Much progress has been made by cognitive neuroscientists in understanding the separate roles of the medial temporal and prefrontal lobes in memory, but the way in which these regions interact in the processes of remembering has been neglected. This review provides a synthesis of evidence from human and animal neuropsychology, functional neuroimaging, neurophysiology and computational modelling, through which the functional interactions between prefrontal and medial temporal cortices can be better understood.
Since the first reports of patients with amnesia, evidence has converged on a role for the medial temporal lobes in the encoding, storage and retrieval of long-term memories. Controversies include whether there is differential involvement of regions such as the hippocampus and perirhinal cortex in processes of recollection and familiarity, and the long-term role of these regions in consolidation of memories from the past.
The prefrontal cortex is considered to support processes of cognitive control that are important for memory function. Accordingly, frontal lobe damage is often associated with particular memory impairments. Regional distinctions are evident within the frontal lobes, with left/right lateralization on the basis of material type and medial/lateral differentiation between reward-based mapping and goal-directed mnemonic control, respectively. Within lateral prefrontal cortex, there is a further distinction between ventral (specification and maintenance) and dorsal (monitoring and manipulation) regions.
Recent advances in primate crossed-lesion neuropsychology, human functional effective connectivity, single-cell electrophysiology and computational modelling highlight the importance of interactions between prefrontal cortex and medial temporal lobe in remembering. These new insights indicate that an understanding of these interactions will be crucial if we are to move closer to a full account of how memory is supported in the brain.
At encoding, information is processed by a hierarchy of unimodal and polymodal cortical areas, resulting in a bound representation of associated features in the medial temporal lobe. Through interactions with different regions of prefrontal cortex, top-down control of the encoding process is provided, modifying, elaborating and organizing medial temporal lobe representations in a goal-dependent manner, and ensuring that they are sufficiently discrete to be amenable for long-term storage.
During retrieval, the prefrontal cortex and medial temporal lobes interact in the specification of retrieval cues, searching the long-term store using those cues, reactivating stored information, and monitoring, disambiguation and verification of retrieved information. If a retrieval attempt is not sufficiently successful, the retrieval cue might be modified and further search interactions undertaken.
Cognitive neuroscience has made considerable progress in understanding the involvement of the medial temporal and frontal lobes in long-term memory. Whereas the medial temporal lobe has traditionally been associated with the encoding, storage and retrieval of long-term memories, the prefrontal cortex has been linked with cognitive control processes such as selection, engagement, monitoring and inhibition. However, there has been little attempt to understand how these regions might interact during encoding and retrieval, and little consideration of the anatomical connections between them. Recent advances in functional neuroimaging, neurophysiology, crossed-lesion neuropsychology and computational modelling highlight the importance of understanding how the medial temporal and frontal lobes interact to allow successful remembering, and provide an opportunity to explore these interactions.
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Scoville, W. B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).
Marr, D. Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B 262, 23–81 (1971).
Squire, L. R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231 (1992).
Fuster, J. M. Memory in the Cerebral Cortex (MIT Press, Cambridge, Massachusetts, 1995).
Shimamura, A. P. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 803–813 (MIT Press, Cambridge, Massachusetts, 1995).
Cohen, N. J. & Eichenbaum, H. B. Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, Massachusetts, 1993).
Aggleton, J. P. & Brown, M. W. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci. 22, 425–489 (1999). An important paper providing evidence that different anatomical circuits, including the hippocampus and perirhinal cortex, are involved in recollection and familiarity, respectively.
Van Hoesen, G. W., Augustinack, J. C. & Redman, S. J. Ventromedial temporal lobe pathology in dementia, brain trauma, and schizophrenia. Ann. NY Acad. Sci. 877, 575–594 (1999).
Petrides, M. in The Prefrontal Cortex: Executive and Cognitive Functions (eds Roberts, A. C., Robbins, T. W. & Weiskrantz, L.) 103–116 (Oxford Univ. Press, Oxford, 1998).
Preuss, T. M. Do rats have prefrontal cortex: The Rose-Woolsey-Akert program reconsidered. J. Cogn. Neurosci. 7, 1–24 (1995).
Semendeferi, K., Lu, A., Schenker, N. & Damasio, H. Humans and great apes share a large frontal cortex. Nature Neurosci. 5, 272–276 (2002).
Corkin, S. What's new with the amnesic patient H.M.? Nature Rev. Neurosci. 3, 153–160 (2002).
Zola, S. M. et al. Impaired recognition memory in monkeys after damage limited to the hippocampal region. J. Neurosci. 20, 451–463 (2000).
Morris, R. G. M., Garrud, P., Rawlins, J. P. & O'Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681–683 (1982).
Aggleton, J. P., Hunt, P. R. & Rawlins, J. N. P. The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav. Brain Res. 40, 145–157 (1986).
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).
O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, Oxford, 1978).
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).
Meunier, M., Bachevalier, J., Mishkin, M. & Murray, E. A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J. Neurosci. 13, 5418–5432 (1993).
Suzuki, W. A., Zola-Morgan, S., Squire, L. R. & Amaral, D. G. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J. Neurosci. 13, 2430–2451 (1993).
Ennaceur, A., Neave, N. & Aggleton, J. P. Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav. Brain Res. 80, 9–25 (1996).
Murray, E. A. & Mishkin, M. Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J. Neurosci. 18, 6568–6582 (1998).
Gaffan, D., Shields, C. & Harrison, S. Delayed matching by fornix-transected monkeys: The sample, the push and the bait. Q J Exp Psychol B. 36, 305–317 (1984).
Clark, R. E., Zola, S. M. & Squire, L. R. Impaired recognition memory in rats after damage to the hippocampus. J. Neurosci. 20, 8853–8860 (2000). Evidence against a functional dissociation between the hippocampus and perirhinal cortex in memory.
Miller, E. K., Li, L. & Desimone, R. A neural mechanism for working and recognition memory in inferior temporal cortex. Science 254, 1377–1379 (1991).
Fahy, F. L., Riches, I. P. & Brown, M. W. Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex. Exp. Brain Res. 96, 457–472 (1993).
Riches, I. P., Wilson, F. A. W. & Brown, M. W. The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate. J. Neurosci. 11, 1763–1779 (1991).
Rolls, E. T., Cahusac, P. M. B., Feigenbaum, J. D. & Miyashita, Y. Responses of single neurons in the hippocampus of the macaque related to recognition memory. Exp. Brain Res. 93, 299–306 (1993).
Buckley, M. J., Booth, M. C. A., Rolls, E. T. & Gaffan, D. Selective perceptual impairments after perirhinal cortex ablation. J. Neurosci. 21, 9824–9836 (2001).
Murray, E. A. & Bussey, T. J. Perceptual-mnemonic functions of the perirhinal cortex. Trends Cogn. Sci. 3, 142–151 (1999).
Aggleton, J. P. & Shaw, C. Amnesia and recognition memory: a re-analysis of psychometric data. Neuropsychologia 34, 51–62 (1996).
Baddeley, A. D., Vargha-Khadem, F. & Mishkin, M. Preserved recognition in a case of developmental amnesia: implications for the acquisition of semantic memory? J. Cogn. Neurosci. 13, 357–369 (2001).
Holdstock, J. S. et al. A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage. Neuropsychologia 38, 410–425 (2000).
Yonelinas, A. P. et al. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nature Neurosci. 5, 1236–1241 (2002). An elegant study examining whether damage to different regions of the human medial temporal lobe leads to differential impairment in recollection and familiarity.
Manns, J. R. & Squire, L. R. Impaired recognition memory on the Doors and People Test after damage limited to the hippocampal region. Hippocampus 9, 495–499 (1999).
Buffalo, E. A., Reber, P. J. & Squire, L. R. The human perirhinal cortex and recognition memory. Hippocampus 8, 330–339 (1998).
Holdstock, J. S., Gutnikov, S. A., Gaffan, D. & Mayes, A. R. Perceptual and mnemonic matching-to-sample in humans: contributions of the hippocampus, perirhinal and other medial temporal lobe cortices. Cortex 36, 301–322 (2000).
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).
Simons, J. S., Graham, K. S. & Hodges, J. R. Perceptual and semantic contributions to episodic memory: evidence from semantic dementia and Alzheimer's disease. J. Mem. Lang. 47, 197–213 (2002).
Graham, K. S. & Hodges, J. R. Differentiating the roles of the hippocampal complex and the neocortex in long-term memory storage: evidence from the study of semantic dementia and Alzheimer's disease. Neuropsychology 11, 77–89 (1997).
Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia, and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217–227 (1997).
Cipolotti, L. et al. Long-term retrograde amnesia...the crucial role of the hippocampus. Neuropsychologia 39, 151–172 (2001).
Spiers, H. J., Maguire, E. A. & Burgess, N. Hippocampal amnesia. Neurocase 7, 357–382 (2001). A useful reference for a description of 147 cases of amnesia after damage to the medial temporal lobes.
Schacter, D. L. & Wagner, A. D. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 9, 7–24 (1999).
Maguire, E. A. et al. Knowing where and getting there: a human navigation network. Science 280, 921–924 (1998).
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).
Schacter, D. L., Alpert, N. M., Savage, C. R., Rauch, S. L. & Albert, M. S. Conscious recollection and the human hippocampal formation: Evidence from positron emission tomography. Proc. Natl Acad. Sci. USA 93, 321–325 (1996).
Burgess, N., Maguire, E. A., Spiers, H. J. & O'Keefe, J. A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. Neuroimage 14, 439–453 (2001). A neuroimaging experiment providing evidence for a network of brain regions, including medial temporal and prefrontal cortices, that are activated during retrieval of different episodic contexts.
Eldridge, L. L., Knowlton, B. J., Furmanski, C. S., Bookheimer, S. Y. & Engel, S. A. Remembering episodes: a selective role for the hippocampus during retrieval. Nature Neurosci. 3, 1149–1152 (2000).
Cansino, S., Maquet, P., Dolan, R. J. & Rugg, M. D. Brain activity underlying encoding and retrieval of source memory. Cereb. Cortex 12, 1048–1056 (2002).
Dobbins, I. G., Rice, H. J., Wagner, A. D. & Schacter, D. L. Memory orientation and success: separable neurocognitive components underlying episodic recognition. Neuropsychologia 41, 318–333 (2003).
Davachi, L., Mitchell, J. P. & Wagner, A. D. Multiple routes to memory: distinct medial temporal lobe processes build item and source memories. Proc. Natl Acad. Sci. USA 100, 2157–2162 (2003).
Henson, R. N. A., Cansino, S., Herron, J. E., Robb, W. G. K. & Rugg, M. D. A familiarity signal in human anterior medial temporal cortex? Hippocampus 13, 259–262 (2003).
Hasselmo, M. E. & Wyble, B. P. Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function. Behav. Brain Res. 89, 1–34 (1997).
McClelland, J. L., McNaughton, B. L. & O'Reilly, R. C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the success and failure 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).
O'Reilly, R. C. & Rudy, J. W. Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol. Rev. 108, 311–345 (2001).
Murre, J. M. J. TraceLink: a model of amnesia and consolidation of memory. Hippocampus 6, 675–684 (1996).
Nadel, L., Samsonovich, A., Ryan, L. & Moscovitch, M. Multiple trace theory of human memory: computational, neuroimaging, and neuropsychological results. Hippocampus 10, 352–368 (2000).
Brown, M. A. & Sharp, P. E. Simulation of spatial-learning in the Morris water maze by a neural-network model of the hippocampal-formation and nucleus-accumbens. Hippocampus 5, 171–188 (1995).
Burgess, N., Donnett, J. G., Jeffery, K. J. & O'Keefe, J. Robotic and neuronal simulation of the hippocampus and rat navigation. Phil. Trans. R. Soc. Lond. B 352, 1535–1543 (1997).
Burgess, N., Becker, S., King, J. A. & O'Keefe, J. Memory for events and their spatial context: models and experiments. Phil. Trans. R. Soc. Lond. B 356, 1493–1503 (2001).
Shimamura, A. P., Janowsky, J. S. & Squire, L. R. Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients. Neuropsychologia 28, 803–813 (1990).
Schacter, D. L., Harbluk, J. L. & McLachlan, D. R. Retrieval without recollection: an experimental analysis of source amnesia. J. Verb. Learn. Verb. Behav. 23, 593–611 (1984).
Simons, J. S. et al. Recollection-based memory in frontotemporal dementia: implications for theories of long-term memory. Brain 125, 2523–2536 (2002). Evidence that frontal lobe dysfunction can be a better predictor than hippocampal atrophy of recollection impairment.
Incisa della Rocchetta, A. & Milner, B. Strategic search and retrieval inhibition: the role of the frontal lobes. Neuropsychologia 31, 503–524 (1993).
Moscovitch, M. in Varieties of Memory and Consciousness: Essays in Honour of Endel Tulving (eds Roediger, H. L. & Craik, F. I. M.) 133–160 (Erlbaum, London, 1989).
Burgess, P. W. & Shallice, T. Confabulation and the control of recollection. Memory 4, 359–411 (1996). An influential model of the processes of episodic retrieval in relation to frontal lobe function.
Rolls, E. T., Hornak, J., Wade, D. & McGrath, J. Emotion-related learning in patients with social and emotional changes associated with frontal-lobe damage. J. Neurol. Neurosurg. Psychiatry 57, 1518–1524 (1994).
Henson, R. N. A., Rugg, M. D., Shallice, T., Josephs, O. & Dolan, R. J. Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. J. Neurosci. 19, 3962–3972 (1999). Functional magnetic resonance imaging (fMRI) evidence that different prefrontal patterns of activity are characteristic of recollection and familiarity during encoding and retrieval.
Wilson, F. A. W., Ó Scalaidhe, S. P. & Goldman-Rakic, P. S. Dissociation of object and spatial processing domains in prefrontal cortex. Science 260, 1955–1958 (1993).
Duncan, J. & Owen, A. M. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 23, 475–483 (2000).
Freedman, D. J., Riesenhuber, M., Poggio, T. & Miller, E. K. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291, 312–316 (2001).
Duncan, J. An adaptive coding model of neural function in prefrontal cortex. Nature Rev. Neurosci. 2, 820–829 (2001).
Tulving, E., Kapur, S., Craik, F. I. M., Moscovitch, M. & Houle, S. Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc. Natl Acad. Sci. USA 91, 2016–2020 (1994).
Nyberg, L., Cabeza, R. & Tulving, E. PET studies of encoding and retrieval: the HERA model. Psychon. Bull. Rev. 3, 135–148 (1996).
Kelley, W. M. et al. Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron 20, 927–936 (1998).
Wagner, A. D. et al. Material-specific lateralization of prefrontal activation during episodic encoding and retrieval. Neuroreport 9, 3711–3717 (1998).
Simons, J. S., Graham, K. S., Owen, A. M., Patterson, K. & Hodges, J. R. Perceptual and semantic components of memory for objects and faces: a PET study. J. Cogn. Neurosci. 13, 430–443 (2001).
Baxter, M. G., Parker, A., Lindner, C. C. C., Izquierdo, A. D. & Murray, E. A. Control of response selection by reinforcer values requires interaction of amygdala and orbital prefrontal cortex. J. Neurosci. 20, 4311–4319 (2000).
Elliott, R., Dolan, R. J. & Frith, C. D. Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb. Cortex 10, 308–317 (2000).
Fletcher, P. C. & Henson, R. N. A. Frontal lobes and human memory: insights from functional neuroimaging. Brain 124, 849–881 (2001).
Wagner, A. D. et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281, 1188–1191 (1998).
Dobbins, I. G., Foley, H., Schacter, D. L. & Wagner, A. D. Executive control during episodic retrieval: multiple prefrontal processes subserve source memory. Neuron 35, 989–996 (2002). fMRI evidence that different regions of prefrontal cortex are involved in the cue specification, maintenance and monitoring/evaluation stages of episodic memory.
D'Esposito, M., Postle, B. R., Ballard, D. & Lease, J. Maintenance versus manipulation of information held in working memory: an event-related fMRI study. Brain Cogn. 41, 66–86 (1999).
Wagner, A. D., Maril, A., Bjork, R. A. & Schacter, D. L. Prefrontal contributions to executive control: fMRI evidence for functional distinctions within lateral prefrontal cortex. Neuroimage 14, 1337–1347 (2001).
Poldrack, R. A. et al. Functional specialization for semantic and phonological processing in the left inferior frontal cortex. Neuroimage 10, 15–35 (1999).
Fletcher, P. C., Shallice, T. & Dolan, R. J. The functional roles of prefrontal cortex in episodic memory. I. Encoding. Brain 121, 1239–1248 (1998).
Petrides, M., Alivisatos, B., Evans, A. C. & Meyer, E. Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. Proc. Natl Acad. Sci. USA 90, 873–877 (1993).
Rugg, M. D., Fletcher, P. C., Chua, P. M. L. & Dolan, R. J. The role of the prefrontal cortex in recognition memory and memory for source: an fMRI study. Neuroimage 10, 520–529 (1999).
Koechlin, E., Basso, G., Pietrini, P., Panzer, S. & Grafman, J. The role of the anterior prefrontal cortex in human cognition. Nature 399, 148–151 (1999).
Christoff, K. & Gabrieli, J. D. E. The frontopolar cortex and human cognition: evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex. Psychobiology 28, 168–186 (2000). A proposal that anterior prefrontal cortex might lie at the top of a processing hierarchy in the prefrontal cortex, operating on higher-order representations such as internally generated information.
Burgess, P. W., Scott, S. K. & Frith, C. D. The role of the rostral frontal cortex (area 10) in prospective memory: a lateral versus medial dissociation. Neuropsychologia 41, 906–918 (2003).
Norman, D. A. & Shallice, T. in Consciousness and Self-Regulation (eds Davidson, R. J., Schwartz, G. & Shapiro, D.) 1–18 (Plenum, New York, 1986).
Dehaene, S. & Changeux, J. P. A hierarchical neuronal network for planning behavior. Proc. Natl Acad. Sci. USA 94, 13293–13298 (1997).
Becker, S. & Lim, J. A computational model of prefrontal control in free recall: strategy memory use in the California Verbal Learning Task. J. Cogn. Neurosci. (in the press). A computational model of the interaction between the prefrontal and medial temporal regions in long-term memory.
Warrington, E. K. & Weiskrantz, L. Amnesia: a disconnection syndrome? Neuropsychologia 20, 233–248 (1982). A seminal paper suggesting that amnesia might be caused by a disconnection between frontal and temporal brain regions.
Levine, B. et al. Episodic memory and the self in a case of isolated retrograde amnesia. Brain 121, 1951–1973 (1998).
Pascual-Leone, A. & Walsh, V. Fast backprojections from the motion to the primary visual area necessary for visual awareness. Science 292, 510–512 (2001).
Gaffan, D. & Harrison, S. Inferotemporal-frontal disconnection and fornix transection in visuomotor conditional learning by monkeys. Behav. Brain Res. 31, 149–163 (1988).
Gaffan, D., Easton, A. & Parker, A. Interaction of inferior temporal cortex with frontal cortex and basal forebrain: double dissociation in strategy implementation and associative learning. J. Neurosci. 22, 7288–7296 (2002). An interesting paper that used crossed-lesion methodology to show that disruption of different frontotemporal connections affects performance on different memory tasks.
Bussey, T. J., Wise, S. P. & Murray, E. A. Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. Behav. Neurosci. 116, 703–715 (2002).
Eacott, M. J. & Gaffan, D. Inferotemporal-frontal disconnection: the uncinate fascicle and visual associative learning in monkeys. Eur. J. Neurosci. 4, 1320–1332 (1992).
Hunt, P. R. & Aggleton, J. P. Medial dorsal thalamic lesions and working memory in the rat. Behav. Neural Biol. 55, 227–246 (1991).
Parker, A., Eacott, M. J. & Gaffan, D. The recognition memory deficit caused by mediodorsal thalamic lesion in nonhuman primates: a comparison with rhinal cortex lesion. Eur. J. Neurosci. 9, 2423–2431 (1997).
Lee, I. & Kesner, R. P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J. Neurosci. 23, 1517–1523 (2003).
Kirchhoff, B. A., Wagner, A. D., Maril, A. & Stern, C. E. Prefrontal-temporal circuitry for episodic encoding and subsequent memory. J. Neurosci. 20, 6173–6180 (2000).
Otten, L. J. & Rugg, M. D. Task-dependency of the neural correlates of episodic encoding as measured by fMRI. Cereb. Cortex 11, 1150–1160 (2001).
McDermott, K. B., Buckner, R. L., Petersen, S. E., Kelley, W. M. & Sanders, A. L. Set- and code-specific activation in the frontal cortex: an fMRI study of encoding and retrieval of faces and words. J. Cogn. Neurosci. 11, 631–640 (1999).
Nyberg, L. et al. Functional brain maps of retrieval mode and recovery of episodic information. Neuroreport 7, 249–252 (1995).
Maril, A., Simons, J. S., Mitchell, J. P., Schwartz, B. L. & Schacter, D. L. Feeling-of-knowing in episodic memory: an event-related fMRI study. Neuroimage 18, 827–836 (2003).
McIntosh, A. R., Nyberg, L., Bookstein, F. L. & Tulving, E. Differential functional connectivity of prefrontal and medial temporal cortices during episodic memory retrieval. Hum. Brain Mapp. 5, 323–327 (1997).
Büchel, C., Coull, J. T. & Friston, K. J. The predictive value of changes in effective connectivity for human learning. Science 283, 1538–1541 (1999).
Köhler, S., McIntosh, A. R., Moscovitch, M. & Winocur, G. Functional interactions between the medial temporal lobes and posterior neocortex related to episodic memory retrieval. Cereb. Cortex 8, 451–461 (1998).
Maguire, E. A., Vargha-Khadem, F. & Mishkin, M. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124, 1156–1170 (2001). One of the few studies that has examined effective connectivity associated with memory retrieval and explored the effects of damage to one of the primary brain regions on interactivity.
Frackowiak, R. S. J., Friston, K. J., Frith, C. D., Dolan, R. J. & Price, C. J. Human Brain Function (Academic, New York, in the press).
Fuster, J. M., Bodner, M. & Kroger, J. K. Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405, 347–351 (2000).
Miller, E. K., Erickson, C. A. & Desimone, R. Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J. Neurosci. 16, 5154–5167 (1996).
Hasegawa, I., Fukushima, T., Ihara, T. & Miyashita, Y. Callosal window between prefrontal cortices: cognitive interaction to retrieve long-term memory. Science 281, 814–818 (1998).
Rainer, G., Rao, S. C. & Miller, E. K. Prospective coding for objects in primate prefrontal cortex. J. Neurosci. 19, 5493–5505 (1999).
Tomita, H., Ohbayashi, M., Nakahara, K., Hasegawa, I. & Miyashita, Y. Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature 401, 699–703 (1999). A study that used extracellular electrode recordings and cortical disconnection to examine the role of prefrontal cortex in providing top-down control of memory representations in temporal cortex.
Brewer, J. B., Zhao, Z., Desmond, J. E., Glover, G. H. & Gabrieli, J. D. E. Making memories: brain activity that predicts how well visual experience will be remembered. Science 281, 1185–1187 (1998).
Schacter, D. L., Buckner, R. L., Koutstaal, W., Dale, A. M. & Rosen, B. R. Late onset of anterior prefrontal activity during true and false recognition: an event-related fMRI study. Neuroimage 6, 259–269 (1997).
Henson, R. N. A., Shallice, T. & Dolan, R. J. Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain 122, 1367–1381 (1999).
Rempel-Clower, N. L. & Barbas, H. The laminar pattern of connections between prefrontal and anterior temporal cortices in the rhesus monkey is related to cortical structure and function. Cereb. Cortex 10, 851–865 (2000).
Lavenex, P. & Amaral, D. G. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10, 420–430 (2000).
Rosene, D. L. & Van Hoesen, G. W. Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198, 315–317 (1977).
Barbas, H. & Blatt, G. J. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 5, 511–533 (1995).
Goldman-Rakic, P. S., Selemon, L. D. & Schwartz, M. L. Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12, 719–743 (1984).
Barbas, H., Ghashghaei, H., Dombrowski, S. M. & Rempel-Clower, N. L. Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J. Comp. Neurol. 410, 343–367 (1999).
Suzuki, W. A. & Amaral, D. G. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J. Comp. Neurol. 350, 497–533 (1994).
Thierry, A. -M., Gioanni, Y., Degenetais, E. & Glowinski, J. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 10, 411–419 (2000).
Martin, J. H. Neuroanatomy: Text and Atlas 2nd edn (Appleton & Lange, Stamford, Connecticut, 1996).
Baddeley, A. D., Emslie, H. & Nimmo-Smith, I. The Doors and People Test (Thames Valley Test Company, Bury St. Edmunds, 1994).
We are very grateful to M. Baxter, S. Becker, N. Burgess, J. Gimpel, R. Henson, M. Rugg and D. Schacter for valuable comments on an earlier draft. J.S.S. is supported by a Wellcome Trust grant and H.J.S. by the Alzheimer's Research Trust.
A major input/output of the hippocampus, connecting it to prefrontal cortex and a range of subcortical structures.
- FAMILIARITY-BASED MEMORY
Recognition of previously presented items based on a feeling of familiarity in the absence of recollection of the earlier study episode.
- DELAYED NON-MATCHING-TO-SAMPLE
A task in which an object/item is presented and following a delay, presented again along with a new item, and the participant is required to choose the new item.
- SEMANTIC DEMENTIA
A degenerative neuropathological condition that results in the progressive loss of semantic knowledge as revealed through naming, description and non-verbal tests of semantic knowledge, resulting from disease of the anterior and lateral aspects of the temporal lobes.
- RECURRENT COLLATERALS
Axon connections between pyramidal cells in the CA3 region of the hippocampus.
- PATTERN SEPARATION
A process by which overlapping neural representations are separated to keep episodes independent of each other in memory.
- PATTERN COMPLETION
A process by which a stored neural representation is reactivated by a cue that consists of a subset of the stored pattern.
- EPISODIC MEMORY
Memory for events and episodes, which are uniquely characterized by a specific time and place.
- WORKING MEMORY
Short-lasting memory associated with active maintenance and rehearsal of information.
- EFFECTIVE CONNECTIVITY
Multivariate analysis of activity in different regions to model the influence that regions exert over each other.
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Simons, J., Spiers, H. Prefrontal and medial temporal lobe interactions in long-term memory. Nat Rev Neurosci 4, 637–648 (2003). https://doi.org/10.1038/nrn1178
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