MEMORY AND THE HIPPOCAMPUS 203 on Mishkin.1983:Graff-Radford.Tranel.Var amygdala lesions were typically produced stereotaxically This en. Amaral, gan,Krit edure makes it possible to prod amygdala les sons with &Sc uri.1985).Most of th is a repo ppocampa that conjoint lesions of amygdala and h pus impa extent diencephalicand medial temp al lobe pat ogy in h ons of hi edala had no effect mans and mon t (for ntof view :Victor animals .This up to delays of 60s(A et al,1989).Al ching- ple task used with gion may belong to a tightly linked functional s d for choosing the arm of a Y maz hat damage able arm on the starting arm anda second arm that diff Memory Impairment in Rats ight expect from studies of mo keys that perf at ha pocamp: cen work with rats and work with humansan et al 1989a)rats with hippocampalles mance ona varietyofm mory tasks.T mcthaoeCcdwHhlhelesioasOaepOSbifg discrimination task that reouin d,is tha of this wor been to c st non uman prin ectso hist ved hy ces in studiesdirectedatthisbe us and the ar la in orx The rtains to there is noe e that ygdala le n rat contr re hippo ampal ons or les hn ngs from mo eys,amely that the ory functi and that the am ygdala isnot part of this functiona work in what obs the hip ent of affe on alor (Aggletc d&MeD by thed nce Io Imull,as expr 1990).One important feature of the studies with rats is that toward conditioned stimuli (Davis,1986:Gaffan&Harrison Task Hippocampus Amygdala Reference 1990 1986 oto 0.1980MEMORY AND THE HIPPOCAMPUS 203 tract (Aggleton & Mishkin, 1983; Graff-Radford, Tranel, Van Hoesen, & Brandt, 1990; Squire, Amaral, Zola-Morgan, Krit￾chevsky, & Press, 1989; Victor, Adams, & Collins, 1989; von Cramon, Rebel, & Schuri, 1985). Most of these thalamic re￾gions have anatomical connections to either the hippocampal formation or the perirhinal cortex. It is also unclear to what extent diencephalic and medial temporal lobe pathology in hu￾mans and monkeys might produce different patterns of mem￾ory impairment (for two points of view, see Parkin, 1984; Victor et al, 1989). Although one would expect that these brain re￾gions make different contributions to normal memory, each region may belong to a tightly linked functional system such that damage to any component causes rather similar kinds of impairment. Memory Impairment in Rats During the past several years, many points of contact have developed between work with rats and work with humans and nonhuman primates. In the rat, hippocampal lesions or lesions of related structures (fornix or entorhinal cortex) impair perfor￾mance on a wide variety of memory tasks. These include spatial memory tasks, odor-discrimination learning, timing tasks, and discrimination tasks that require learning relationships be￾tween stimuli. One major focus of this work has been to charac￾terize the kind of learning and memory that is impaired (see next section). Another focus has been to compare the effects of hippocampal lesions with the effects of lesions in adjacent structures. Studies directed at this second objective have obtained two important findings. The first pertains to the roles of the hippo￾campus and the amygdala in memory. The second pertains to the separate contributions of the structures and connections within the hippocampal formation. First, at least seven exam￾ples can be identified where hippocampal lesions or lesions of anatomically related structures produce an effect on memory, but amygdala lesions produce no impairment (Table 3). In ad￾dition, three studies have found that adding an amygdala lesion to a lesion of the hippocampal system did not increase the deficit beyond what was observed following the hippocampal lesion alone (Aggleton, Hunt, & Rawlins, 1986, Experiment 2; Eichenbaum, Pagan, & Cohen, 1986; Sutherland & McDonald, 1990). One important feature of the studies with rats is that amygdala lesions were typically produced stereotaxically. This procedure makes it possible to produce amygdala lesions with￾out damaging cortical areas surrounding the amygdala. An apparent exception to this pattern of findings is a report that conjoint lesions of amygdala and hippocampus impaired performance on a task of object recognition, whereas separate lesions of hippocampus or amygdala had no effect, even when animals had to retain information up to delays of 60 s (Aggie￾ton, Blindt, & Rawlins, 1989). This task was a modified version of the visual delayed nonmatching-to-sample task used with monkeys. Rats were rewarded for choosing the arm of a Y maze that differed visually from the starting arm. Multiple, remov￾able arms were used so that on each trial rats saw one arm identical to the starting arm and a second arm that differed from the starting arm along several dimensions. Although one might expect from studies of monkeys that performance on such a task should be measurably impaired by hippocampal lesions alone (Mahut et al., 1982; Mishkin, 1978; Zola-Morgan et al, 1989a), rats with hippocampal lesions performed this task normally. Because hippocampal lesions alone did not disrupt performance on this task, it is difficult to interpret the impair￾ment that occurred with larger lesions. One possibility, which has scarcely been explored, is that rats might approach some variants of the delayed nonmatching-to-sample task with a dif￾ferent strategy than nonhuman primates. For example, Suther￾land and Rudy (1989) pointed out that this task could in princi￾ple be solved by two fundamentally different strategies (also see the note to Table 2 for the importance of strategy differences in how monkeys and humans accomplish pattern-discrimination learning). In any case, there is no evidence that amygdala lesions in rats impair performance on tasks that are also impaired by hippo￾campal lesions. The findings in rats are therefore in agreement with the findings from monkeys, namely that the hippocampus and related structures participate in a particular kind of mem￾ory function and that the amygdala is not part of this functional system. Indeed, work in both monkeys and rats suggests that the amygdala is important for other functions, including the acquisition of conditioned fear and the establishment of affec￾tive significance for neutral stimuli, as expressed, for example, by the development of conditioned responses that are directed toward conditioned stimuli (Davis, 1986; Gaffan & Harrison, Table 3 Effects of Lesions of the Hippocampal System or the Amygdala on Memory Tasks in the Rat Task Hippocampus Amygdala Reference Water maze Odor discrimination Timing of events Learning cue relationships Spatial alternation Nonspatial alternation Radial maze Sutherland & McDonald, 1990 Eichenbaum, Pagan, & Cohen, 1986' Olton, Meek, & Church, 1987' Sutherland, McDonald, Hill, & Rudy 1989 Aggleton, Hunt, & Rawlins, 1986; Aggleton, Blindt, & Rawlins, 1989 Raffaele & Olton, 1988" Becker, Walker, & Olton, 1980* Note. Plus sign indicates impairment; minus sign indicates no impairment. • These lesions damaged the fornix rather than the hippocampus itself