The hippocampus appears to be crucial for long-term episodic memory, yet its precise role remains elusive. Electrophysiological studies in rodents offer a useful starting point for developing models of hippocampal processing in the spatial domain. Here we review one such model that points to an essential role for the hippocampus in the construction of mental images. We explain how this neural-level mechanistic account addresses some of the current controversies in the field, such as the role of the hippocampus in imagery and short-term memory, and discuss its broader implications for the neural bases of episodic memory.
Damage to the hippocampus in humans can cause profound impairments in long-term episodic memory, but the precise functional contribution of the hippocampus remains the subject of several competing theories.
Electrophysiological studies in rodents have characterized the firing properties of 'place cells' in the hippocampus in great detail. Place cells appear to represent where an animal 'thinks' it is located in an environment, relative to environmental boundaries. Acting cooperatively, place cells encode specific environments, performing both pattern completion and pattern separation.
A new model of hippocampal processing that is driven by the properties of place cells (the BBB model) provides an alternative to existing psychological theories, at least in the spatial domain. The BBB model proposes that the hippocampus is needed to impose a location from which to retrieve and construct a coherent mental image of an environment. This mental image supports the online maintenance and manipulation of representations of the locations of objects and features in an environment.
The model suggests that episodic memory will always be hippocampus-dependent if it is associated with rich mental imagery of an environment. Other sophisticated long-term spatial (and non-spatial) representations can be acquired, stored and retrieved independent of the hippocampus. However, the hippocampus is often needed to mediate behaviours that allow such learning to take place (such as when learning a new route).
The BBB model further suggests that the hippocampus is required for both short-term and long-term memory for some types of information, for imagining complex visual scenes (be they real or fictitious), and more for the recognition of scenes than faces. Recent experimental evidence from studies of the effects of damage to the hippocampus in humans supports all three of these proposals.
Hippocampal processing beyond the spatial domain cannot be explained by the BBB model, but several theoretical positions have been advanced to address the broader role of the hippocampus in mnemonic processing.
Subscribe to Journal
Get full journal access for 1 year
only $22.08 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Andersen, P., Morris, R., Amaral, D., Bliss, T. & O'Keefe, J. The Hippocampus Book (Oxford Univ. Press, New York, 2007). This book is an excellent source for anyone interested in hippocampal function: it reviews molecular, synaptic, physiological and cognitive data.
Scoville, W. B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957). This study provided one of the first detailed descriptions of the effects of bilateral medial temporal lobe resection on memory. It included an account of the famous patient H. M.
Milner, B. Disorders of learning and memory after temporal lobe lesions in man. Clin. Neurosurg. 19, 421–446 (1972).
Zola-Morgan, S., Squire, L. R. & Amaral, D. G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 6, 2950–2967 (1986).
Rempel-Clower, N. L., Zola, S. M., Squire, L. R. & Amaral, D. G. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J. Neurosci. 16, 5233–5255 (1996).
Milner, B., Squire, L. R. & Kandel, E. R. Cognitive neuroscience and the study of memory. Neuron 20, 445–468 (1998).
Squire, L. R. Mechanisms of memory. Science 232, 1612–1619 (1986). This influential review outlines the main tenets of the Declarative Theory, and includes sections on short-term versus long-term memory, declarative versus procedural memory, and memory consolidation over time.
Squire, L. R., Stark, C. E. & Clark, R. E. The medial temporal lobe. Annu. Rev. Neurosci. 27, 279–306 (2004).
Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217–227 (1997). This paper lays out the Multiple-Trace Theory alternative to the extra-hippocampal consolidation of all memories.
Moscovitch, M. et al. Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J. Anat. 207, 35–66 (2005).
Aggleton, J. P. & Brown, M. W. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behavioural Brain Sci. 22, 425–444; discussion 445–490 (1999). This paper reviews evidence that the hippocampal–anterior-thalamic system supports recollection and the perirhinal-cortex–mammilliary-bodies system supports familiarity.
Cohen, N. J. & Eichenbaum, H. Memory, Amnesia and the Hippocampal System (MIT Press, Cambridge, Massachusettes, 1993). This book outlines the theory that the hippocampal system has a crucial role in binding together multiple inputs to permit representations of the relations among the constituent elements of scenes or events.
Cohen, N. J., Poldrack, R. A. & Eichenbaum, H. Memory for items and memory for relations in the procedural/declarative memory framework. Memory 5, 131–178 (1997).
Eichenbaum, H. & Cohen, N. J. From Conditioning to Conscious Recollection: Memory Systems of the Brain (Oxford Univ. Press, Oxford, 2001).
O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, 1978). This book lays out the Cognitive-Map Theory, summarizing the properties of hippocampal place cells, the effects of hippocampal lesions in rats and implications for the role of the hippocampus, including one of the first suggestions of a specific role in context-dependent memory.
Marr, D. A theory for cerebral cortex. Proc. R. Soc. Lond. B Biol. Sci. 176, 161–234 (1970).
Marr, D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 262, 23–81 (1971). This paper laid out the model that continues to be the dominant model of hippocampal function today (updated by references 18–22), including the ideas of memory-as-attractor-representations and pattern completion, and the relationship between rapid hippocampal learning and the slow accumulation of semantic knowledge in the neocortex.
Teyler, T. J. & DiScenna, P. The hippocampal memory indexing theory. Behav. Neurosci. 100, 147–154 (1986).
McNaughton, B. L. & Morris, R. G. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10, 408–415 (1987).
Treves, A. & Rolls, E. T. Computational analysis of the role of the hippocampus in memory. Hippocampus 4, 374–391 (1994).
McClelland, J. L., McNaughton, B. L. & O'Reilly, R. C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419–457 (1995).
Alvarez, P. & Squire, L. R. Memory consolidation and the medial temporal lobe: a simple network model. Proc. Natl Acad. Sci. USA 91, 7041–7045 (1994).
Damasio, A. R. The brain binds entities and events by multiregional activation from convergence zones. Neural Comput. 1, 123–132 (1989).
Patterson, K., Nestor, P. J. & Rogers, T. T. Where do you know what you know? The representation of semantic knowledge in the human brain. Nature Rev. Neurosci. 8, 976–987 (2007).
Tulving, E. in Organisation and Memory (eds Tulving, E. & Donaldson, W.) 382–403 (Academic, New York, 1972).
Tulving, E. Episodic memory: from mind to brain. Annu. Rev. Psychol. 53, 1–25 (2002).
Steinvorth, S., Levine, B. & Corkin, S. Medial temporal lobe structures are needed to re-experience remote autobiographical memories: evidence from H. M. and W. R. Neuropsychologia 43, 479–496 (2005). This provocative article suggested that, although remote memories might be retained following extensive medial temporal lobe damage, such memories are inflexible and cannot be 're-experienced'.
Cipolotti, L. et al. Long term retrograde amnesia. The crucial role of the hippocampus. Neuropsychologia 39, 151–172 (2001).
Gilboa, A. et al. Hippocampal contributions to recollection in retrograde and anterograde amnesia. Hippocampus 16, 966–980 (2006).
Noulhiane, M. et al. Autobiographical memory after temporal lobe resection: neuropsychological and MRI volumetric findings. Brain 130, 3184–3199 (2007).
Bayley, P. J., Hopkins, R. O. & Squire, L. R. Successful recollection of remote autobiographical memories by amnesic patients with medial temporal lobe lesions. Neuron 38, 135–144 (2003).
Bright, P. et al. Retrograde amnesia in patients with hippocampal, medial temporal, temporal lobe, or frontal pathology. Learn. Mem. 13, 545–557 (2006).
Manns, J. R., Hopkins, R. O. & Squire, L. R. Semantic memory and the human hippocampus. Neuron 38, 127–133 (2003).
Cabeza, R. & St Jacques, P. Functional neuroimaging of autobiographical memory. Trends Cogn. Sci. 11, 219–227 (2007).
Jacoby, L. L. & Dallas, M. On the relationship between autobiographical memory and perceptual learning. J. Exp. Psychol. Gen. 110, 306–340 (1981).
Mandler, G. Recognizing: the judgment of previous occurrence. Psychol. Rev. 87, 252–271 (1980).
Tulving, E. Memory and consciousness. Can. Psychol. 26, 1–12 (1985).
O'Reilly, R. C. & Norman, K. A. Hippocampal and neocortical contributions to memory: advances in the complementary learning systems framework. Trends Cogn. Sci. 6, 505–510 (2002).
Rugg, M. D. & Yonelinas, A. P. Human recognition memory: a cognitive neuroscience perspective. Trends Cogn. Sci. 7, 313–319 (2003).
Eichenbaum, H., Yonelinas, A. P. & Ranganath, C. The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123–152 (2007).
Wais, P. E., Wixted, J. T., Hopkins, R. O. & Squire, L. R. The hippocampus supports both the recollection and the familiarity components of recognition memory. Neuron 49, 459–466 (2006). This elegant study reported that recollection decays before familiarity in both healthy adults and patients with hippocampal damage, and that both processes are impaired by hippocampal damage.
Manns, J. R., Hopkins, R. O., Reed, J. M., Kitchener, E. G. & Squire, L. R. Recognition memory and the human hippocampus. Neuron 37, 171–180 (2003).
Kopelman, M. D. et al. Recall and recognition memory in amnesia: patients with hippocampal, medial temporal, temporal lobe or frontal pathology. Neuropsychologia 45, 1232–1246 (2007).
Aggleton, J. P. et al. Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology. Neuropsychologia 43, 1810–1823 (2005).
Mayes, A. R., Holdstock, J. S., Isaac, C. L., Hunkin, N. M. & Roberts, N. Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus. Hippocampus 12, 325–340 (2002).
Vargha-Khadem, F. et al. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376–380 (1997).
Turriziani, P., Fadda, L., Caltagirone, C. & Carlesimo, G. A. Recognition memory for single items and for associations in amnesic patients. Neuropsychologia 42, 426–433 (2004). This group study of hippocampal amnesics described intact recognition memory for faces but not for face–face or face–word pairs.
Yonelinas, A. P. et al. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nature Neurosci. 5, 1236–1241 (2002).
Aggleton, J. P. & Brown, M. W. Interleaving brain systems for episodic and recognition memory. Trends Cogn. Sci. 10, 455–463 (2006).
Squire, L. R., Wixted, J. T. & Clark, R. E. Recognition memory and the medial temporal lobe: a new perspective. Nature Rev. Neurosci. 8, 872–883 (2007).
O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).
Ekstrom, A. D. et al. Cellular networks underlying human spatial navigation. Nature 425, 184–188 (2003).
Ono, T., Nakamura, K., Fukuda, M. & Tamura, R. Place recognition responses of neurons in monkey hippocampus. Neurosci. Lett. 121, 194–198 (1991).
O'Keefe, J. in The Hippocampus Book (eds Andersen, P., Morris, R., Amaral, D., Bliss, T. & O'Keefe, J.) 475–540 (Oxford Univ. Press, New York, 2007).
Cressant, A., Muller, R. U. & Poucet, B. Failure of centrally placed objects to control the firing fields of hippocampal place cells. J. Neurosci. 17, 2531–2542 (1997).
O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425–428 (1996).
O'Keefe, J. & Speakman, A. Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res. 68, 1–27 (1987).
Lenck-Santini, P. P., Muller, R. U., Save, E. & Poucet, B. Relationships between place cell firing fields and navigational decisions by rats. J. Neurosci. 22, 9035–9047 (2002).
Hafting, T., Fyhn, M., Molden, S., Moser, M. B. & Moser, E. I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).
Lever, C., Wills, T., Cacucci, F., Burgess, N. & O'Keefe, J. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90–94 (2002).
Wills, T., Lever, C., Cacucci, F., Burgess, N. & O'Keefe, J. Attractor dynamics in the hippocampal representation of the local environment. Science 308, 873–876 (2005).
Bostock, E., Muller, R. U. & Kubie, J. L. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1, 193–205 (1991).
Byrne, P., Becker, S. & Burgess, N. Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340–375 (2007). This paper provided an updated version of the model first proposed in references 64 and 65, which quantitatively describes the interactions between brain regions involved in spatial memory and mental imagery; the hippocampus is required to constrain the retrieval of information to be consistent with occupying a specific location in an imagined scene.
Burgess, N., Becker, S., King, J. A. & O'Keefe, J. Memory for events and their spatial context: models and experiments. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1493–1503 (2001).
Becker, S. & Burgess, N. A model of spatial recall, mental imagery and neglect. Adv. Neural Inf. Process. Syst. 13, 96–102 (2001).
Recce, M. & Harris, K. D. Memory for places: a navigational model in support of Marr's theory of hippocampal function. Hippocampus 6, 735–748 (1996).
Epstein, R. & Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998).
Buckley, M. J. & Gaffan, D. Impairment of visual object-discrimination learning after perirhinal cortex ablation. Behav. Neurosci. 111, 467–475 (1997).
Wagner, A. D., Shannon, B. J., Kahn, I. & Buckner, R. L. Parietal lobe contributions to episodic memory retrieval. Trends Cogn. Sci. 9, 445–453 (2005).
Schacter, D. L. & Addis, D. R. The cognitive neuroscience of constructive memory: remembering the past and imagining the future. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 773–786 (2007).
Hassabis, D. & Maguire, E. A. Deconstructing episodic memory with construction. Trends Cogn. Sci. 11, 299–306 (2007).
Teng, E. & Squire, L. R. Memory for places learned long ago is intact after hippocampal damage. Nature 400, 675–677 (1999). This influential paper described intact remote topographical memory across a variety of test paradigms in a patient with extensive medial temporal lobe damage, demonstrating that sophisticated spatial memory representations exist outside of the hippocampus.
Rosenbaum, R. S. et al. Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions. Nature Neurosci. 3, 1044–1048 (2000).
White, N. M. & McDonald, R. J. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 77, 125–184 (2002).
Hartley, T., Maguire, E. A., Spiers, H. J. & Burgess, N. The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37, 877–888 (2003).
Iaria, G., Petrides, M., Dagher, A., Pike, B. & Bohbot, V. D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J. Neurosci. 23, 5945–5952 (2003).
Doeller, C. F. & Burgess, N. Distinct error-correcting and incidental learning of location relative to landmarks and boundaries. Proc. Natl Acad. Sci. USA (in the press).
Pearce, J. M., Roberts, A. D. & Good, M. Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature 396, 75–77 (1998).
Maguire, E. A., Nannery, R. & Spiers, H. J. Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain 129, 2894–2907 (2006).
Hassabis, D., Kumaran, D., Vann, S. D. & Maguire, E. A. Patients with hippocampal amnesia cannot imagine new experiences. Proc. Natl Acad. Sci. USA 104, 1726–1731 (2007). This study presented evidence that hippocampal damage causes impairment in imagining complex visual scenes, using a task that did not require the recall of specific events. The patients' reports of the imagined scenes were particularly lacking in spatial coherence.
Hassabis, D., Kumaran, D. & Maguire, E. A. Using imagination to understand the neural basis of episodic memory. J. Neurosci. 27, 14365–14374 (2007).
Buckner, R. L. & Carroll, D. C. Self-projection and the brain. Trends Cogn. Sci. 11, 49–57 (2007).
Schmolck, H., Kensinger, E. A., Corkin, S. & Squire, L. R. Semantic knowledge in patient H. M. and other patients with bilateral medial and lateral temporal lobe lesions. Hippocampus 12, 520–533 (2002).
Cipolotti, L. et al. Recollection and familiarity in dense hippocampal amnesia: a case study. Neuropsychologia 44, 489–506 (2006). Together with references 87–89, this study highlighted differential effects on recognition memory following hippocampal damage, with the effects depending on the nature of the to-be-remembered materials.
Carlesimo, G. A., Fadda, L., Turriziani, P., Tomaiuolo, F. & Caltagirone, C. Selective sparing of face learning in a global amnesic patient. J. Neurol. Neurosurg. Psychiatry 71, 340–346 (2001).
Holdstock, J. S., Mayes, A. R., Gong, Q. Y., Roberts, N. & Kapur, N. Item recognition is less impaired than recall and associative recognition in a patient with selective hippocampal damage. Hippocampus 15, 203–215 (2005).
Taylor, K. J., Henson, R. N. & Graham, K. S. Recognition memory for faces and scenes in amnesia: dissociable roles of medial temporal lobe structures. Neuropsychologia 45, 2428–2438 (2007).
Bird, C. M., Shallice, T. & Cipolotti, L. Fractionation of memory in medial temporal lobe amnesia. Neuropsychologia 45, 1160–1171 (2007).
Bird, C. M., Vargha-Khadem, F. & Burgess, N. Impaired memory for scenes but not faces in developmental hippocampal amnesia: a case study. Neuropsychologia (in the press).
Kanwisher, N., McDermott, J. & Chun, M. M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997).
Simons, J. S., Graham, K. S., Galton, C. J., Patterson, K. & Hodges, J. R. Semantic knowledge and episodic memory for faces in semantic dementia. Neuropsychology 15, 101–114 (2001).
Olson, I. R., Plotzker, A. & Ezzyat, Y. The enigmatic temporal pole: a review of findings on social and emotional processing. Brain 130, 1718–1731 (2007).
Baddeley, A. D. & Warrington, E. K. Amnesia and the distinction between long-and short-term memory. J. Verbal Learn. Verbal Behav. 9, 176–189 (1970).
Shallice, T. From Neuropsychology to Mental Structure (Cambridge Univ. Press, New York, 1988).
Cave, C. B. & Squire, L. R. Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus 2, 151–163 (1992).
Spiers, H. J., Maguire, E. A. & Burgess, N. Hippocampal amnesia. Neurocase 7, 357–382 (2001).
Milner, B. Interhemispheric differences in the localization of psychological processes in man. Br. Med. Bull. 27, 272–277 (1971).
Olson, I. R., Moore, K. S., Stark, M. & Chatterjee, A. Visual working memory is impaired when the medial temporal lobe is damaged. J. Cogn. Neurosci. 18, 1087–1097 (2006).
Nichols, E. A., Kao, Y. C., Verfaellie, M. & Gabrieli, J. D. Working memory and long-term memory for faces: evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus 16, 604–616 (2006).
Piekema, C. et al. Spatial and non-spatial contextual working memory in patients with diencephalic or hippocampal dysfunction. Brain Res. 1172, 103–109 (2007).
Finke, C. et al. The human hippocampal formation mediates short-term memory of colour–location associations. Neuropsychologia 16 Oct 2007 (doi:10.1016/j.neuropsychologia.2007.10.004).
Owen, A. M., Sahakian, B. J., Semple, J., Polkey, C. E. & Robbins, T. W. Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia 33, 1–24 (1995).
King, J. A., Trinkler, I., Hartley, T., Vargha-Khadem, F. & Burgess, N. The hippocampal role in spatial memory and the familiarity-recollection distinction: a single case study. Neuropsychology 18, 405–417 (2004).
King, J. A., Burgess, N., Hartley, T., Vargha-Khadem, F. & O'Keefe, J. Human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12, 811–820 (2002).
Shrager, Y., Bayley, P. J., Bontempi, B., Hopkins, R. O. & Squire, L. R. Spatial memory and the human hippocampus. Proc. Natl Acad. Sci. USA 104, 2961–2966 (2007).
Hartley, T. et al. The hippocampus is required for short-term topographical memory in humans. Hippocampus 17, 34–48 (2007). This study provided evidence that the hippocampus is specifically required for the representation of topographical information in visual scenes, even over very short durations.
Lee, A. C. et al. Specialisation in the medial temporal lobe for processing of objects and scenes. Hippocampus 15, 782–797 (2005).
Lee, A. C. et al. Perceptual deficits in amnesia: challenging the medial temporal lobe 'mnemonic' view. Neuropsychologia 43, 1–11 (2005).
Graham, K. S. et al. Abnormal categorization and perceptual learning in patients with hippocampal damage. J. Neurosci. 26, 7547–7554 (2006).
Shrager, Y., Gold, J. J., Hopkins, R. O. & Squire, L. R. Intact visual perception in memory-impaired patients with medial temporal lobe lesions. J. Neurosci. 26, 2235–2240 (2006).
Olson, I. R., Page, K., Moore, K. S., Chatterjee, A. & Verfaellie, M. Working memory for conjunctions relies on the medial temporal lobe. J. Neurosci. 26, 4596–4601 (2006).
Eacott, M. J. & Norman, G. Integrated memory for object, place, and context in rats: a possible model of episodic-like memory? J. Neurosci. 24, 1948–1953 (2004).
Gaffan, D. & Parker, A. Interaction of perirhinal cortex with the fornix-fimbria: memory for objects and “object-in-place” memory. J. Neurosci. 16, 5864–5869 (1996).
Lavenex, P. B., Amaral, D. G. & Lavenex, P. Hippocampal lesion prevents spatial relational learning in adult macaque monkeys. J. Neurosci. 26, 4546–4558 (2006).
Hannula, D. E., Tranel, D. & Cohen, N. J. The long and the short of it: relational memory impairments in amnesia, even at short lags. J. Neurosci. 26, 8352–8359 (2006). Together with references 106, 107 and 111, this study found relational memory impairments over short delays in patients with focal medial temporal lobe lesions, demonstrating a role for the hippocampus in processing within the time frame traditionally thought of as 'short-term memory'.
Mayes, A., Montaldi, D. & Migo, E. Associative memory and the medial temporal lobes. Trends Cogn. Sci. 11, 126–135 (2007).
Mayes, A. R. et al. Memory for single items, word pairs, and temporal order of different kinds in a patient with selective hippocampal lesions. Cogn. Neuropsychol. 18, 97–123 (2001).
Spiers, H. J., Burgess, N., Hartley, T., Vargha-Khadem, F. & O'Keefe, J. Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching. Hippocampus 11, 715–725 (2001).
Bunsey, M. & Eichenbaum, H. Conservation of hippocampal memory function in rats and humans. Nature 379, 255–257 (1996).
Chun, M. M. & Phelps, E. A. Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage. Nature Neurosci. 2, 844–847 (1999).
Ryan, J. D., Althoff, R. R., Whitlow, S. & Cohen, N. J. Amnesia is a deficit in relational memory. Psychol. Sci. 11, 454–461 (2000). Together with reference 120, this study suggested that the hippocampus has a role in implicit or non-declarative relational memory.
Norman, K. A. & O'Reilly, R. C. Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol. Rev. 110, 611–646 (2003).
Bogacz, R. & Brown, M. W. Comparison of computational models of familiarity discrimination in the perirhinal cortex. Hippocampus 13, 494–524 (2003).
Holdstock, J. S. et al. Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? Hippocampus 12, 341–351 (2002).
Bayley, P. J., Wixted, J. T., Hopkins, R. O. & Squire, L. R. Yes/no recognition, forced-choice recognition, and the human hippocampus. J. Cogn. Neurosci. 15 Nov 2007 (doi:10.1162/jocn.2008.20038).
Yonelinas, A. P., Kroll, N. E., Dobbins, I. G. & Soltani, M. Recognition memory for faces: when familiarity supports associative recognition judgments. Psychon. Bull. Rev. 6, 654–661 (1999).
Blum, K. I. & Abbott, L. F. A model of spatial map formation in the hippocampus of the rat. Neural Comput. 8, 85–93 (1996).
Redish, A. D. & Touretzky, D. S. The role of the hippocampus in solving the Morris water maze. Neural Comput. 10, 73–111 (1998).
Samsonovich, A. V. & Ascoli, G. A. A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval. Learn. Mem. 12, 193–208 (2005).
Jensen, O. & Lisman, J. E. Novel lists of 7 +/- 2 known items can be reliably stored in an oscillatory short-term memory network: interaction with long-term memory. Learn. Mem. 3, 257–263 (1996).
Minai, A. A. & Levy, W. B. The dynamics of sparse random networks. Biol. Cybern. 70, 177–187 (1993).
Howard, M. W., Fotedar, M. S., Datey, A. V. & Hasselmo, M. E. The Temporal Context Model in spatial navigation and relational learning: toward a common explanation of medial temporal lobe function across domains. Psychol. Rev. 112, 75–116 (2005).
Burgess, N. & Hitch, G. J. Computational models of working memory: putting long term memory into context. Trends Cogn. Sci. 9, 535–541 (2005).
Howard, M. & Kahana, M. J. A distributed representation of temporal context. J. Math. Psychol. 46, 269–299 (2002).
Manns, J. R., Howard, M. W. & Eichenbaum, H. Gradual changes in hippocampal activity support remembering the order of events. Neuron 56, 530–540 (2007).
Wallenstein, G. V., Eichenbaum, H. & Hasselmo, M. E. The hippocampus as an associator of discontiguous events. Trends Neurosci. 21, 317–323 (1998).
Eichenbaum, H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109–120 (2004).
Frank, L. M., Brown, E. N. & Wilson, M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178 (2000).
Wood, E. R., Dudchenko, P. A., Robitsek, R. J. & Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000).
Ferbinteanu, J. & Shapiro, M. L. Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227–1239 (2003).
Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828–832 (2003).
Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C. & Fried, I. Invariant visual representation by single neurons in the human brain. Nature 435, 1102–1107 (2005). This study described neurons in the human hippocampus that are tuned to respond to a single bit of abstract information, such as the identity of a specific person or monument, in a manner analogous to the place-cell representation of location.
Jeffery, K. J. & Burgess, N. A metric for the cognitive map: found at last? Trends Cogn. Sci. 10, 1–3 (2006).
We gratefully acknowledge the support of the Medical Research Council UK, the Biotechnology and Biological Sciences Research Council, UK, and a European Union Wayfinding Grant. We thank T. Shallice, J. O'Keefe, and three anonymous referees for their invaluable help in the preparation of this manuscript.
- Short-term memory
The conscious retention of information over a few seconds, often through active maintenance (rehearsal). When the information held in short-term memory is manipulated, this is often referred to as working memory.
A behavioural change that is manifested in the speed or accuracy with which a stimulus is processed following prior exposure to the same or a similar stimulus.
- Procedural learning
The unconscious learning of a skill, such as a series of actions or perceptual processing functions (for example, learning to ride a bike), which typically results in increased speed or accuracy with repetition.
- Recurrent connections
The extensive reciprocal connections between principal CA3 neurons. This unusual neural architecture might provide a substrate for the implementation of an attractor network that supports associative memory.
- Pattern completion
A process by which a stored neural representation is reactivated by a cue that consists of a subset of that representation.
- Path integration
The ability to keep track of the start position of a trajectory by integrating the movements made along the path.
- Pattern separation
A process by which small differences in patterns of input activity are amplified as they propagate through a network. This creates distinct representations.
- Attractor network
Neural networks that have one or more stable 'states' (that is, patterns of firing across neurons). The stable states are determined by the strengths of the recurrent connections between the neurons in the network. Depending on the initial conditions, the network will end up in one of the stable states. This can allow pattern completion to occur.
- Papez's circuit
A network of limbic brain structures that was originally thought to subserve emotional processing. These structures include the cingulate cortex, the hippocampus, the mammillary bodies, the anterior thalamus and the projections between these areas, such as the fornix.
Quick, simultaneous movements of both eyes in the same direction, allowing one to fixate rapidly on elements of a visual scene or a passage of text.
- Receiver operating characteristics
(ROCs). An ROC describes the relationship between hits and false alarms across varying confidence levels. Yonelinas has argued that the shape of the ROC varies according to the independent contributions of recollection and familiarity to performance on a memory task.
- Sensory buffers
Dedicated neocortical systems that (independently) support the short-term maintenance of sensory, motor, linguistic or other information.
- Unitized stimuli
Uni-modal elements of an event that, according to dual-process and relational theories, can be represented and subsequently recognized by brain regions outside of the hippocampus.
- Theta frequency range
Rhythmic activity (4–12 Hz) detected in the local field potential or by electroencephalogram. This rhythm is particularly prominent in the hippocampus of rats during locomotion and has recently been related to mnemonic processing in both rats and humans.
About this article
Brain Imaging and Behavior (2019)
Effective connectivity within the ventromedial prefrontal cortex-hippocampus-amygdala network during the elaboration of emotional autobiographical memories
Association of interleukin-6 rs1800796 polymorphism with reduced cognitive performance in healthy older adults
Meta Gene (2019)
Atmospheric pressure mass spectrometric imaging of bio-tissue specimen using electrospray-assisted CW laser desorption and ionization source
Behavioural Brain Research (2019)