Abstract
Recent neuroimaging studies have provided a wealth of information about areas within prefrontal cortex involved in long-term memory. These studies prompted a proposal by Tulving and colleagues (Tulving, Kapur, Craik, Habib, & Houle, 1994) that prefrontal contributions to memory function are related to laterality differences (the hemispheric encoding/retrieval asymmetry model). This review goes beyond a general characterization of prefrontal lobes to a more specific analysis of distinct areas within the prefrontal cortex. Separate prefrontal areas, sometimes within the same hemisphere, are discussed in terms of selective contributions that they might make to memory retrieval. In the end, it is concluded that a framework which tries to understand prefrontal function in terms of specific areas is a useful complement to models, like HERA, which attempt to find unifying principles across multiple areas.
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Andreasen, N. C., O’Leary, D. S., Arndt, S., Cizadlo, T., Hurtig, R., Rezai, K., Watkins, G. L., Boles Ponto, L. L., &Hichwa, R. D. (1995). Short-term and long-term verbal memory: A positron emission tomography study.Proceedings of the National Academy of Science,92, 5111–5115.
Barbas, H., &Pandya, D. N. (1989). Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey.Journal of Comparative Neurology,286, 353–375.
Brodmann, K. (1994).Localisation in the cerebral cortex (L. J. Garey, Trans.) London: Smith-Gordon. (Original work published 1909)
Buckner, R. L., &Petersen, S. E. (1996). What does neuroimaging tell us about the role of prefrontal cortex in memory retrieval?Seminars in the Neurosciences,8, 47–55.
Buckner, R. L., Petersen, S. E., Ojemann, J. G., Miezin, F. M., Squire, L. R., &Raichle, M. E. (1995). Functional anatomical studies of explicit and implicit memory retrieval tasks.Journal of Neuroscience,15, 12–29.
Buckner, R. L., Raichle, M. E., Miezin, F. M., &Petersen, S. E. (1995). PET studies of the recall of pictures and words from memory.Society for Neuroscience Abstracts,21, 1441.
Buckner, R. L., Raichle, M. E., &Petersen, S. E. (1995). Activation of human prefrontal cortex across different speech production tasks and gender groups.Journal of Neurophysiology,74, 2163–2173.
Buckner, R. L., &Tulving, E. (1995). Neuroimaging studies of memory: Theory and recent PET results. In F. Boller & J. Grafman (Eds.),Handbook of neuropsychology (Vol. 10, pp. 439–466). Amsterdam: Elsevier.
Carmichael, S. T., &Price, J. L. (1994). Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey.Journal of Comparative Neurology,346, 366–402.
Courtney, S. M.,Ungerleider, L. G.,Keil, K., &Haxby, J. V. (in press). Object and spatial visual working memory activate separate neural systems in human cortex.Cerebral Cortex.
Demb, J. B., Desmond, J. E., Wagner, A. D., Vaidya, C. J., Glover, G. H., &Gabrieli, J. D. E. (1995). Semantic encoding and retrieval in the left inferior prefrontal cortex: A functional MRI study of task difficulty and process specificity.Journal of Neuroscience,15, 5870–5878.
DeYoe, E. A., Bandettini, P., Neitz, J., Miller, D., &Winans, P. (1994). Functional magnetic resonance imaging (fMRI) of the human brain.Journal of Neuroscience Methods,54, 171–187.
Fiez, J. A., Damasio, H., &Tranel, D. (1995). The left frontal operculam in phonological processing: Converging evidence from PET and the lesion method.Society for Neuroscience Abstracts,21, 1763.
Fiez, J. A., Raife, E. A., Balota, D., Schwarz, J. P., Raichle, M. E., &Petersen, S. E. (1996). A positron emission tomography study of the short-term maintenance of verbal information.Journal of Neuroscience,16, 808–822.
Fletcher, P. C., Frith, C. D., Grasby, P. M., Shallice, T., Frackowiak, R. S. J., &Dolan, R. J. (1995). Brain systems for encoding and retrieval of auditory-verbal memory: An in vivo study in humans.Brain,118, 401–416.
Frith, C. D., Friston, K. J., Liddle, P. F., &Frackowiak, R. S. J. (1991). Willed action and the prefrontal cortex in man: A study with PET.Proceedings of the Royal Society of London: Series B,244, 241–246.
Fuster, J. M. (1989).The prefrontal cortex. New York: Raven Press.
Goldman-Rakic, P. S. (1987). Circuitry of primate prefrontal cortex and regulation of behavior by representational memory In F. Plum & V. Mountcastle (Eds.),The handbook of physiology: Section 1. The nervous system: Vol. V. Higher functions of the brain: Pt. 1 (pp. 373–417). Bethesda, MD: American Physiological Society.
Grady, C. L., Maisog, J. M., Horwitz, B., Ungerleider, L. G., Mentis, M. J., Salerno, J. A., Pietrini, P., Wagner, E., &Haxby, J. V. (1994). Age-related changes in cortical blood flow activation during visual processing of faces and locations.Journal of Neuroscience,14, 1450–1462.
Grady, C. L., McIntosh, A. R., Horwitz, B., Maisog, J. M., Ungerleider, L. G., Mentis, M. J., Pietrini, P., Schapiro, M. B., &Haxby, J. V. (1995, July 14). Age-related reductions in human recognition memory due to impaired encoding.Science,269, 218–221.
Haxby, J. V., Horwitz, B., Ungerleider, L. G., Maisog, J. M., Pietrini, P., &Grady, C. L. (1994). The functional organization of human extrastriate cortex: A PET-rCBF study of selective attention to faces and locations.Journal of Neuroscience,14, 6336–6353.
Haxby, J. V., Ungerleider, L. G., Horwitz, B., Maisog, J. M., Rapoport, S. L., &Grady, C. L. (1996). Face encoding and recognition in the human brain.Proceedings of the National Academy of Science,93, 922–927.
Kapur, S., Craik, F. I. M., Tulving, E., Wilson, A. A., Houle, S., &Brown, G. M. (1994). Neuroanatomical correlates of encoding in episodic memory: Levels of processing effect.Proceedings of the National Academy of Science,91, 2008–2011.
Klein, D., Milner, B., Zatorre, R. J., Meyer, E., &Evans, A. C. (1995). The neural substrates underlying word generation: A bilingual functional-imaging study.Proceedings of the National Academy of Science,92, 2899–2903.
Martin, A., Haxby, J. V., Lalonde, F. M., Wiggs, C. L., &Ungerleider, L. G. (1995, October 6). Discrete cortical regions associated with knowledge of color and knowledge of action.Science,270, 102–105.
Milner, B., Petrides, M., &Smith, M. L. (1985). Frontal lobes and the temporal organization of memory.Human Neurobiology,4, 137–142.
Moscovitch, M. (1982). Multiple dissociations of function in amnesia. In L. S. Cermak (Ed.),Human memory and amnesia (pp. 337–370). Hillsdale, NJ: Erlbaum.
Moscovitch, M. (1989). Confabulation and the frontal systems: Strategic versus associated retrieval in neuropsychological theories of memory. In H. L. Roediger III & F. I. M. Craik (Eds.),Varieties of memory and consciousness: Essays in honour of Endel Tulving (pp. 133–155). Hillsdale, NJ: Erlbaum.
Nyberg, L., Cabeza, R., &Tulving, E. (1996). PET studies of encoding and retrieval: The HERA model.Psychonomic Bulletin & Review,3, 135–148.
Petersen, S. E., Fox, P. T., Posner, M. I., Mintun, M. [A.], &Raichle, M. E. (1988). Positron emission tomographic studies of the cortical anatomy of single-word processing.Nature,331, 585–589.
Petersen, S. E., Fox, P. T., Posner, M. I., Mintun, M. [A.], &Raichle, M. E. (1989). Positron emission tomographic studies of the processing of single words.Journal of Cognitive Neuroscience,1, 153–170.
Petrides, M., Alivisatos, B., &Evans, A. C. (1995). Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information.Proceedings of the National Academy of Science,92, 5803–5807.
Petrides, M., Alivisatos, B., Evans, A. C., &Meyer, E. (1993). Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing.Proceedings of the National Academy of Science,90, 873–877.
Petrides, M., &Pandya, D. N. (1994). Comparative architectonic analysis of the human and the macaque frontal cortex. In F. Boller & J. Grafman (Eds.),Handbook of neuropsychology (Vol. 9, pp. 17–58). Amsterdam: Elsevier.
Posner, M. I., &Raichle, M. E. (1994).Images of mind. New York: Scientific American Books.
Preuss, T. M., &Goldman-Rakic, P. S. (1991). Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhineGalago and the anthropoid primateMacaca.Journal of Comparative Neurology,310, 429–474.
Raichle, M. E. (1987). Circulatory and metabolic correlates of brain function in normal humans. In F. Plum & V. Mountcastle (Eds.),The handbook of physiology: Section 1. The nervous system: Vol. V. Higher functions of the brain: Pt. 1 (pp. 643–674). Bethesda, MD: American Physiological Association.
Raichle, M. E., Fiez, J. A., Videen, T. O., MacLeod, A.-M. K., Pardo, J. V., Fox, P. T., &Petersen, S. E. (1994). Practice-related changes in human brain functional anatomy during nonmotor learning.Cerebral Cortex,4, 8–26.
Rajkowska, G., &Goldman-Rakic, P. S. (1995a). Cytoarchitectonic definition of prefrontal areas in normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria.Cerebral Cortex,5, 307–322.
Rajkowska, G., &Goldman-Rakic, P. S. (1995b). Cytoarchitectonic definition of prefrontal areas in normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach coordinate system.Cerebral Cortex,5, 323–337.
Schacter, D. L. (1987). Memory, amnesia, and frontal lobe dysfunction.Psychobiology,15, 21–36.
Schacter, D. L., Alpert, N. M., Savage, C. R., Rauch, S. L., &Albert, M. S. (1996). Conscious recollection and the human hippocampal formation: Evidence from positron emission tomography.Proceedings of the National Academy of Science,93, 321–325.
Schacter, D. L., &Tulving, E. (Eds.) (1994).Memory systems 1994. Cambridge, MA: MIT Press.
Shimamura, A. P., Janowsky, J. S., &Squire, L. R. (1991). What is the role of frontal lobe damage in memory disorders? In H. Levin, H. M. Eisenberg, & A. L. Benton (Eds.),Frontal lobe function and dysfunction (pp. 173–198). New York: Oxford University Press.
Squire, L. R., Ojemann, J. G., Miezin, F. M., Petersen, S. E., Videen, T. O., &Raichle, M. E. (1992). Activation of the hippocampus in normal humans: A functional anatomical study of memory.Proceedings of the National Academy of Science,89, 1837–1841.
Swick, D., &Knight, R. T. (in press). Is prefrontal cortex involved in cued recall? A neuropsychological test of PET findings.Neuropsychologia.
Talairach, J., &Tournoux, P. (1988).Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical Publishers.
Tulving, E. (1983).Elements of episodic memory. New York: Oxford University Press.
Tulving, E., Kapur, S., Craik, F. I. M., Moscovitch, M., &Houle, S. (1994). Hemispheric encoding/retrieval asymmetry in episodic memory: Positron emission tomography findings.Proceedings of the National Academy of Science,91, 2016–2020.
Tulving, E., Kapur, S., Markowitsch, H. J., Craik, F. I. M., Habib, R., &Houle, S. (1994). Neuroanatomical correlates of retrieval in episodic memory: Auditory sentence recognition.Proceedings of the National Academy of Science,91, 2012–2015.
Wise, R., Chollet, F., Hadar, U., Friston, K. [J.], Hoffner, E., &Frackowiak, R. [S. J.] (1991). Distribution of cortical neural networks involved in word comprehension and word retrieval.Brain,114, 1803–1817.
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I thank Steve Petersen, Julie Fiez, Adina Roskies, and Susan Courtney for helpful comments on various versions of this manuscript and Dan Schacter, Roger Ratcliff, John Gabrieli, Henry Roediger, and an anonymous reviewer for thoughtful comments during the review process. Support was provided by NIH Grant NS32979 and grants from the Charles A. Dana Foundation and the McDonnell Center for Higher Brain Function. The present research was conducted at Washington University School of Medicine, Department of Neurology and Neurological Surgery.
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Buckner, R.L. Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval. Psychonomic Bulletin & Review 3, 149–158 (1996). https://doi.org/10.3758/BF03212413
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DOI: https://doi.org/10.3758/BF03212413