iw:Mier.Squre,and Kande LONG-TERN MEMOR David Amaral has reviewed tone:unconditioned stimulus ditioned re 1997).He finds that Scoville's removal I was in fac h ce that the of th 8 cm origina th h ded th ain ste ircuitry and that ory traces nd th nt he p and Krupa,1994).To date,eyeblink condi spard.Mostimp rtantly,the ter of a within the mam the localiza me died y h ude adap Prir nas H.M.was describe h1959 monkey. con cept of onscious knowle dge about categories in ntal animals？Se e the ms th nory to mic (Squire et al. 1993 all reas re on e t Part s of the Medial poral Lobe rpola Are i ortant for Memory te rtan e of specific structur region fo which memory tasks were apr priate to other bra ugh So in 1978 when Mort M shkin eir paper,th r exper the sult in an r obje ching to sia they n vith th by single-tria delayedReview: Milner, Squire, and Kandel 451 Figure 3. A Taxonomy of Mammalian Mem￾ory Systems This taxonomy lists the brain structures and connections thought to be especially impor￾tant for each kind of declarative and nonde￾clarative memory. colleagues has focused on basic delay conditioning of David Amaral has recently reviewed the results of a the rabbit eyeblink response (conditioned stimulus 5 magnetic resonance imaging study of H. M. (Corkin et tone; unconditioned stimulus 5 airpuff; conditioned re- al., 1997). He finds that Scoville’s removal was in fact sponse 5 eyeblink). Based on anatomical findings, elec- exactly as he had described it, except that the resection trical stimulation, and reversible lesion techniques, the only extends about 5 cm posteriorly in both hemi￾results provide strong evidence that the essential mem- spheres, instead of the radical 8 cm originally reported. ory trace circuit includes the cerebellum and related Thus, in both hemispheres the removal included the brain stem circuitry and that the memory traces them- amygdala, the perirhinal and entorhinal cortex, and the selves are formed and stored in the cerebellum (Thomp- anterior hippocampus. The parahippocampal cortex son and Krupa, 1994). To date, eyeblink conditioning was largely spared. Most importantly, the temporal neo￾provides the clearest information about the localization cortex and the temporal stem were spared. If the roles of a memory within the mammalian brain. of these various structures were to be understood, an animal model clearly was needed. In humans, several kinds of nondeclarative memory have been studied, which are likely based on perceptual learning. These include adaptation-level effects, the Nonhuman Primate Models of Declarative Memory ability to resolve random-dot stereograms, the ability to As soon as H. M. was described in 1957, efforts began to establish an animal model of his condition in the rat learn the regularities of “artificial grammars” by studying and monkey. If the concept of conscious recollection lawfully ordered letter strings, and the ability to acquire is central to declarative memory, how can declarative knowledge about categories. In category learning, one memory be studied in experimental animals? Several extracts and stores information about the prototype (or characteristics have been useful in extending the notion representative instance) of a series of items by studying many different items that, when averaged together, de- of declarative memory to mice, rats, and monkeys (Eichenbaum, 1997). These include its flexibility and the scribe the prototype. All these forms of memory are ability to use it inferentially in novel situations. It took intact in amnesic patients (Squire et al., 1993; Squire considerable time to achieve such a model, and the first and Zola-Morgan, 1996). These kinds of memory likely results of lesion studies in the monkey were puzzling. involve changes within the same cortical areas responsi- Animals with bilateral medial temporal-lobe resections ble for perceiving and analyzing the materials that are similar to what was described in H. M. showed normal studied. performance on visual discrimination learning tasks, even when concurrent trials on a different task were What Parts of the Medial Temporal Lobe interpolated as potential “distractors” for the discrimina- Are Important for Memory? tion learning. This led many investigators to question The behavioral studies reviewed above provide compel- either thehuman findings or the validity of cross-species ling evidence that the human declarative memory sys- comparisons. It was not until the early 1980s, with the tem is critically dependent upon the medial temporal concept of multiple memory systems and the idea that region. Yet we still have much to learn about the relative amnesia impaired only one kind of memory, that it be￾importance of specific structures within the region for came clearer which memory tasks were appropriate to memory processes and the mode of interaction of these give to experimental animals. The beginning of the solu￾structures with other brain areas. Although Scoville and tion came in 1978 when Mort Mishkin described severe Milner (1957) drew attention to the hippocampus in the deficits in monkeys with bilateral medial temporal-lobe title to their paper, this was only because in their experi- lesions, when the monkeys were given a one-trial task ence bilateral removals limited to the amygdala and un- of object recognition memory (delayed nonmatching to cus did not result in amnesia; they never claimed that the sample). This finding was consistent with the severe hippocampal lesions alone were responsible for H. M.’s impairment shown by H. M. on single-trial delayed severe memory loss. matching tasks