Abstract
We review positron emission tomography (PET) studies whose results converge on the hemispheric encoding/retrieval asymmetry (HERA) model of the involvement of prefrontal cortical regions in the processes of human memory. The model holds that the left prefrontal cortex is differentially more involved in retrieval of information from semantic memory, and in simultaneously encoding novel aspects of the retrieved information into episodic memory, than is the right prefrontal cortex. The right prefrontal cortex, on the other hand, is differentially more involved in episodic memory retrieval than is the left prefrontal cortex. This general pattern holds for different kinds of information (e.g., verbal materials, pictures, faces) and a variety of conditions of encoding and retrieval.
Article PDF
Similar content being viewed by others
References
Andreasen, N. C.,Arndt, S.,Cizadlo, T.,O’Leary, D. S.,Watkins, G. L.,Boles Ponto, L. L., &Hichwa, R. D. (1995).Sample size and statistical power in [15O] H 2 O studies of human cognition. Manuscript submitted for publication.
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. (1995a).Neural substrates of face recognition. Manuscript submitted for publication.
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. (1995b). Short-term and long-term verbal memory: A positron emission tomography study.Proceedings of the National Academy of Science,92, 5111–5115.
Arndt, S., Cizadlo, T., Andreasen, N. C., Zeien, G., Harris, G., O’Leary, D. S., Watkins, G. L., Boles Ponto, L. L., &Hichwa, R. D. (1995). A comparison of approaches to the statistical analysis of [15O]H2O PET cognitive activation studies.Journal of Psychiatry,7, 155–168.
Bäckman, L.,Almkvist, O.,Andersson, J.,Nordberg, A.,Windblad, B.,Reineck, R., &Långström, B. (1995).Brain activation in young and older adults during implicit and explicit retrieval. Manuscript submitted for publication.
Baron, J. C., Petit-Taboué, M. C., Le Doze, F., Desgranges, B., Ravenel, N., &Marchal, G. (1994). Right frontal cortex hypometabolism in transient global amnesia: A PET study.Brain,117, 545–552.
Benson, D. F. (1988). Classical syndromes of aphasia. In F. Foller & J. Grafman (Eds.),Handbook of neuropsychology (Vol. 1, pp. 267–280). Amsterdam: Elsevier.
Bottini, G., Corcoran, R., Sterzi, R., Paulesu, E., Schenone, P., Scarpa, P., Frackowiak, R. S. J., &Frith, C. D. (1994). The role of the right hemisphere in the interpretation of figurative aspects of language: A positron emission tomography activation study.Brain,117, 1241–1253.
Buckner, R. (1996). Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval.Psychonomic Bulletin & Review,3, 149–158.
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., &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.
Butters, N., &Stuss, D. T. (1989). Diencephalic amnesia. In F. Boller & J. Grafman (Eds.),Handbook of neuropsychology (Vol. 3, pp. 107–148). Amsterdam: Elsevier.
Cabeza, R.,Kapur, S.,Craik, F. I. M.,McIntosh, A. R.,Houle, S., &Tulving, E. (in press). Functional neuroanatomy of recall and recognition: A PET study of episodic memory.Journal of Cognitive Neuroscience.
Cabeza, R.,Tulving, E.,Kapur, S.,McIntosh, A. R.,Jennings, J. M.,Nyberg, L.,Houle, S. ,Craik, F. I. M. (1995).Age-related decreases and increases in brain activity during encoding, recall, and recognition. Manuscript in preparation.
Craik, F. I. M., &Jennings, J. M. (1992). Human memory. In F. I. M. Craik & T. A. Salthouse (Eds.),Handbook of aging and cognition (pp. 51–110). Hillsdale, NJ: Erlbaum.
Craik, F. I. M., &Lockhart, R. S. (1972). Levels of processing: A framework for memory research.Journal of Verbal Learning & Verbal Behavior,11, 671–684.
Craik, F. I. M., &Tulving, E. (1975). Depth of processing and the retention of words in episodic memory.Journal of Experimental Psychology: General,104, 268–294.
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.
Démonet, J.-F., Chollet, F., Ramsay, S., Cardebat, D., Nespoulous, J.-L., Wise, R., Rascol, A., &Frackowiak, R. S. J. (1992). The anatomy of phonological and semantic processing in normal subjects.Brain,115, 1753–1768.
Démonet, J.-F., Wise, R., &Frackowiak, R. S. J. (1993). Language functions explored in normal subjects by positron emission tomography: A critical review.Human Brain Mapping,1, 30–47.
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.
Fox, P. T. (1991). Physiological ROI definition by image subtraction.Journal of Cerebral Blood Flow & Metabolism,11, A79-A82.
Fox, P. T., Mintun, M. A., Reiman, E. M., &Raichle, M. E. (1988). Enhanced detection of focal brain responses using intersubject averaging and change-distributed analysis of subtracted PET images.Journal of Cerebral Blood Flow & Metabolism,8, 642–653.
Frackowiak, R. S. J. (1994). Functional mapping of verbal memory and language.Trends in Neurosciences,17, 109–115.
Frackowiak, R. S. J., &Friston, K. J. (1994). Functional neuroanatomy of the human brain: Positron emission tomography—a new neuroanatomical technique.Journal of Anatomy,184, 211–225.
Friston, K. J., Frith, C. D., Liddle, P. F., &Frackowiak, R. S. J. (1991). Comparing functional (PET) images: The assessment of significant change.Journal of Cerebral Blood Flow & Metabolism,11, 690–699.
Friston, K. J., Frith, C. D., Liddle, P. F., &Frackowiak, R. S. J. (1993). Functional connectivity: The principal-component analysis of large (PET) data sets.Journal of Cerebral Blood Flow & Metabolism,13, 5–14.
Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J.-P., Frith, C. D., &Frackowiak, R. S. J. (1995). Statistical parametric maps in functional imaging: A general linear approach.Human Brain Mapping,2, 189–210.
Frith, C. D., Friston, K. J., Liddle, P. F., &Frackowiak, R. S. J. (1991a). A PET study of word finding.Neuropsychologia,29, 1137–1148.
Frith, C. D., Friston, K. J., Liddle, P. F., &Frackowiak, R. S. J. (1991b). Willed action and the prefrontal cortex in man: A study with PET.Proceedings of the Royal Society of London: Series B,244, 241–246.
Geschwind, N. (1972). Language and the brain.Scientific American,226, 76–83.
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.
Grasby, P. M., Frith, C. D., Friston, K. J., Bench, C., Frackowiak, R. S. J., &Dolan, R. J. (1993). Functional mapping of brain areas implicated in auditory-verbal memory function.Brain,116, 1–20.
Grasby, P. M., Frith, C. D., Friston, K. J., Simpson, J., Fletcher, P. C., Frackowiak, R. S. J., &Dolan, R. J. (1994). A graded task approach to the functional mapping of brain areas implicated in auditory-verbal memory.Brain,117, 1271–1282.
Haxby, J. V., Horwitz, B., Maisog, J. M., Ungerleider, L. G., Mishkin, M., Schapiro, M. B., Rapoport, S. I., &Grady, C. L. (1993). Frontal and temporal participation in long-term recognition memory for faces: A PET-rCBF activation study.Journal of Cerebral Blood Flow & Metabolism,13 (Suppl. 1), 499.
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.
Hyde, T. S., &Jenkins, J. J. (1969). Differential effects of incidental tasks on the organization of recall of a list of highly associated words.Journal of Experimental Psychology,83, 472–481.
Jenkins, I. H., Brooks, D. J., Nixon, P. D., Frackowiak, R. S. J., &Passingham, R. E. (1994). Motor sequence learning: A study with positron emission tomography.Journal of Neuroscience,14, 3775–3790.
Jones-Gottman, M., Zatorre, R. J., Evans, A. C., &Meyer, E. (1993). Functional activation of right hippocampus during an olfactory recognition memory.Society for Neuroscience Abstracts,19, 1002.
Jonides, J., Smith, E. E., Koeppe, R. A., Awh, E., Minoshima, S., &Mintun, M. A. (1993). Spatial working memory in humans as revealed by PET.Nature,363, 623–625.
Kapur, N., Friston, K. J., Young, A., Frith, C. D., &Frackowiak, R. S. J. (1995). Activation of human hippocampal formation during memory for faces: A PET study.Cortex,31, 99–108.
Kapur, S., Craik, F. I. M., Jones, C., Brown, G. M., Houle, S., &Tulving, E. (1995). Functional role of the prefrontal cortex in memory retrieval: A PET study.Neuroreport,6, 1880–1884.
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.
Kapur, S., Rose, R., Liddle, P. F., Zipursky, R. B., Brown, G. M., Stuss, D., Houle, S., &Tulving, E. (1994). The role of left prefrontal cortex in verbal processing: Semantic processing or willed action?Neuroreport,5, 2193–2196.
Kapur, S.,Tulving, E.,Cabeza, R.,McIntosh, A. R.,Houle, S., &Craik, F. I. M., (1996).The neural correlates of intentional learning of verbal materials: A PET study in humans. Manuscript in preparation.
Kinsbourne, M., &George, J. (1974). The mechanism of the wordfrequency effect on recognition memory.Journal of Verbal Learning & Verbal Behavior,13, 63–69.
Knight, R. T. (1984). Decreased response to novel stimuli after prefrontal lesions in man.Electroencephalography & Clinical Neurophysiology,59, 9–20.
Knight, R. T. (in press). Distributed cortical network for visual stimulus detection.Journal of Cognitive Neuroscience.
Köhler, S., Kapur, S., Moscovitch, M., Winocur, G., &Houle, S. (1995). Dissociation of pathways for object and spatial vision in the intact human brain.Neuroreport,6, 1865–1868.
Kosslyn, S. M., Nathaniel, M. A., Thompson, W. L., Chabris, C. F., Rauch, S. L., &Anderson, A. K. (1994). Identifying objects seen from different viewpoints: A PET investigation.Brain,117, 1055–1071.
Lockhart, R. S., &Craik, F. I. M. (1990). Levels of processing: A retrospective commentary on a framework for memory research.Canadian Journal of Psychology,44, 87–112.
Lockhart, R. S., Craik, F. I. M., &Jacoby, L. L. (1976). Depth of processing, recognition and recall. In J. Brown (Ed.),Recall and recognition (pp. 75–102). New York: Wiley.
Markowitsch, H. J. (1995). Anatomical basis of memory disorders. In M. S. Gazzaniga (Ed.),The cognitive neurosciences (pp. 765–779). Cambridge, MA: MIT Press.
Markowitsch, H. J., &Pritzel, M. (1985). The neuropathology of amnesia.Progress in Neurobiology,25, 189–287.
Markowitsch, H. J., &Tulving, E. (1994a). Cognitive processes and cerebral cortical fundi: Findings from positron-emission tomography studies.Proceedings of the National Academy of Science,91, 10507–10511.
Markowitsch, H. J., &Tulving, E. (1994b). Cognitive processing in cerebral cortical sulci.Neuroreport,6, 413–418.
McIntosh, A. R., &Gonzalez-Lima, F. (1994). Structural equation modeling and its application to network analysis in functional brain imaging.Human Brain Mapping,2, 2–22.
Mesulam, M.-M. (1990). Large-scale neurocognitive networks and distributed processing for attention, language, and memory.Annals of Neurology,28, 597–613.
Molchan, S. E., Sunderland, T., McIntosh, A. R., Herscovitch, P., &Schreurs, B. G. (1994). A functional anatomical study of associative learning in humans.Proceedings of the National Academy of Science,91, 8122–8126.
Moscovitch, M., Kapur, S., Köhler, S., &Houle, S. (1995). Distinct neural correlates of visual long-term memory for spatial location and object identity: A positron emission tomography (PET) study in humans.Proceedings of the National Academy of Science,92, 3721–3725.
Nyberg, L.,McIntosh, A. R.,Cabeza, R.,Nilsson, L.-G.,Houle, S.,Habib, R., &Tulving, E. (in press). Network analysis of PET rCBF data: Ensemble inhibition during episodic memory retrieval.Journal of Neuroscience.
Nyberg, L., Tulving, E., Habib, R., Nilsson, L.-G., Kapur, S., Houle, S., Cabeza, R., &McIntosh, A. R. (1995). Functional brain maps of retrieval mode and recovery of episodic informationNeuroreport,7, 249–252.
Owen, A. M.,Milner, B.,Petrides, M., &Evans, A. C. (in press). A specific role for the right parahippocampal gyrus in the retrieval of object-location: A positron emission tomography study.Journal of Cognitive Neuroscience.
Pardo, J. V., &Fox, P. T. (1993). Preoperative assessment of the cerebral hemispheric dominance for language with CBF PET.Human Brain Mapping,1, 57–68.
Paulesu, E., Frith, C. D., &Frackowiak, R. S. J. (1993). The neural correlates of the verbal component of working memory.Nature,362, 342–345.
Petersen, S. E., Corbetta, M., Miezin, F. M., &Shulman, G. L. (1994). PET studies of parietal involvement in spatial attention: Comparison of different task types.Canadian Journal of Experimental Psychology,48, 319–338.
Petersen, S. E., &Fiez, J. A. (1993). The processing of single words studied with positron emission tomography.Annual Review of Neuroscience,16, 509–530.
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., Snyder, A. Z., &Raichle, M. E. (1990, August 31). Activation of extrastriate and frontal cortical areas by visual words and word-like stimuli.Science,249, 1041–1044.
Petrides, M., Alivasatos, 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., Alivasatos, 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., Alivisatos, B., Meyer, E., &Evans, A. C. (1993). Functional activation of the human frontal cortex during the performance of verbal working memory tasks.Proceedings of the National Academy of Science,90, 878–882.
Posner, M. I., &Raichle, M. E. (1994).Images of mind. New York: Scientific American Books.
Price, C., Wise, R., Ransay, S., Friston, K. [J.], Howard, D., Patterson, K., &Frackowiak, R. [S. J.] (1992). Regional response differences within the human auditory cortex when listening to words.Neuroscience Letters,146, 179–182.
Raichle, M. E. (1994a). Images of the mind: Studies with modern imaging techniques.Annual Review of Psychology,45, 333–356.
Raichle, M. E. (1994b, April). Visualizing the mind.Scientific American, pp. 58–64.
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.
Roland, P. E. (1982). Cortical regulation of selective attention in man: A regional cerebral blood flow study.Journal of Neurophysiology,48, 1059–1078.
Roland, P. E., Kawashima, R., Gulyas, B., &O’Sullivan, B. (1995). Positron emission tomography in cognitive neuroscience: Methodological constraints, strategies, and examples from learning and memory. In M. S. Gazzaniga (Ed.),The cognitive neurosciences (pp. 781–788). Cambridge, MA: MIT Press.
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., Reiman, E., Uecker, A., Polster, M. R., Yung, L. S., &Cooper, L. A. (1995). Brain regions associated with retrieval of structurally coherent visual information.Nature,368, 633–635.
Schacter, D. L.,Savage, C. R.,Alpert, N. M.,Rauch, S. L., &Albert, M. (in press). The role of the hippocampus and frontal cortex in age-related memory loss.Neuroreport.
Seitz, R., &Roland, P. (1992). Learning of sequential finger movements in man: A combined kinematic and positron emission tomography (PET) study.European Journal of Neuroscience,4, 154–165.
Sergent, J., Ohta, S., &MacDonald, B. (1992). Functional neuroanatomy of face and object processing.Brain,115, 15–36.
Shallice, T., Fletcher, P., Frith, C. D., Grasby, P., Frackowiak, R. S. J., &Dolan, R. J. (1994). Brain regions associated with acquisition and retrieval of verbal episodic memory.Nature,368, 633–635.
Snodgrass, J. G., &Vanderwart, M. A. (1980). A standardized set of 260 pictures: Norms for name agreement, image agreement, familiarity, and visual complexity.Journal of Experimental Psychology: Human Learning & Memory,6, 174–215.
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.
Squire, L. R., &Zola-Morgan, S. (1991, September 20). The medial temporal lobe memory system.Science,253, 1380–1386.
Steinmetz, H., &Seitz, R. J. (1991). Functional anatomy of language processing: Neuroimaging and the problem of individual variability.Neuropsychologia,29, 1149–1161.
Stuss, D. T., &Benson, D. F. (1986).The frontal lobes. New York: Raven Press.
Talairach, J., &Tournoux, P. (1988).Co-planar steorotaxic atlas of the human brain. New York: Thieme Medical Publishers.
Tamas, L. B., Shibasaki, T., Horikoshi, S., &Ohye, C. (1993). General activation of cerebral metabolism with speech: A PET study.International Journal of Psychophysiology,14, 199–208.
Tulving, E. (1972). Episodic and semantic memory. In E. Tulving & W. Donaldson (Eds.),Organization of memory (pp. 381–403). New York: Academic Press.
Tulving, E. (1983).Elements of episodic memory. New York: Oxford University Press.
Tulving, E. (1993). What is episodic memory?Current Perspectives in Psychological Science,2, 67–70.
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.
Tulving, E., &Kroll, N. (1995). Novelty assessment in the brain and long-term memory encoding.Psychonomic Bulletin & Review,2, 387–390.
Tulving, E., Markowitsch, H. J., Craik, F. I. M., Habib, R., &Houle, S. (1996). Novelty and familiarity activations in PET studies of memory encoding and retrieval.Cerebral Cortex,6, 71–79.
Tulving, E., Markowitsch, H. J., Kapur, S., Habib, R., &Houle, S. (1994). Novelty encoding networks in the human brain: Positron emission tomography data.Neuroreport,5, 2525–2528.
Tulving, E., &Pearlstone, Z. (1966). Availability versus accessibility of information in memory for words.Journal of Verbal Learning & Verbal Behavior,5, 381–391.
Wheeler, M. A., Stuss, D. T., &Tulving, E. (1995). Frontal lobe damage produces episodic memory impairment.Journal of the International Neuropsychological Society,1, 525–536.
Wilson, F. A., &Rolls, E. T. (1993). The effects of stimulus novelty and familiarity on neuronal activity in the amygdala of monkeys performing recognition memory tasks.Experimental Brain Research,93, 367–382.
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.
Worsley, K. J., Evans, A. C., Marrett, S., &Neelin, P. (1992). A threedimensional statistical analysis for CBF activation studies in human brain.Journal of Cerebral Blood Flow & Metabolism,12, 900–918.
Author information
Authors and Affiliations
Corresponding author
Additional information
We thank John Gabrieli, Roger Ratcliff, Dan Schacter, and one anonymous reviewer for valuable comments. We also thank Randy Buckner, Paul Fletcher, Narinder Kapur, and Stefan Köhler for assistance.
Rights and permissions
About this article
Cite this article
Nyberg, L., Cabeza, R. & Tulving, E. PET studies of encoding and retrieval: The HERA model. Psychonomic Bulletin & Review 3, 135–148 (1996). https://doi.org/10.3758/BF03212412
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.3758/BF03212412