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Extended Temporal Gradient for the Retrograde and Anterograde Amnesia Produced by Lbotenate Entorhinal Cortex Lesions in Mice

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Extended Temporal Gradient for the Retrograde and Anterograde Amnesia Produced by Lbotenate Entorhinal Cortex Lesions in Mice The Journal of Neuroscience, April 1993, 13(4): 1759-1766 Extended Temporal Gradient for the Retrograde and Anterograde Amnesia Produced by lbotenate Entorhinal Cortex Lesions in Mice Yoon H. Cho, Daniel Beracochea, and Robert Jaffard Laboratoire de Neurosciences Comportementales et Cognitives, CNRS URA 339, UniversitB de Bordeaux I, 33405 Talence CQdBx, France Effects of ibotenic entorhinal cortex (EC) lesions on both extend back as far as several years with an identifiable gradient, retrograde and anterograde amnesia in mice were assessed recent memoriesbeing selectively impaired while very remote using two-choice discrimination tasks learned at different memories remain intact. These findings provide evidence for a intervals before surgery in two eight-arm radial mazes. The consolidation processthat lasts considerably longer than the results indicated that EC-lesioned mice were severely im- minutes initially envisioned (for reviews, seePolster et al., 1991; paired in postoperative retention of discrimination problems Squire, 1992). learned 3 d or 2 weeks prior to surgery, but showed no deficit More precisely, this suggeststhat the creation of permanent on problems learned between 4, and up to 6 weeks before memoriesrequires a gradual transformation in the organization surgery, as compared to sham-operated controls. When of memory traces rather than a simple fixation process.Thus, trained on a novel two-choice discrimination problem (not in line with this idea, it hasbeen proposedthat limbic structures acquired preoperatively), experimental subjects demon- remain involved for a lengthy period of time in the organization strated quite normal rates of acquisition, but were impaired ofenduring extra-limbic memory tracesthat ultimately become in learning its reversal. Furthermore, they exhibited a faster capableofindependently supporting the retrieval of information rate of forgetting (anterograde amnesia) relative to controls (Squire et al., 1984). over a 2-week retention interval. These results indicate that The difficulties inherent to neuropsychologicalstudies aimed approximately 4 weeks is required before memory for a two- at testing memoriesconcerning the remote past, and in address- choice spatial discrimination problem no longer depends on ing the question of how these phenomenaare organized in the the integrity of the entorhinal cortex, and suggests that, be- brain, have recently led to the development of a number of yond this time, an EC-independent memory storage system animal models. A seriesof studieshave succeededin attempts is capable of supporting the retrieval of information. The to describe a temporal gradient in retrograde amnesiaas evi- data, together with complementary behavioral results, are dence for a long-term consolidation process(Squire and Spanis, discussed in the context of current theories of memory stor- 1984; Salmon et al., 1987; Sutherland et al., 1987); however, age. similar neuropsychologicalstudies have failed to find evidence [Key words: retrograde amnesia, entorhinal cortex, ibo- for such a temporal gradient (Dean and Weiskrantz, 1974; Salm- tenate lesions, spatial reference memory, radialmaze, mice] on et al., 1987). The present experiment was mainly aimed at determining whether ibotenate entorhinal cortex (EC) lesionsin mice could The human amnesicsyndrome is characterized by a severe loss produce differential and temporally graded retrograde amnesia of memory for events that occur subsequentto brain insult for successivetwo-choice discrimination problems,each learned (anterograde amnesia), together with a much more variable at different time periods prior to surgery. Basically, the method memory impairment for premorbid events (retrograde amne- was the sameas that previously used by Dean and Weiskrantz sia). (1974) and more recently by Zola-Morgan and Squire (1990). Neuropsychological studies of both anterograde and retro- In addition, anterograde amnesia was assessedboth by post- grade amnesiahave been useful in addressingthe memory con- operative learning and by ratesof forgetting for similar problems solidation issue.Thus, it has been suggestedthat, at least for as those learned preoperatively. bitemporal lesionsor dysfunction, anterograde amnesia could be attributed to a consolidation deficit, that is, a failure to trans- Materials and Methods form short-term into long-term memory traces. More impor- Subjects tantly, these studieshave shown that retrograde amnesiacould Twenty-oneadult mice of the BALBK by JIco strain were used. During training, the mice were kept on a food deprivation schedule so that their body weight was maintained at 80-84% of their free-feeding weight. Received Feb. 19, 1992; revised Aug. 27, 1992; accepted Oct. 29, 1992. This work was supported by the Centre National de la Recherche Scientifique Apparatus and the Fondation pour la Recherche M&licale. We wish to thank Professor L. E. Jarrard for his advice and evaluation of ibotenic acid entorhinal cortex lesions. Two identical elevated radial mazes (A and B), located in two different A part of these results were presented at the 2 1st Annual Society for Neuroscience rooms decorated with different sets of pictures and objects, were used. Meeting, New Orleans, 199 1. Each maze was composed of a circular platform (30 cm diameter) from Correspondence should be addressed to Y. H. Cho, Department of Psychology, which eight arms (50 cm long) radiated in a symmetrical fashion. Bach University of Utah, Salt Lake City, UT 84 112. arm was fitted with a door at the entrance and a food cup at the other Copyright 0 1993 Society for Neuroscience 0270-6474/93/131759-08$05.00/O extremity. In maze B, each arm was differentiated by inserts of different 1760 Cho et al. * Retrograde Amnesia and Entorhinal Cortex Maze A Maze B + Pair Al PiA PairBl Pair B2 Pair B4 Pair B4 Pair B4 Reversal long-teml Retention Figure1. Behavioral procedure used for studying retrograde and anterograde amnesia following ibotenate EC lesion. black and white visual cues placed on the floor so that the animals could side-strategies to resolve the problems. Half of each of the three sub- learn the discrimination tasks on the bases of both extramaze (place) groups was attributed to the experimental group and the other half to and intramaze cues. the sham-operated group. Postoperativetest&g. Retention and reacquisition of the preopera- tively learned pairs (Bl-B3) were assessed in maze B. In each daily session, the three pairs were presented eight times each in a mixed order. Behavioral testing Upon completion of testing in maze B, animals were given a single Preoperativetraining. The general procedure is summarized in Figure retention session for the two pairs (Al and A2) learned preoperatively 1. All mice were successively trained on five two-choice discrimination in maze A, each presented eight times in a mixed order. Postoperative problems. For each of the five problems, two adjacent arms were pre- performance in maze B was assessed on each pair (Bl-B3) by the per- sented, one of which was always baited. Animals were given daily ses- centage of correct responses recorded on both the first eight trials (first sions of 16 trials each as follows. At the start of a trial, the mouse was session) and the first 16 trials (first two sessions). Moreover, the number placed on the central platform, and after 15 set, the doors giving access of trials needed to achieve a criterion of five correct responses in five to the first pair of selected arms were opened simultaneously. Once the consecutive trials was also determined. The rate of complete reacquisi- mouse had reached the food tray (baited or not) at the end of the chosen tion was assessed by the number of trials needed to reachieve the 13/ arm, it was allowed to return to the central platform where it was again 16 criterion used for preoperative acquisition. Retention scores in maze confined. After 15 set, the same two doors were opened for the next A (Al + A2) were assessed by the percentage of correct responses trial. Training continued (three to five daily sessions) until the animal recorded on both the first eight and 16 trials of the single retention reached a criterion of 13 correct choices in the same 16-trial session. session. Training for the second problem (second pair of arms), A2, commenced Postoperativelearning, reversal, and retentiontesting (problem B4). the next day and was continued until animals attained the same criterion This experiment was designed to evaluate the anterograde effects of EC of performance on the second pair of arms. The next set of three dis- lesions on learning, reversal, and long-term retention of a new pair. crimination problems was carried out using maze B. Thus, at each of Thus, after completion of postoperative retention tests, animals were five time periods prior to surgery, animals had learned a different two- trained on the final (fourth) pair in maze B (B4) according to the same choice discrimination problem. In maze A only, training for the second procedure as that described for preoperative training. Once the mouse problem (A2) began the day after the end of discrimination training for had reached the 13/ 16 criterion, the baited arm was reversed and train- the first pair of arms. Moreover, animals were given an additional ing continued until the animal reattained the same criterion. Two weeks session the following day after attaining criterion on pair A2 where both later, retention for discrimination reversal was assessed in a single ses- pairs (Al + A2) were presented in a mixed order. This last session, sion of 16 trials. aimed at familiarizing mice with the mixed-testing procedure used post- Contributionof intramazecues to discriminationperformance. This operatively in maze B, was given about 6.5 weeks before surgery. Two last experiment was designed to determine the extent to which subjects weeks later (4.5 weeks before surgery) animals began the first pair (Bl) used intramaze cues in discrimination. Accordingly, control animals (n in maze B; they were subsequently trained on pairs B2 and B3, at around = 6) and EC-lesioned mice (n = 12) were trained concurrently on the 2.5 weeks and 4 d before surgery, respectively.
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