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The Cognitive Neuroscience of Human Memory Since H.M NE34CH12-Squire ARI 13 May 2011 12:29 The Cognitive Neuroscience of Human Memory Since H.M. Larry R. Squire1,2,3,4 and John T. Wixted4 1Veterans Affairs Healthcare System, San Diego, California 92161 2Department of Psychiatry, 3Department of Neurosciences, and 4Department of Psychology, University of California, San Diego, La Jolla, California 92093; email: [email protected], [email protected] Annu. Rev. Neurosci. 2011. 34:259–88 Keywords First published online as a Review in Advance on medial temporal lobe, hippocampus, neocortex, anterograde amnesia, March 29, 2011 retrograde amnesia by University of California - San Diego on 09/02/11. For personal use only. The Annual Review of Neuroscience is online at neuro.annualreviews.org Annu. Rev. Neurosci. 2011.34:259-288. Downloaded from www.annualreviews.org Abstract This article’s doi: Work with patient H.M., beginning in the 1950s, established key prin- 10.1146/annurev-neuro-061010-113720 ciples about the organization of memory that inspired decades of experi- Copyright c 2011 by Annual Reviews. mental work. Since H.M., the study of human memory and its disorders All rights reserved has continued to yield new insights and to improve understanding of 0147-006X/11/0721-0259$20.00 the structure and organization of memory. Here we review this work with emphasis on the neuroanatomy of medial temporal lobe and dien- cephalic structures important for memory, multiple memory systems, visual perception, immediate memory, memory consolidation, the locus of long-term memory storage, the concepts of recollection and famil- iarity, and the question of how different medial temporal lobe structures may contribute differently to memory functions. 259 NE34CH12-Squire ARI 13 May 2011 12:29 of memory are not fixed and were not easily es- Contents tablished. Even the question of which cognitive operations reflect memory and which depend INTRODUCTION.................. 260 on other faculties has a long history of empiri- ANATOMY OF MEMORY . 261 cal work and discussion. PRINCIPLES OF ORGANIZATION One needs only to sample nineteenth- SUGGESTED BY H.M.’S century writings to recognize how differently FINDINGS....................... 265 memory was viewed then and now. For MULTIPLE MEMORY SYSTEMS . 266 example, in his classic treatment of memory VISUALPERCEPTION............. 267 disorders, Ribot (1881) considered amnesias IMMEDIATE MEMORY AND due to neurological injury together with WORKING MEMORY . 268 amnesias due to psychological trauma. And REMOTE MEMORY AND he viewed aphasia and agnosia as disorders MEMORY CONSOLIDATION. 271 of memory, wherein (in aphasia, for example) MEMORY IN THE NEOCORTEX . 273 patients have lost their memory for words or Achromatopsia..................... 275 memory for the movements needed to produce Prosopagnosia..................... 275 words. Today, aphasia is considered a deficit Amusia............................ 276 of language, and agnosia a deficit of visual KnowledgeSystems................ 277 perception. Memory is affected but only as part RECOLLECTION AND of a more fundamental defect in a specific kind FAMILIARITY.................... 278 of information processing. Recall versus Recognition . 278 The notion that the study of brain injury can Remember/Know Procedure . 279 elucidate the organization of memory was itself Analysis of the Receiver Operating a matter for empirical inquiry. If brain regions Characteristic................... 279 were highly interconnected, and the brain’s Newer (Model-Free) Methods . 281 functions distributed and integrated one with GROUP STUDIES AND another, then damage to any one area would MULTIPLEMETHODS......... 281 produce a global impairment, blurred across CONCLUSIONS.................... 282 multiple faculties and affecting all of mental life. But the fact of the matter is different. The brain is highly specialized and modular, with differ- ent regions dedicated to specific operations. As INTRODUCTION a result, localized damage can produce strik- In the earliest systematic writings about human ingly specific effects, including a selective and by University of California - San Diego on 09/02/11. For personal use only. memory, it was already appreciated that the circumscribed impairment of memory. Annu. Rev. Neurosci. 2011.34:259-288. Downloaded from www.annualreviews.org study of memory impairment can provide valu- The idea that functions of the nervous sys- able insights into the structure and organiza- tem can be localized was already well accepted tion of normal function (Ribot 1881, Winslow by the end of the nineteenth century. This lo- 1861). This tradition of research has contin- calizationist view had its roots in the writings ued to prove fruitful and has yielded a broad of Gall (1825) and was supported by the exper- range of fundamental information about the imental work of Broca (1861), Ferrier (1876), structure and organization of memory. What Fritsch & Hitzig (1870), and others (see Finger is memory? Is it one thing or many? What are 1994). Yet, these ideas centered mainly around the concepts and categories that guide our cur- sensory functions, motor control, and language rent understanding of how memory works and and did not usefully address the topic of mem- that underlie the classification of its disorders? ory. Then, in the early twentieth century, an It is sometimes not appreciated that the con- influential program of experimental work in ro- cepts and categories used in current discussions dents investigated directly the localization of 260 Squire · Wixted NE34CH12-Squire ARI 13 May 2011 12:29 memory with the conclusion that memory is cent parahippocampal gyrus. Which structures distributed throughout the cortex and that the within H.M.’s lesion are important for memory contribution to memory is equivalent across re- became understood only gradually during the gions (Lashley 1929). This idea was strongly 1980s following the successful development of challenged (Hebb 1949, Hunter 1930) by the an animal model of human amnesia in the non- alternative, and more modern, interpretation human primate (Mishkin 1978). Cumulative that memory storage is indeed distributed but studies in the monkey (Murray 1992, Squire & that different areas store different features of the Zola-Morgan 1991, Zola-Morgan et al. 1994) whole. Still, as the midpoint of the twentieth considerably clarified this issue. The impor- century approached, memory functions, while tant structures proved to be the hippocam- distributed, were thought to be well integrated pus and the adjacent entorhinal, perirhinal, with perceptual and intellectual functions, and and parahippocampal cortices, which make up no region of the brain was believed to be dis- much of the parahippocampal gyrus (Figure 2). proportionately dedicated to memory. All that One particularly instructive case of human was about to change. memory impairment became available during In 1957, Brenda Milner reported the this same time period (Zola-Morgan et al. profound effect on memory of bilateral medial 1986). R.B. developed a moderately severe, temporal lobe resection, carried out to relieve enduring impairment following an ischemic epilepsy in a patient who became known as episode in 1978. During the five years until his H.M. (1926–2008) (Scoville & Milner 1957, death, his memory deficit was well documented Squire 2009) (Figure 1). Remarkably, H.M. with formal tests. Detailed histological exami- exhibited profound forgetfulness but in the nation of his brain revealed a circumscribed bi- absence of any general intellectual loss or lateral lesion involving the entire CA1 field of perceptual disorders. He could not form new the hippocampus. Note that a lesion confined memories (anterograde amnesia) and also to the CA1 field must substantially disrupt hip- could not access some memories acquired pocampal function because the CA1 field is a before his surgery (retrograde amnesia). His bottleneck in the unidirectional chain of pro- impairment extended to both verbal and non- cessing that begins at the dentate gyrus and ends verbal material, and it involved information in the subiculum and entorhinal cortex. R.B. acquired through all sensory modalities. These was the first case of memory impairment fol- findings established the fundamental principle lowing a lesion limited to the hippocampus that that memory is a distinct cerebral function, was supported by extensive neuropsychological separable from other perceptual and cognitive testing as well as neuropathological analysis. abilities, and also identified the medial aspect The findings from R.B., considered together by University of California - San Diego on 09/02/11. For personal use only. of the temporal lobe as important for memory. with the much more severe impairment in Annu. Rev. Neurosci. 2011.34:259-288. Downloaded from www.annualreviews.org The early descriptions of H.M. can be said to H.M., made two useful points. First, damage to have inaugurated the modern era of memory re- the hippocampus itself is sufficient to produce search, and the findings from H.M. enormously a clinically significant and readily detectable influenced the direction of subsequent work. memory impairment. Second, additional dam- age to the adjacent cortical regions along the parahippocampal gyrus (as in H.M.) greatly ex- ANATOMY OF MEMORY acerbates the memory impairment. These same The work with H.M. is sometimes cited incor- conclusions about the neuroanatomy of mod- rectly as evidence of the importance of the hip- est and severe memory impairment were also pocampus for memory, but this
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