Abstract
Many studies have identified the prefrontal cortex as the brain area that is critical for spatial memory, both in humans and in other primates. Other studies, however, have failed to establish this relation. Therefore, the aim of this paper was to review the literature regarding the role of the human prefrontal lobe in spatial memory. This was done by examining the evidence obtained from neuropsychological patients and from studies using brain-imaging techniques (PET and fMRI). Evidence supporting the notion that the prefrontal cortex is extensively involved in spatial working memory was found. The majority of these studies, however, suggests that frontal-lobe involvement is not related to the type of material that is being processed (e.g., spatial vs. nonspatial), but to process-specific functions, such as encoding and retrieval. Theoretically, these functions could be linked to the central executive within Baddeley's working-memory model, or to recent theories that emphasize the various processes that play a role in working memory. Also, methodological issues were discussed. Further research is needed to enhance our understanding of the precise interaction of domain-specific and general processes.
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REFERENCES
Aine, C. J. (1995). A conceptual overviewand critique of functional neuroimaging techniques in humans: I. MRI/fMRI and PET. Critical Reviews in Neurobiology 9: 229–309.
Bachevalier, J., and Mishkin, M. (1986). Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys. Behavioural Brain Research 20: 249–261.
Baddeley, A. D. (1996). Exploring the central executive. Quarterly Journal of Experimental Psychology 49A: 5–28.
Baddeley, A. D., and Hitch, G. J. (1994). Developments in the concept of working memory. Neuropsychology 8: 495–493.
Baker, S. C., Frith, C. D., Frackowiak, R. S. J., and Dolan, R. J. (1996). Active representation of shape and spatial location in man. Cerebral Cortex 6: 612–619.
Barbas, H., and Rempel-Clower, N. (1997). Cortical structure predicts the pattern of corticocortical connections. Cerebral Cortex 7: 635–646.
Belger, A., Puce, A., Krystal, J. H., Gore, J. C., Goldman-Rakic, P., and McCarthy, G. (1998). Dissociation of mnemonic and perceptual processes during spatial and nonspatial working memory using fMRI. Human Brain Mapping 6: 14–32.
Benton, A. L. (1969). Disorders of spatial orientation. In Vinken, P. J., and Bruyn, G. W. (eds.), Disorders of Higher Neurons Activity, North-Holland, Amsterdam, pp. 212–228.
Berch, D. B., Kirkorian, R., and Huha, E. M. (1998). The Corsi Block-Tapping Task: Methodological and theoretical considerations. Brain and Cognition 38: 317–338.
Berg, M. L., and May, J. G. (1998). Parallel processing in visual perception and memory: What goes where and when? Current Psychology: Developmental, Learning, Personality, Social 16: 247–283.
Buckner, R. L., Kelley, W. M., and Petersen, S. E. (1999). Frontal cortex contribution to human memory formation. Nature Neuroscience 2: 311–314.
Cabezo, R., Kapur, S., Craik, F. I. M., McIntosh, A. R., Houle, S., and Tulving, E. (1997). Functional neuroanatomy of recall and recognition: A PET study of episodic memory. Journal of Cognitive Neuroscience 9: 254–265.
Canavan, A. G. M. (1983). Stylus-maze performance in patients with frontal-lobe lesions: Effects of signal valency and relationship to verbal and spatial abilities. Neuropsychologia 21: 375–382.
Carlson, S., Martinkauppi, S., Räma, P., Salli, E., Korvenoja, A., and Aronen, H. J. (1998). Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. Cerebral Cortex 8: 743–752.
Casey, B. J., Cohen, J. D., O'Craven, K., Davidson, R. J., Irwin, W., Nelson, C. A., Noll, D. C., Hu, X., Lowe, M. J., Rosen, B. R., Truwitt, C. L., and Turski, P. A. (1998). Reproducibility of fMRI results across four institutions using a spatialworking memory task. Neuroimage 8: 249–261.
Chalfonte, B. L., and Johnson, M. K. (1996). Feature memory and binding in young and older adults. Memory and Cognition 24: 403–416.
Cohen, J. D., Perlstein, W. M., Braver, T. S., Nystrom, L. E., Noll, D. C., Jonides, J., and Smith, E. E. (1997). Temporal dynamics of brain activation during a working memory task. Nature 386: 604–608.
Corkin, S. (1965). Tactually-guided maze learning in man: Effects of unilateral cortical excisions and bilateral hippocampal lesions. Neuropsychologia 3: 339–351.
Courtney, S. M., Petit, L., Haxby, J. V., and Ungerleider, L. G. (1998a). The role of prefrontal cortex in working memory: Examining the contents of consciousness. Philosophical Transactions of the Royal Society of London 353B: 1819–1928.
Courtney, S. M., Petit, L., Maisog, J. M., Ungerleider, L. G., and Haxby, J. V. (1998b). An area specialized for spatial working memory in human frontal cortex. Science 279: 1347–1351.
Courtney, S. M., Ungerleider, L. M., Keil, K., and Haxby, J. V. (1996). Object and spatial visual working memory activate separate neural systems in human cortex. Cerebral Cortex 6: 39–49.
Damasio, A. R. (1995). On some functions of the human prefrontal cortex. Annals of the New York Academy of Sciences 769: 241–251.
D'Esposito, M., Aguirre, G. K., Zarahn, E., Ballard, D., Shin, R. K., and Lease, J. (1998). Functional MRI studies of spatial and nonspatial working memory. Cognitive Brain Research 7: 1–13.
D'Esposito, M., Detre, J. A., Alsop, D. C., Shin, R. K., Atlas, S., and Grossman, M. (1995). The neural basis of the central executive of working memory. Nature 378: 279–281.
D'Esposito, M., Zarahn, E., and Aguirre, G. K. (1999). Event-related functional MRI: Implications for cognitive psychology. Psychological Bulletin 125: 155–164.
De Haan, E. H. F., Young, A. W., and Newcombe, F. (1991). Covert and overt recognition in prosopagnosia. Brain 114: 2575–2591.
De Renzi, E., Faglioni, P., and Previdi, P. (1977). Spatial memory and hemispheric locus of lesion. Cortex 13: 424–433.
Ferreira, C. T., Vérin, M., Pillon, B., Levy, R., Dubois, B., and Agid, Y. (1998). Spatio-temporal working memory and frontal lesions in man. Cortex 34: 83–98.
Fletcher, P. C., Frith, C. D., and Rugg, M. D. (1997). The functional neuroanatomy of episodic memory. Trends in Neurosciences 20: 213–218.
Fletcher, P. C., Shallice, T., and Dolan, R. J. (1998a). The functional roles of prefrontal cortex in episodic memory: I. Encoding. Brain 121: 1239–1248.
Fletcher, P. C., Shallice, T., Frith, C. D., Frackowiak, R. S. J., and Dolan, R. J. (1998b). The functional roles of prefrontal cortex in episodic memory: II. Retrieval. Brain 121: 1249–1256.
Foong, J., Rozewics, L., Quaghebeur, G., Davie, C. A., Kartsounis, L. D., Thompson, A. J., Miller, D. H., and Ron, M. A. (1997). Executive functions in multiple sclerosis: The role of frontal lobe pathology. Brain 120: 15–26.
Fuster, J. M. (1995). Memory and planning: Two temporal perspectives of frontal lobe function. Advances in Neurology 66: 9–20.
Fuster, J. M. (1997). The Prefrontal Cortex, Lippincott-Raven, Philadelphia.
Gevins, A., Smith, M. E., Le, J., Leong, H., Bennet, J., Martin, N., McEvoy, L., Du, R., and Whitfield, S. (1996). High resolution evoked potential imaging of the cortical dynamics of human working memory. Electroencephalography and Clinical Neurophysiology 98: 327–348.
Goldman-Rakic, P. S. (1987). Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In Plum, F. (ed.), Handbook of Physiology: The Nervous System, Vol. 5, American Physiological Society, Bethesa, MD, pp. 373–417.
Goodale, M. A., and Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences 15: 20–25.
Hecker, R., and Mapperson, B. (1997). Dissociation of visual and spatial processing in working memory. Neuropsychologia 35: 599–603.
Heil, M., Rösler, F., and Hennighausen, E. (1997). Topography of brain electrical activity dissociates the retrieval of spatial versus verbal information from episodic long-term memory in humans. Neuroscience Letters 222: 45–48.
Johnsrude, I. S., Owen, A. M., Crane, J., Milner, B., and Evans, A. C. (1999). A cognitive activation study of memory for spatial relationships. Neuropsychologia 37: 829–841.
Jonides, J., Reuter-Lorenz, P. A., Smith, E. E., Awh, E., Barnes, L. L., Drain, M., Glass, J., Lauber, E. J., Patalano, A. L., and Schumacher, E. H. (1996). Verbal and spatial working memory in humans. Psychology of Learning and Motivation 35: 43–88.
Jonides, J., Smith, E. E., Koeppe, R. A., Awh, E., Minoshima, S., and Mintun, M. A. (1993). Spatial working memory in humans as revealed by PET. Nature 363: 623–625.
Joyce, E. M., and Robbins, T. W. (1991). Frontal lobe function in Korsakoff and non-Korsakoff alcoholics: Planning and spatial working memory. Neuropsychologia 29: 709–723.
Kessels, R. P. C., Postma, A., and De Haan, E. H. F. (1999). P and M channel-specific interference in the what and where pathway. Neuroreport 10: 3765–3767.
Kessels, R. P. C., Postma, A., Wester, A. J., and De Haan, E. H. F. (2000). Memory for object locations in Korsakoff's amnesia. Cortex 36: 47–57.
Kapur, S., Craik, F. I. M., Jones, C., Brown, G. M., Houle, S., and Tulving, E. (1995). Functional role of the prefrontal cortex in retrieval of memories: A PET study. Neuroreport 6: 1880–1884.
Köhler, S., Moscovitch, M., Winocur, G., Houle, S., and McIntosh, A. R. (1998). Networks of domain-specific and general regions involved in episodic memory for spatial location and object identity. Neuropsychologia 36: 129–142.
Kopelman, M. D., Stanhope, N., and Kingsley, D. (1997). Temporal and spatial context memory in patiants with focal frontal, temporal lobe, and diencephalic lesions. Neuropsychologia 35: 1533–1545.
Lepage, M., Ghaffar, O., Nyberg, L., and Tulving, E. (2000). Prefrontal cortex and episodic memory retrieval mode. Proceedings of the National Academy of Sciences of the United States of America 97: 506–511.
Lewis, R. S. (1989). Remembering and the prefrontal cortex. Psychobiology 17: 102–107.
Luzzatti, C., Vecchi, T., Agazzi, D., Cesa-Bianchi, M., and Vergani, C. (1998). A neurological dissociation between preserved visual and impaired spatial processing in mental imagery. Cortex 34: 461–469.
McCarthy, G., Blamire, A. M., Puce, A., Nobre, A. C., Bloch, G., Hyder, F., Goldman-Rakic, P., and Shulman, R. G. (1994). Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. Proceedings of the National Academy of Sciences of the United States of America 91: 8690–8694.
McCarthy, G., Puce, A., Constable, R. T., and Krystal, J. H. (1996). Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. Cerebral Cortex 6: 600–611.
Milner, B. (1965). Visually-guided maze learning in man: Effects of bilateral hippocampal, bilateral frontal and unilateral cerebral lesions. Neuropsychologia 3: 317–338.
Milner, B. (1971). Interhemispheric differences in the localization of psychological processes in man. British Medical Bulletin 27: 272–277.
Miotto, E. C., Bullock, P., Polkey, C. E., and Morris, R. G. (1996). Spatial working memory and strategy formation in patients with frontal lobe excisions. Cortex 32: 613–630.
Morris, R. G., Miotto, E. C., Feigenbaum, J. D., Bullock, B., and Polkey, C. E. (1997). The effect of goal-subgoal conflict on planning ability after frontal-and temporal-lobe lesions in humans. Neuropsychologia 35: 1147–1157.
Morris, R. G., Rowe, A., Fox, N., Feigenbaum, J. D., Miotto, E. C., and Howlins, P. (1999). Spatial working memory in Asperger's syndrome and in patients with focal frontal and temporal lobe lesions. Brain and Cognition 41: 9–26.
Moscovitch, M. (1992). Memory and working-with-memory: A component process model based on modules and central systems. Journal of Cognitive Neuroscience 4: 257–267.
Moscovitch, M., Kapur, S., Köhler, S., and Houle, S. (1995). Distinct neural correlates of visual long-term memory for spatial location and object identity: A positron emission tomography study in humans. Proceedings of the National Academy of Sciences of the United States of America 92: 3721–3725.
Newcombe, F., Ratcliff, G., and Damasio, H. (1987). Dissociable visual and spatial impairments following right posterior cerebral lesions: Clinical, neuropsychological and anatomical evidence. Neuropsychologia 25: 149–161.
Nyberg, L., Tulving, E., Habib, R., Nilsson, L., Kapur, S., Houle, S., Cabeza, R., and McIntosh, A. R. (1995). Functional brain maps of retrieval mode and recovery of episodic information. Neuroreport 7: 249–252.
Okada, Y. C., and Salenius, S. (1998). Roles of attention, memory and motor preparation in modulating human brain activity in a spatial working memory task. Cerebral Cortex 8: 80–96.
O'Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map, Clarendon Press, Oxford.
Olton, D. S., Becker, J. T., and Handelmann, G. E. (1979). Hippocampus, space, and memory. Behavioral and Brain Sciences 2: 313–365.
Owen, A. M. (1997). The functional organization of working memory processes within human lateral frontal cortex: The contribution of functional neuroimaging. European Journal of Neuroscience 9: 1329–1339.
Owen, A. M., Beksinska, M., James, M., and Leigh, P. N. (1993). Visuospatial deficits at different stages of Parkinson's disease. Neuropsychologia 31: 627–644.
Owen, A. M., Downes, J. J., Sahakia, B. J., Polkey, C. E., and Robbins, T. W. (1990). Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia 28: 1021–1034.
Owen, A. M., Doyon, J., Petrides, M., and Evans, A. C. (1996a). Planning and spatial working memory: A positron emission tomography study in humans. European Journal of Neuroscience 8: 353–364.
Owen, A. M., Evans, A. C., and Petrides, M. (1996b). Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: A positron emission tomography study. Cerebral Cortex 6: 31–38.
Owen, A. M., Herrod, N. J., Menon, D. K., Clark, J. C., Downey, S. P. M. J., Carpenter, T. A., Minhas, P. S., Turkheimer, F. E., Williams, E. J., Robbins, T. W., Sahakian, B. J., Petrides, M., and Pickard, J. D. (1999). Redefining the functional organization of working memoru processes within human lateral prefrontal cortex. European Journal of Neuroscience 11: 567–574.
Owen, A. M., Milner, B., Petrides, M., and Evans, A. C. (1996c). A specific role for the right parahippocampal gyrus in the retrieval of object-location: A positron emission tomography study. Journal of Cognitive Neuroscience 8: 588–602.
Owen, A. M., Milner, B., Petrides, M., and Evans, A. C. (1996d). Memory for object features versus memory for object location: A positronemission tomography study of encoding and retrieval processes. Proceedings of the National Academy of Sciences of the United States of America 93: 9212–9217.
Owen, A. M., Morris, R. G., Sahakian, B. J., Polkey, C. E., and Robbins, T. W. (1996e). Double dissociation of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Brain 119: 1597–1615.
Owen, A. M., Sahakian, B. J., Semple, J., and Polkey, C. E. (1995). Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalohippocampectomy in man. Neuropsychologia 33: 1–24.
Owen, A. M., Stern, C. E., Look, R. B., Tracey, I., Rosen, B. R., and Petrides, M. (1998). Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. Proceedings of the National Academy of Sciences of the United States of America 95: 7721–7726.
Pantelis, C., Barnes, T. R., Nelson, H. E., Tanner, S., Weatherly, L., Owen, A. M., and Robbins, T. W. (1997). Frontal-striatal cognitive deficits in patients with chronic schizophrenia. Brain 120: 1823–1843.
Petit, L., Courtney, S. M., Ungerleider, L. G., and Haxby, J. V. (1998). Sustained activity in the medial wall during working memory delays. Journal of Neuroscience 18: 9429–9437.
Petrides, M. (1994). Frontal lobes and behavior. Current Opinion in Neurobiology 4: 207–211.
Petrides, M. (1995). Functional organization of the human frontal cortex for mnemonic processing. Annals of the New York Academy of Sciences 769: 85–96.
Petrides, M., Alivisatos, B., Evans, A. C., and Meyer, E. (1993). Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. Proceedings of the National Academy of Sciences of the United States of America 90: 873–877.
Petrides, M., and Milner, B. (1982). Deficits on subject-ordered tasks after frontal-and temporal-lobe lesions in man. Neuropsychologia 20: 249–262.
Pillon, B., Deweer, B., Vidailhet, M., Bonnet, A. M., Hahn-Barma, V., and Dubois, B. (1998). Is impaired memory for spatial location in Parkinson's disease domain specific or dependant on 'strategic' processes? Neuropsychologia 36: 1–9.
Pillon, B., Ertle, S., Deweer, B., and Bonnet, A. M. (1997). Memory for spatial location in “de novo” Parkinsonian patients. Neuropsychologia 35: 221–228.
Postle, B. R., and D'Esposito, M. (1999a). “What”-then-“where” in visual working memory: An event-related fMRI study. Journal of Cognitive Brain Research 11: 585–597.
Postle, B. R., and D'Esposito, M. (1999b). Dissociation of human caudate nucleus activity in spatial and nonspatial working memory: An event-related fMRI study. Cognitive Brain Research 8: 107–115.
Postma, A., and De Haan, E. H. F. (1996). What was where? Memory for object locations. Quarterly Journal of Experimental Psychology 49A: 178–199.
Postma, A., Izendoorn, R., and De Haan, E. H. F. (1998). Sex differences in object location memory. Brain and Cognition 36: 334–345.
Prabhakan, V., Narayanan, K., and Gabrieli, J. D. E. (2000). Integration of diverse information in working memory within the frontal lobe. Nature Neuroscience 3: 85–90.
Räma, P., Kesseli, K., Reinikainen, K., Kekoni, J., Hämäläinen, H., and Carlson, S. (1997). Visuospatial mnemonic load modulates eventrelated slow potentials. Neuroreport 8: 871–876.
Ramsey, N. F., Kirkby, B. S., Van Gelderen, P., Berman, K. F., Duyn, J. H., Frank, J. A., Mattay, V. S., Van Horn, J. D., Esposito, G., Moonen, C. T. W., and Weinberger, D. R. (1996). Functional mapping of human sensorimotor cortex with 3D BOLD fMRI correlates high with H2 15O PET rCBF. Journal of Cerebral Blood Flow and Metabolism 16: 755–764.
Rao, S. C., Rainer, G., and Miller, E. K. (1997). Integration of what and where in the primate prefrontal cortex. Science 276: 821–824.
Robbins, T. W. (1996). Dissociating executive functions of the prefrontal cortex. Philosophical Transactions of the Royal Society of London 351B: 1463–1471.
Roberts, A. C. (1996). Comparison of cognitive function in human and non-human primates. Cognitive Brain Research 3: 319–327.
Rösler, F., Heil, M., and Hennighausen, E. (1995). Exploring memory function by means of brain electrical topography: A review. Brain Topography 7: 301–313.
Ruchkin, D. S., Johnson Jr., R., Grafman, J., Canoune, H., and Ritter, W. (1992). Distinctions and similarities among working memory processes: An event-related potential study. Cognitive Brain Research 1: 53–66.
Schacter, D. L. (1987). Memory, amnesia, and frontal lobe dysfunction. Psychobiology 15: 21–36.
Schacter, D. L., and Nadel, L. (1991). Varieties of spatial memory: A problem for cognitive neuroscience. In Lister, R. G., and Weingartner, H. J. (eds.), Perspectives on Cognitive Neuroscience, Oxford University Press, New York, pp. 165–185.
Shallice, T., Fletcher, P., Frith, C. D., Grasby, P., Frackowiak, R. S. J., and Dolan, R. J. (1994). Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature 3668: 633–635.
Smith, E. E., and Jonides, J. (1997). Working memory: A view from neuroimaging. Cognitive Psychology 33: 5–42.
Smith, E. E., and Jonides, J. (1999). Storage and executive processes in the frontal lobes. Science 283: 1657–1661.
Smith, E. E., Jonides, J., and Koeppe, R. A. (1996). Dissociating verbal and spatial working memory using PET. Cerebral Cortex 6: 11–20.
Smith, M. L., Leonard, G., Crane, J., and Milner, B. (1995). The effects of frontal-or temporal-lobe lesions on susceptibility to interference in spatial memory. Neuropsychologia 33: 275–285.
Smith, M. L., and Milner, B. (1984). Differential effects of frontal lobelesions on cognitive estimation and spatial memory. Neuropsychologia 22: 697–705.
Smyth, M. M., and Scholey, K. A. (1996). Serial order in spatial immediate memory. Quarterly Journal of Experimental Psychology 49A: 159–177.
Stuss, D. T., and Benson, D. F. (1987). The frontal lobes and control of cognition and memory. In Perecman, E. (ed.), The Frontal Lobes Revisited, IRBN Press, New York, pp. 141–158.
Thomas, K. M., King, S. W., Franzen, P. L., Welsh, T. F., Berkowitz, A. L., Noll, D. C., Birmaher, V., and Casey, B. J. (1999). A developmental functional MRI study of spatial working memory. Neuroimage 10: 327–338.
Ungerleider, L. G., and Mishkin, M. (1982). Two cortical visual systems. In Ingle, D. J., Goodale, M. A., and Mansfield, R. J. W. (eds.), Analysis of Visual Behavior, MIT Press, Cambridge, MA, pp. 549–586.
Vilkki, J., and Holst, P. (1989). Deficient programming in spatial learning after frontal lobe damage. Neuropsychologia 27: 971–976.
Walker, R., Husain, M., Hodgson, T. L., Harrison, J., and Kennard, C. (1998). Saccadic eye movement and working memory deficits following frontal damage to human prefrontal cortex. Neuropsychologia 36: 1141–1159.
Wheeler, M. A., Stuss, D. T., and Tulving, E. (1997). Toward a theory of episodic memory: The frontal lobes and autonoetic consciousness. Psychological Bulletin 121: 331–354.
Wickelgren, I. (1997). Getting a grasp on working memory. Science 275: 1580–1582.
Zarahn, E., Aguirre, G. K., and D'Esposito, M. (1999). Temporal isolation of the neural correlates of spatial mnemonic processing with fMRI. Cognitive Brain Research 7: 255–268.
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Kessels, R.P.C., Postma, A., Wijnalda, E.M. et al. Frontal-Lobe Involvement in Spatial Memory: Evidence from PET, fMRI, and Lesion Studies. Neuropsychol Rev 10, 101–113 (2000). https://doi.org/10.1023/A:1009016820717
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DOI: https://doi.org/10.1023/A:1009016820717