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The Role of the Hippocampus in Declarative Memory

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The Role of the Hippocampus in Declarative Memory LETTER TO THE EDITORS The Role of the Hippocampus in gyrus, and subiculum to include the adjacent entorhinal cortex and parahippocampal gyrus (the Htgroup) and Declarative Memory: A Comment on the perirhinal cortex and anterior entorhinal cortex (the Zola-Morgan, Squire, and Ramus (1994) H+ + group). In this note I will not address the broader claims the authors make about the role of structures be- Lynn Nadel yond those involved in the H group, nor will I address the proposed naturc of declarative memory; I have ad- dressed some of these points elsewhere (Nadel, 1991, Department of Psychology and ARL Neural Systems, 1992, 1994). Memory and Aging Division, University of Arizona, This commentary is focused on the data from the Tucson, Arizona eight monkeys in the H group, and what can be con- cluded from these data about the hnctions of the hip- pocampus. Of these animals, four received radiofre- In a recent article (Zola-Morgan et al., 1994), a set of data were presented quency lesions (H-RF) and four received ischemic lesions in support of the view that “damage limited to the hippocampus proper, the (H-ISC). The authors analyzed performance of the le- dentate and the subicular complex causes significant memory im- gyrus, sioned animals on a battery of five tasks, given to all the pairment” (p. 493). These data come from a series of elegant studies utiliz- animals in sequence: trial-unique delayed nonmatching ing monkeys tested on a standard battery of tasks, several of which are taken to sample (DNMTS-l), pattern discrimination, delayed as requiring the involvement of a proposed declarative memory system, a hy- retention of object discriminations (OBJECT), concur- pothetical construct composed in humans of memory for facts and events rent discrimination learning, and a retest of trial-unique that can be called up to conscious recollection. This claim, and these data, delayed nonmatching to sample (DNMTS-2). Based on are critical in evaluating the current debate between proponents of cogni- correlational analyses and a factor analysis of these data, tivelspatial map theory (e.g., O’Keefe and Conway, 1978; Nadel, 1991; it was concluded that only the DNMTS task and delayed O’Keefe, 1991) and those of declarative theory (e.g., Squire, 1992; Cohen retention of object discrimination unambiguously tapped and Eichenbaum, 1993). For that reason, the present note seeks to clari@ declarative memory. Data from these two tasks were then exactly what can, and cannot, be concluded from the reported results. used in an analysis of the extent to which damage in var- To begin, it is important to clarify the distinction between cognitive ious parts of the medial temporal lobe caused deficits in map theory and declarative memory theory. Both theories have addressed declarative memory. In order to do this a single z score the selective role that the hippocampus plays in memory. Both theories was computed for each monkey, using the data from both agree that there are many forms of memory that do not require the func- DNMTS-1 and DNMTS-2 and the OBJECT task. The tioning of the hippocampus. The cognitive map theory asserts that the hip- data from DNMTS were treated in the following way: pocampus is essential only for the kind of memory that incorporates spa- One measure was derived from the number of trials to tial information, which includes memory for places, environments, or reach criterion (90/100) on DNMTS-1, during which spatial contexts and episodes, and for the exploratory behavior during an 8-s retention interval was used. Another measure was which animals incorporate novel information into their cognitive maps. derived from the percent correct scores obtained during Declarative theory is silent about exploration of novelty, and asserts that 100 post-criterion trials given with 15-s retention inter- the stated categories of spatial memory are merely very good examples of val, 100 such trials given with 60-s retention interval, the broader category of memories involving facts and events. The two the- and 50 such trials given with 10-min retention interval. ories diverge on the issue of the role of hippocampus in exploration, and The animals received 20 trialdday in the 15-s and 60-s in just those memories that have nothing to do with space, contexts, or conditions, followed by five trialdday in the 10-min con- episodes. Hence, data from studies using tasks that are demonstrably now dition. Critically, a single percent correct score was ob- spatial have been taken as a critical testing ground for contrasting these tained by averaging across the three retention intervals in two theories. There is no debate about the role of the hippocampus in each case. A separate score was derived for DNMTS-1 learning about places and contexts, which is well established in the litcra- and for DNMTS-2. ture in all species so far examined. Thus, the z score for each animal was generated from Zola-Morgan et al. (1 994) are concerned with the impact of a variety four data points: a percent correct score for OBJECT of lesions in the medial temporal lobe, including monkeys with lesions lim- discrimination retention, a score on trials to criterion on ited to the hippocampus proper, dentate gyrus, and subiculum (H group), initial learning of the DNMTS, and two scores gener- and those with lesions going beyond the hippocampus proper, dentate aced by averaging across percent correct for all three de- lay retention intervals used (15 s, 60 s, 10 min) in DN- Accepted for publication April 4, 1995. MTS-1 and DNMTS-2. Address correspondence and reprint requests to Lynn Nadel, Department Combining all these data into a single Z score, it ap- of Psychology, University of Arizona, Tucson, AZ 85721. pears that H lesions cause a statistically significant, but 0 1995 WLEY-LISS INC. HIPPOCAMPUS IN DECLARATIVE MEMORY 233 mild deficit in declarative memory, and the authors conclude that animals. They took mure trials to reacquire DNMTS-2 than did the the hippocampus is therefore involved in forms of declarative N animals 6-9 month later, but redthat these reaquisition data memory that are non-spatial. However, this conclusion seems were not used in generating the z scores for the analysis in Zola- quite inappropriate, given the actual data under the various per- Morgan et al. (1994) because “more than half of the monkeys (24 formance conditions that went into making up the single z score of 42) obtained a score of 0 trials on this part of the task” (p. 488). for each animal. In order to make this clear, it is necessary to go There were no Qfferences between H-RF and control monkeys in to the original studies in which these data are reported, and to trials to criterion on the DNMTS (Alvarez et al., 1995). consider each task, and each retention interval, in its own right. What does this all amount to? What is clear from the above The data on the four H-ISC animals in the H group appear in is that the exercise of combining four different measures of “de- Zola-Morgan et al. (1992), whereas the data from the four other clarative” memory to demonstrate a mild memory defect in H animals in the H group, who received radiofrequency lesions of animals obscures the quite circumscribed nature of the “defect” the hippocampus, dentate gyrus, and subiculum, have been re- that has been observed. The H-RF animals did not differ from ferred to in several publications (e.g., Clower et al., 1991; Squire, control monkeys on any of the measures used to assess perfor- 1994), and are about to be published (Alvarez et al., 1995). mance on the two tasks that, according to the authors, unam- Let us consider each task and condition separately, beginning biguously tap declarative memory. The H-ISC animals were dif- with the OBJECI’ discrimination retention task. In Zola-Morgan ferent on the averaged performance across three retention intervals et al. (1992), the data on the OBJECT task for the four H-ISC an- during retest, but, as noted, they were consistently deficient only imals are presented in Table 2. The percent correct scores averaged on performance of the DNMTS with a 10-min retention inter- across 3 test days (the same measure used in Zola-Morgan et al. val. Why does this procedural point matter? It matters because 1994) were 86% for the control group (N) and 85% for the H-ISC the investigators introduced a critical methodological change into group. In Alvarez et al. (1995) the data for the four H-RF animals the DNMTS studies when they used a 10-min retention inter- are presented in Table 1. The percent correct score averaged across val, one that might account for why a deficit was observed in this three test days for these animals was 85%. Thus, the data from the case, and this case alone. When the 10-min retention interval was OBJECT task are absolutely clear: there is no deficit whatever in the used, the animals were removedfiom the test apparatus during the retention of object discrimination in monkeys with lesions restricted retention interval and returned to their home cage. At the end of to the hippocampus proper, dentate gym and subiculum. 1,2 the interval they were returned to the apparatus and given the Consider next the data from the DNMTS task, taking into ac- critical choice trial. This manipulation creates a new situation for count the different retention intervals used. Once again the raw the animal: Now it must not only remember the sample stimu- data are presented in Zola-Morgan et al.
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