to step through was noted. When the animal had all four paws in the small compartment, the door was lowered and a 2-sec inescapable footshock was administered. The rat was immediately removed from the shock compartment. Each animal was restrained and electrodes were applied to the temporal area just behind the eyes. The electrodes were wet with saline solution mixed with red ink in order to verify that the electrodes had been correctly placed. Twenty-two animals received ECS and 20 sham ECS (no current).
Twenty-four hours later the rats were tested individually by placing them in the large compartment facing away from the closed door. For 11 ECS and 10 sham-ECS animals, the door was opened immediately. For the remaining 11 ECS and 10 sham-ECS animals, there was a 30-sec delay in opening the door. Thus, these animals were forced to "avoid" the small compartment formore than 30 sec at the beginning of the testing period. In this way four groups were generated: sham ECS and ECS, tested with the door immediately open (Groups ECSop and NECSop), and sham ECS and ECS, tested with the door closed for 30 sec (Groups NECScl and ECScl). The step-through latency after the door was opened was recorded for each rat. The testing period 24 hr after training lasted for 3 min after the door was opened.
Results and Discussion In both NECS groups all 10 animals avoided for the full 180-sec testing period. Ten animals stepped through and one avoided in the ECSop condition, and six stepped through and five avoided in Group ECScl. The difference between those two groups is significant (Fisher exact probability, p = .032). It should be noted, however, that the effect is only partial, since five of the ECScl stepped through, but no animals in either NECS group stepped through. Furthermore, the difference between the ECScl group and the NECScl group is significant (Fisher, p = .023). The results suggest that, although the position of the door at the beginning of the testing period is of no consequence for the animals that were trained but not convulsed, it is an important factor in the avoidance performance of those animals that are convulsed after footshock. If the step-through response is prevented for at least 30 sec (Group ECScl), there is a significantly greater tendency to avoid the shock compartment when compared with the ECS group whose step-through response is not delayed (Group ECSop). EXPERIMENT 2 It is possible that the position of the door of the shock compartment at testing could cause higher latencies in any group that would otherwise be expected to have low latencies, whether these low latencies are due to ECS treatment or absence of footshock reinforcement at training. This ex-
PASSIVE AVOIDANCE BEHAVIOR AFTER ECS
491
periment compares the effect of a 30-sec matically with the footshock and that triggered delay on an ECS group with the effect on an auditory signal to the experimenter 8 sec after termination. All animals were kept intwo other groups expected to have low test footshock dividually in small plastic cages for 15 min after latencies because of no footshock. The treatment and were then returned to the home motor activity in the shock chamber after a cage. Before testing, the groups were subdivided step-through response was monitored, and to permit two testing conditions for each training the total time spent in the shock chamber treatment. Half the animals were tested with the door open immediately and half with a 30-sec during a 60-sec period was recorded for each delay in door opening. If the rat avoided for 60 group. The purpose of these measures was sec, it was removed and assigned a score of 60. For to provide additional behavioral indices those animals stepping through, the latency was that might reveal memory of training foot- noted and the test was continued for 60 sec after the step-through response in order to have the shock, even for these animals that failed same duration of measurement of activity for each to produce the avoidance response. rat. If, indeed, the avoidance behavior of Animals were retested with the door in the open Group FS-ECScl is mediated by an orga- position (5-10 min after the first retention test); nized memory, the expression of this memory this second test lasted 180 sec. should be possible when tested with the door Results open. So all animals were retested 5-10 min after the first retention test. A slippage test (Conover, 1971) was performed on the initial step-through latencies, Method and there were no differences among the Subjects. Eighty-one male Wistar rats were ob- eight groups. The median latencies before tained from the same commercial breeder as in and after training for each group can be Experiment 1. They weighed 145-190 g at the time of the experiment. The housing, lighting, and ha- seen in Hgure 1. The influence of the posibituation period were the same as in Experiment 1. tion of the door on the step-through test Apparatus. The training cage used in Experi- latency was evaluated by calculating the ment 1 was modified so that the start compartment difference between initial step-through and and door remained the same, but the shock com- posttraining latency for each animal. Table partment was enlarged to 37 X 28 X 14 cm. This chamber was equipped with four pairs of photo- 1 lists the frequencies of positive and negaelectric cells to measure horizontal and vertical tive changes, for each treatment group activity. Two pairs of cells were located 10 cm under each door condition. The only case and 20 cm from the wall with the door, two pairs in which the door position has a significant at 3 cm from the floor, and the other two at a height of 8 cm. The cells were connected to a effect on training-to-test latency differences Sedco counter, which was controlled by a timer was in Group 1'S-ECS (Fisher exact probato register activity for 60 sec from the step- bility test, p = .025). through response. Further analysis of the step-through laThe floor of the shock chamber was composed tencies was made by Mann-Whitney U of 30 rods 1 cm apart. The shock generator and ECS apparatus were the same as in Experiment 1. tests. (All tests in this experiment are twoExperimental plan and procedure. Animals were tailed). The door-open and the door-closed divided into four groups: FS-ECS, FS-sham ECS conditions were compared in each treatment (FS-NECS), no FS-ECS (NFS-ECS), and a group group; the only difference was between that received neither footshock nor ECS (NFSNEC8). The groups of animals were housed to- FS-ECSop and FS-ECScl (U = 22, p < .02). In all other groups the position of the gether and treated in a quasi random order. The rat was placed in the start compartment in door did not influence step-through latencies. the corner opposite the opening to the shock chamThe NFS-ECS animals entered and stayed ber, facing the wall. After 20 sec, the door was in the shock compartment under both door raised and the latency to step through was recorded. When the animal had four paws in the conditions, and FS-NECS animals consistshock chamber, the door was lowered and a 3-sec, ently avoided the shock compartment. 1-mA footshock was administered. The animal Similar comparisons were made between was immediately removed and received KCS or FS-ECSop and FS-NECSop groups, and the sham ECS. The time between the termination of footshock and ECS was controlled as in Experi- difference was significant (U = 18.5, p < ment 1 by a timing device that was activated auto- .02), indicating that ECS effectively pro-
492
S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
60-
50
40
! 30-
7 7
m 5> 10-
NFS BECSoj,
NFS
NECScL
FS ECS»p
"bi
NFS
ECS il
FIGURE 1. Median step-through latency before training (dotted bars), at test 24 hr later (white bars), and at retest 7 min after initial test (striped bars). (Note that Group FS-ECSop failed to avoid on Test 1, but showed avoidance response on subsequent test; FS-ECScl avoids at both tests. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door; cl = closed door.)
duced a deficit in avoidance performance. However, there was no difference between FS-ECScl and FS-NECScl, indicating that the 30-sec delay in the start compartment was sufficient to prevent the amnestic behavior. As noted above, those animals that received NFS and ECS entered and remained in the shock compartment at retest in both the open and the closed door position ; there were no differences between these groups and their respective NFS-NECS groups, indicating no effect of ECS alone. The FS-ECSop group did not differ from the NFS-ECSop group, in step-through latency, but the difference between FS-ECScl and NFS-ECScl was significant (U = 16.5, p < .02). The percentage of animals stepping through and the mean horizontal and vertical activity measures can be seen in Table 2. Only those rats entering the shock chamber were considered in calculating the mean. All rats that stepped through spent the entire 60-sec period in the shock chamber, so the activity measure is for the same temporal duration for each rat. A t test for the horizontal movements between Groups FS-ECSop and NFS-ECSop showed the
difference to be significant, t(l7) = 3.480, p < .01. The difference between vertical measures was not quite significant, t(!7) = 2.145, p > .05. There were no differences between NFS-NECSop and NPS-ECSop or between NFS-NECScl and NtS-ECScl, assuring that the activity difference found between 1'S-ECSop and NTS-ECSop groups was likely due to the influence of the "memory" for footshock, even though this memory was not expressed in adaptive passive avoidance behavior. The median step-through latencies for each group at retest can be seen in Figure 1. The maximum possible latency at retest was 180 sec, but since there were no medians between 60 and 180, all maximum median latencies are shown in Figure 1 as 60+ in order to simplify the presentation of the data. The avoidance behavior of Group FS-ECScl carried over to the door-open position, thus confirming that the avoidance seen on Test 1 was due to an activation of the memory for footshock and the organization of an appropriate response during the preliminary 30-sec door-closed period. This memory mediated avoidance behavior on Test 2. Avoidance in Group FS-ECSop,
PASSIVE AVOIDANCE BEHAVIOR AFTER ECS TABLE 1 FREQUENCIES OF POSITIVE AND NEGATIVE CHANGES IN STEP-THROUGH LATENCIES IN EXPERIMENT 2 NFS-NECS
NFS-ECS
FS-ECS"
FS-NECS
Open Closed Open Closed Open* Closed' Open Closed
+ —
1 7
3
7
3 7
6
4
4 8
9 1
10 1
10 0
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock. * p = .025, Fisher exact probability test, significantly different from each other. The p is derived from the distribution of the four values.
which manifested the usual amnestic behavior after ECS on Test 1, tended to increase on Test 2. The difference in stepthrough latencies between this group and Group I1 S-ECScl on Test 2 was not significant, although it was on the first test. Furthermore, the difference between Group FS-ECSop and its nonfootshock control, NFS-ECSop, on Test 2 was significant (Mann-Whitney U test, two-tailed, U = 29, p < .05), whereas there was no difference on Test 1. In other words, animals having footshock and ECS and tested with the door open had step-through latencies similar to those of a group that did not receive footshock, when first tested; on a subsequent test this group showed a recovery of the memory (as measured by step-through latency), whereas the groups that had never received footshock continued to step through. The performance of all other groups did not change from Test 1 to Test 2. EXPERIMENT 3 Adams and Calhoun (1972) have observed that in spontaneous recovery from lick-suppression amnesia after ECS, animals have low response latencies, but after a few licks they stop drinking and freeze. A similar observation has been made in this laboratory for memory of bar-press suppression. Similarly, it would be of interest to know whether the difference in activity levels during the 60-sec test were evenly distributed over the period or, if there was no initial difference, whether a greater de-
493
crease in activity in the FS-ECSop group occurred as memory for footshock was reinstated. If there was no difference during the first 30-sec period, the difference appearing only after a delay, this would further confirm the hypothesis that memory retrieval activities need time and that in Experiments 1 and 2 the 30-sec "forced avoidance" provided the time for these processes to occur, thereby enabling the animal to produce the appropriate response. This experiment replicates Experiment 2, but in addition, activity after step through is monitored and recorded in 30-sec blocks. Method Subjects. The subjects were 55 male Wistar rats, weighing 150-190 g, supplied by the same breeder and fed and housed as in Experiments 1 and 2. Apparatus. The apparatus was the same as in the previous experiments except that the counter was connected to a print-out mechanism, set to print activity results every 30 sec. Procedure. Training, ECS, and testing were exactly as in Experiment 2. Since interest in this experiment centered on activity after step through, only those groups that normally would be expected to step through were included, with the exception of Group FS-ECScl. Experiment 2 showed that this group could be used as a control for avoidance learning. The first test was of 60sec duration. Animals not stepping through after 60 sec at retest were assigned a score of 60+ as before. Test 2 was continued for 180 sec to ensure that a rat's avoidance persisted; the total time spent in each compartment was also recorded. TABLE 2 MEAN ACTIVITY LEVELS IN SHOCK COMPARTMENT FOE ALL GROUPS IN EXPERIMENT 2 Group
% step through
NFS-NECSop NFS-NECScl NFS-ECSop NFS-ECScl FS-ECSop FS-ECScl FS-NECS op FS-NECScl
100 100 90 100 83 30 18 0.0
Horizontal
17
Vertical
5.4
16.6
4
19.3* 14.5 11.7* 10.5 0.0 0.0
3.6 2.9 1.7 .25 0.0 0.0
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door; cl = closed door. * .05 > p > .02, t test, significantly different from each other.
494
S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
ffl
1 Q
771
71
LLI
=
0 ECS Of.
PIOUKE 2. Median step-through latencies before training (dotted bars), at test 24 hr later (white bars), and at retest 5 min after initial test (striped bars). (Abbreviations for identification of groups: FS = footshock; ECS = electroconvulsive shock; op = open door; ol = closed door; NFS = no footshock.)
Results Training, test, and retest latencies can be seen in Figure 2. Total mean activity level during the two contiguous 30-sec periods of the first test can be seen in Table 3. First and second 30-sec totals for Groups NFS-ECSop and FS-ECSop- are shown in Table 4. As in Experiment 2, there was no difference in vertical movement. The position of the door alone at test had no effect on subsequent activity in the shock compartment, as there was no significant difference between NFS-ECSop and NFSECScl or between FS-ECSop and FS-ECScl. The activity of the animals that stepped through in Group FS-ECScl was very low, but this was not analyzed further, since only 31 % of the animals in the group entered the shock chamber. When FS-ECSop is compared with its control, NFS-ECSop, the difference is significant, p > .02, thus confirming the results of Experiment 2. When the results are viewed in terms of activity in the first 30 sec and the last 30 sec, the difference between FSECSop and NFS-ECSop is significant (.05 > p > .02) for the second 30 sec. For the
first 30 sec, there is a difference that did not reach the level of significance (.10 > p > .05). Perhaps activity measured in still smaller blocks of time would reveal no differences between groups during the first few seconds of the exposure to the shock chamber. Such evidence would further support the contention that cues associated with the response (Adams & Calhoun, 1972) as well as the environment in general can initiate or facilitate retrieval and organization of an avoidance or suppression response. Examination of the data from the retest 5 min after initial retention test confirms the results of Experiment 2— that there is a tendency to recovery from ECS for those animals (FS-ECSop) that behaved amnestically on the first test. As in Experiment 2, there was no longer a difference in stepthrough latencies between FS-ECSop and FS-ECScl (U = 73, p > .05), whereas this difference had been significant at Test 1; the difference in latencies between FSECSop and NFS-ECSop was now significant ([/ = 50, p < .02), whereas there had been no difference on Test 1 for these two groups. It should be noted that on a retest trial that lasted 180 sec, the total time spent in each chamber was a more appropriate index of memory than step-through latency. Animals that are recovering memory on this trial tended to move from shock chamber to safe chamber, a behavior not usually observed in nonfootshocked animals (see also Sara, 1973a, 1973b). Therefore, MannTABLE 3 MEAN ACTIVITY LEVELS IN SHOCK COMPARTMENT IN EXPERIMENT 3 Group
% step through
Horizontal
Vertical
NFS-ECSop NFS-ECScl FS-ECSop FS-ECScl
100 100
26* 26 14*
10.2 8.8
75 31
7.5
7.2 7.8
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door; cl = closed door. — * .05 > p > .02, i test, significantly different from each other.
PASSIVE-AVOIDANCE BEHAVIOR AFTER ECS
Whitney comparisons were made on the total time spent in the shock chamber during a 3-min test for all animals of the NFS groups (n = 26) and the FS groups (ra = 16) that had failed to avoid on the first test. The difference was highly significant (U = 101.5, 2 = 2.75, p = .003). DISCUSSION The principal result of these experiments is that the presence or absence of amnestic behavior after passive avoidance behavior and ECS is directly dependent upon conditions of testing. It is evident that the failure to avoid of Group FS-ECSop cannot be due to consolidation failure since Group I'SECScl, receiving exactly the same training and ECS treatment, did not exhibit this amnestic behavior when the step-through response was prevented for 30 sec. Furthermore, this adaptive behavior cannot be attributed to new information about response contingencies since no step-through response is made and the animal is exposed to neither shock chamber before the expression of avoidance behavior. The results support the point of view that memory traces survive ECS but in a primitive form, which must be integrated into existing functional systems (see Sara & Lefevre, 1973). This memory elaboration (Lewis, 1969) or integration probably takes place at least partially after learning, and the amnestic treatment prevents this activity. But the organization of the traces can take place at a time after learning if triggered by an appropriate stimulus (see Lewis & Nicolas, 1973; Sara, 1973a, 1973b). Retrieval activity could involve such a treatment of existing information. Presumably, animals that did not elaborate the training experience after learning because of ECS would need more time at the moment of retrieval in order to use this information to produce the appropriate response (avoidance). The 30-sec doorclosed period provides this retrieval time. Retest The fact that the FS-ECScl group continued to avoid on a second test (Experiment 2), with the door open, further supports the interpretation that dynamic memory
495
TABLE 4 MEAN 30-SEC HORIZONTAL ACTIVITY IN EXPERIMENT 4 Group
0-30 sec
31-60 sec
NFS -ECS op FS-ECSop
16.8
9.3* 4.3*
10.0
Note. Abbreviations for identification of groups: N = no; FS = footshock; ECS = electroconvulsive shock; op = open door. * .05 > p > .02, two-tailed t test, significantly different from each other.
organization is involved and avoidance is not simply an effect of the door-open position or step-through latency per se. It should be noted that the amnestic group, FSECSop, had a greater tendency to avoid on Test 2 than on Test 1, indicating an increasing capacity to organize the appropriate avoidance response after exposure to the shock chamber. This phenomenon has been reported in other experiments (Quartermain et al., 1972; Sara, 1973a, 1973b) in which either one or several exposures led to increased avoidance. In the present study, the phenomenon is not as robust as was observed in the Sara (1973b) experiment, in which 90 % of the amnestic animals avoided on a second test, 4-5 min after the first. The difference could be due to slight changes in training procedure or to the small difference in the interval between tests. It has been recently demonstrated that retention of passive avoidance is biphasic (Zerbolio, 1971) and that the ECS efficacy depends on the dynamic state of the memory after training. There seems to be a critical period for giving ECS to produce amnesia (Robustelli, Geller, & Jarvik, 1973). A similar biphasic function of retrieval activity could be operative after reinstatement treatments, which could account for the differences between the two experiments. This is currently being investigated in this laboratory. Activity level That Group FS-ECSop has an activity level in the shock chamber significantly lower than that of the other groups that stepped through supports the contention that memory deficit after ECS is not due to-
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S. J. SARA, M. DAVID-REMACLE, AND D. LEFEVRE
consolidation failure. It is evident that this (1973), of Adams and Calhoun (1972), and lower activity level must be mediated by a of the present experiments support the idea memory for footshock. This result can be that the integrativc activity triggered by viewed as similar to those studies that show the very testing of the animal is time deheart beat responses or defecation (Hine & pendent and that the expression of memory Paolino, 1970) after FS-ECS when the for animals that have been submitted to skeletal responses (failure to avoid) indicate amnestic treatments after learning may reamnesia. The fact that these animals pro- quire more prolonged period of such activity. duced an appropriate skeletal response on furthermore, those animals that did not subsequent tests (Experiment 2; Quarter- produce the avoidance response at the first main et al., 1972; Sara, 1973a, 1973b) after test were nevertheless distinguishable from having received no footshock indicates that nonfootshocked animals by their activity the autonomic response was not simply a in the shock compartment. These same anipartial subthrcshold memory (Gherkin, mals tended to avoid if retested 5 min after 1972; Kesner & Connor, 1974) but an un- the initial test. All of these factors tend to organized memory. The information stored support the hypothesis that ECS affects the was sufficient to mediate an appropriate capacity to use acquired information to orgaresponse without further input. Lower ac- nize an appropriate response within a limited tivity levels were probably due to freezing time period. Given enough time, the animal, behavior on the part of the IS-ECSop without any further information, is capable group. This tendency to freeze would pro- of responding adaptively. vide an explanation as to the reason the rats, A revised version of the consolidation once memory for footshock is reinstated, theory, allowing for incomplete memory nevertheless did not immediately cross the storage (Kesner & Conner, 1974), would not safe compartment. However, it remains to be seem to be adequate to deal with the data seen if a good retention group (FS-NECS) presented in this experiment. would produce this active avoidance reREFERENCES sponse when tested by being placed in the shock compartment. Adams, H., & Calhoun, K. Indices of memory Lewis and Nicolas (1973) have recently recovery following electroconvulsive shock. Physiology and Behavior, 1972, 9, 783-787. reported results that further emphasize the A. Retrograde amnesia in the chick: importance of the kind of measure of reten- Gherkin, Resistance to the reminder effect. Physiology tion used after amnestic treatments. In that and Behavior, 1972, 8, 949-955. experiment a memory deficit for active Conover, W. J. Practical nonparametric statistics. New York: Wiley, 1971. avoidance, as measured by relearning, was not evidenced in terms of number of trials to Hine, B., & Paolino, R. Retrograde amnesia: Production of skeletal but not cardiac response relearn. However, the ECS group did not gradient by electroconvulsive shock. Science, avoid on the first test trial, but the NECS 1970, 169, 1224-1226. group did. The performance of the ECS Kesner, R., & Connor, H. Cue-dependent recovery from ECS-induced amnesia: Evidence for time group was indistinguishable from the NECS dependence. Physiological Psychology, 1974, #, group on Subsequent trials. This result sup123-125. ports the contention that the ECS deficit Lewis, D. Sources of experimental amnesia. Psycannot be due to storage failure and that the chological Review, 1969, 76, 461-472. first trial with footshock acts as a reminder Lewis, D., & Nicolas, T. Amnesia for active avoidance. Physiology and Behavior, 1973, 11, 821-825. to bring the memory to expression. Lewis McGaugh, J. L., & Herz, M. J. Memory consolidaargued that this footshock trial cannot be tion. San Francisco: Albion, 1972. considered part of acquisition, as Gherkin Miller, R. R., & Springer, A. D. Induced recovery of memory in rats following electroconvulsive would suggest, because of the dramatic shock. Physiology and Behavior, 1972, 8, 645-651. change in behavior fr0m>/Trial 1 to Trial 2 (a) of relearning, something that was not seen in Miller, R. R., & Springer, A. D. Recovery from acquisition. amnesia following transcorneal electroconvulThus, the results of Lewis and Nicolas sive shock, Psychonomic Science, 1972, 28, 7-9. (b)
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