Hostname: page-component-7dd5485656-bt4hw Total loading time: 0 Render date: 2025-10-31T02:28:32.106Z Has data issue: false hasContentIssue false
  • English
  • Français

Neural substrates of semantic memory

Published online by Cambridge University Press:  14 August 2007

JOHN HART ,
RAKSHA ANAND ,
SANDRA ZOCCOLI ,
MANDY MAGUIRE ,
JACQUE GAMINO ,
GAIL TILLMAN ,
RICHARD KING  and
MICHAEL A. KRAUT
JOHN HART
Affiliation:
Center for BrainHealth, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Texas Department of Neurology, University of Texas Southwestern Medical Center, Dallas, Texas
RAKSHA ANAND
Affiliation:
Center for BrainHealth, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Texas
SANDRA ZOCCOLI
Affiliation:
Department of Psychology, Southern Methodist University, Dallas, Texas
MANDY MAGUIRE
Affiliation:
Center for BrainHealth, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Texas
JACQUE GAMINO
Affiliation:
Center for BrainHealth, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Texas
GAIL TILLMAN
Affiliation:
Center for BrainHealth, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Texas
RICHARD KING
Affiliation:
Center for BrainHealth, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Texas Department of Neurology, University of Texas Southwestern Medical Center, Dallas, Texas
MICHAEL A. KRAUT
Affiliation:
Center for BrainHealth, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Texas Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, Maryland
Get access Rights & Permissions [Opens in a new window]

Abstract

Semantic memory is described as the storage of knowledge, concepts, and information that is common and relatively consistent across individuals (e.g., memory of what is a cup). These memories are stored in multiple sensorimotor modalities and cognitive systems throughout the brain (e.g., how a cup is held and manipulated, the texture of a cup's surface, its shape, its function, that is related to beverages such as coffee, and so on). Our ability to engage in purposeful interactions with our environment is dependent on the ability to understand the meaning and significance of the objects and actions around us that are stored in semantic memory. Theories of the neural basis of the semantic memory of objects have produced sophisticated models that have incorporated to varying degrees the results of cognitive and neural investigations. The models are grouped into those that are (1) cognitive models, where the neural data are used to reveal dissociations in semantic memory after a brain lesion occurs; (2) models that incorporate both cognitive and neuroanatomical information; and (3) models that use cognitive, neuroanatomic, and neurophysiological data. This review highlights the advances and issues that have emerged from these models and points to future directions that provide opportunities to extend these models. The models of object memory generally describe how category and/or feature representations encode for object memory, and the semantic operations engaged in object processing. The incorporation of data derived from multiple modalities of investigation can lead to detailed neural specifications of semantic memory organization. The addition of neurophysiological data can potentially provide further elaboration of models to include semantic neural mechanisms. Future directions should incorporate available and newly developed techniques to better inform the neural underpinning of semantic memory models. (JINS, 2007, 13, 865–880.)

Keywords

SemanticMemoryLexical–semanticMeaningConceptualFunctional MRI

Information

Type
CRITICAL REVIEW
Information
Journal of the International Neuropsychological Society , Volume 13 , Issue 5 , September 2007 , pp. 865 - 880
Copyright
2007 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

Albanese, E., Capitani, E., Barbarotto, R., & Laiacona M. (2000). Semantic category dissociations, familiarity and gender. Cortex, 36, 733–746.Google Scholar
Barbarotto, R., Laiacona, M., Macchi, V., & Capitani E. (2002). Picture reality decision, semantic categories and gender. A new set of pictures, with norms and an experimental study. Neuropsychologia, 40, 1637–1653.Google Scholar
Barsalou, L.W., Kyle Simmons, W., Barbey, A.K., & Wilson, C.D. (2003). Grounding conceptual knowledge in modality-specific systems. Trends in Cognitive Science, 7, 84–91.Google Scholar
Beauchamp, M.S., Lee, K.E., Argall, B.D., & Martin, A. (2004). Integration of auditory and visual information about objects in superior temporal sulcus. Neuron, 41, 809–823.Google Scholar
Capitani, E., Laiacona, M., & Barbarotto, R. (1999). Gender affects word retrieval of certain categories in semantic fluency tasks. Cortex, 35, 273–278.Google Scholar
Capitani, E., Laiacona, M., Mohan, B., & Caramazza, A. (2003). What are the facts of semantic category-specific deficits? A critical review of the clinical evidence. Cognitive Neuropsychology, 20, 213–261.Google Scholar
Caramazza, A., Hillis, A., & Rapp, B. (1990). The multiple semantics hypothesis: Multiple confusions? Cognitive Neuropsychology, 7, 161–189.Google Scholar
Caramazza, A. & Shelton, J.R. (1998). Domain-specific knowledge systems in the brain the animate-inanimate distinction. Journal of Cognitive Neuroscience, 10, 1–34.Google Scholar
Cohen, L., Dehaene, S., Naccache, L., Lehericy, S., Dehaene-Lambertz, G., Henaff, M.A., & Michel, F. (2000). The visual word form area—Spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain, 123, 291–307.Google Scholar
Crosson, B., Benjamin, M., & Levy, I. (2007). Role of the basal ganglia in language and semantics: Supporting cast. In J. Hart & M. Kraut (Eds.), Neural basis of semantic memory. London: Cambridge University Press.
Crosson, B., Moberg, P.J., Boone, J.R., Rothi, L.J.G., & Raymer, A.M. (1997). Category specific naming deficit for medical terms after dominant thalamic/capsular hemorrhage. Brain and Language, 60, 407–442.Google Scholar
Crutch, S.J. & Warrington, E.K. (2003). The selective impairment of fruit and vegetable knowledge: A multiple processing channels account of fine-grain category specificity. Cognitive Neuropsychology, 20, 355–372.Google Scholar
Damasio, A.R. (1989). Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition. Cognition, 33, 25–62.Google Scholar
Damasio, A.R. & Tranel, D. (1993). Nouns and verbs are retrieved with differently distributed neural systems. Proceedings of the National Academy of Sciences United States of America, 90, 4957–4960.Google Scholar
Freese, J.L. & Amaral, D.G. (2005). The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey. Journal of Comparative Neurology, 486, 295–317.Google Scholar
Gainotti, G. (1990). The categorical organization of semantic and lexical knowledge in the brain. Behavioural Neurology, 3, 109–115.Google Scholar
Gainotti, G. (2000). What the locus of brain lesion tells us about the nature of the cognitive defect underlying category-specific disorders: A review. Cortex, 36, 539–559.Google Scholar
Gainotti, G. & Silveri, M.C. (1996). Cognitive and anatomical locus of lesion in a patient with category specific semantic impairment for living beings. Cognitive Neuropsychology, 13, 357–389.Google Scholar
Gainotti, G., Silveri, M., Daniele, A., & Giustolisi, L. (1995). Neuroanatomical correlates of category-specific semantic disorders: A critical survey. Memory, 3, 247–264.Google Scholar
Garrard, P., Lambon Ralph, M., Patterson, K., Pratt, J., & Hodges, J. (2005). Semantic feature knowledge and picture naming in dementia of Alzheimer's type: A new approach. Brain and Language, 93, 79–94.Google Scholar
Gil-da-Costa, R., Martin, A., Lopes, M., Munoz, M., Fritz, J.B., & Braun, A.R. (2006). Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque. Nature Neuroscience, 9, 1064–1070.Google Scholar
Gotts, S.J. & Plaut, D.C. (2002). The impact of synaptic depression following brain damage: A connectionist account of “access/refractory” and “degraded store” semantic impairments. Cognitive, Affective & Behavioral Neuroscience, 2, 187–213.Google Scholar
Grossman, M., Smith, E., Koenig, P., Glosser, G., Rhee, J., & Dennis, K. (2003). Categorization of object descriptions in Alzheimer's disease and frontotemporal dementia: Limitation in rule-based processing. Cognitive, Affective & Behavioral Neuroscience, 3, 120–132.Google Scholar
Gutierrez, C., Cola, M.G., Seltzer, B., & Cusick, C. (2000). Neurochemical and connectional organization of the dorsal pulvinar complex in monkeys. Journal of Comparative Neurology, 419, 61–86.Google Scholar
Hart, J. & Gordon, B. (1990). Delineation of single-word semantic comprehension deficits in aphasia, with anatomical correlation. Annals of Neurology, 27, 226–231.Google Scholar
Hart, J. & Gordon, B. (1992). Neural subsystems for object knowledge. Nature, 359, 60–64.Google Scholar
Hart, J. & Kraut, M. (Eds.) (2007). Neural basis of semantic memory. London: Cambridge University Press.
Hart, J., Moo, L., Segal, J.B., Adkins, E., & Kraut, M. (2002). Neural substrates of semantics. In A. Hillis (Ed.), Handbook of language disorders. Philadelphia: Psychology Press.
Haxby, J., Gobbini, M.I., Furey, M.L., Ishai, A., Schouten, J.L., & Pietrini, P. (2001). Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science, 293, 2405–2407.Google Scholar
Hillis, A.E., Rapp, B., Romani, C., & Caramazza, A. (1990). Selective impairment of semantics in lexical processing. Cognitive Neuropsychology, 7, 191–243.Google Scholar
Hillis, A.E., Wityk, R.J., Tuffiash, E., Beauchamp, N.J., Jacobs, M.A., Barker, P.B., & Selnes, O.A. (2001). Hypoperfusion of Wernicke's area predicts severity of semantic deficit in acute stroke. Annals of Neurology, 50, 561–566.Google Scholar
Howard, D. & Patterson, K. (1992). Pyramids and palm trees: A test of semantic access from pictures and words. Bury St Edmunds: Thames Valley Publishing Company.
Humphreys, G.W. & Forde, E.M.E. (2001). Hierarchies, similarity, and interactivity in object recognition: “Category-specific” neuropsychological deficits. Behavioral and Brain Sciences, 24, 453–509.Google Scholar
Humphreys, G.W. & Riddoch, M.J. (2003). A case series analysis of “category-specific” deficits of living things: The HIT account. Cognitive Neuropsychology, 20, 263–306.Google Scholar
Ilinsky, I.A., Jouandet, M.L., & Goldman-Rakic, P.S. (1985). Organization of the nigrothalamocortical system in the rhesus monkey. Journal of Comparative Neurology, 236, 315–330.Google Scholar
Inase, M., Tokuno, H., Nambu, A., Akazawa, T., & Takada, M. (1996). Origin of thalamocortical projections to the presupplementary motor area (pre-SMA) in the macaque. Neuroscience Research, 25, 217–227.Google Scholar
Klimesch, W. (1996). Memory processes, brain oscillations and EEG synchronization. International Journal of Psychophysiology, 24, 61–100.Google Scholar
Klimesch, W. (1999). EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis. Brain Research Brain Research Reviews, 29, 169–195.Google Scholar
Klimesch, W., Doppelmayr, M., Schwaiger, J., Auinger, P., & Winkler, T. (1999). ‘Paradoxical’ alpha synchronization in a memory task. Brain Research Cognitive Brain Research, 7, 493–501.Google Scholar
Klimesch, W., Schimke, H., & Pfurtscheller, G. (1993). Alpha frequency, cognitive load and memory performance. Brain Topography, 5, 241–251.Google Scholar
Kraut, M., Calhoun, V., Pitcock, J.A., Cusick, C., & Hart, J. (2003). Neural hybrid model of semantic object memory: Implications from event-related timing using fMRI. Journal of the International Neuropsychological Society, 9, 1031–1040.Google Scholar
Kraut, M., Cherry, B., Pitcock, J., Vestal, L., Henderson, V., & Hart, J. (2006b). The Semantic Object Retrieval Test (SORT) in normal aging and Alzheimer's disease. Cognitive and Behavioral Neurology, 19, 177–184.Google Scholar
Kraut, M.A., Kremen, S., Segal, J.B., Calhoun, V., Moo, L., & Hart, J. (2002a). Object activation from features in the semantic system. Journal of Cognitive Neuroscience, 14, 24–36.Google Scholar
Kraut, M., Moo, L., Segal, J., & Hart, J. (2002b). Neural activation during an explicit categorization task: Category- or feature-specific effects? Brain Research Cognitive Brain Research, 13, 213–220.Google Scholar
Kraut, M., Pitcock, J., Calhoun, V., Li, J., & Hart, J. (2006a). Neuroanatomic organization of sound memory in humans. Journal of Cognitive Neuroscience, 18, 1877–1888.Google Scholar
Kraut, M., Pitcock, J., & Hart, J. (2004). Neural mechanisms of semantic memory. Current Neurology and Neuroscience Reports, 4, 461–465.Google Scholar
Kreiman, G., Koch, C., & Fried, I. (2000a). Category specific visual responses of single neurons in the human medial temporal lobe. Nature Neuroscience, 3, 946–953.Google Scholar
Kreiman, G., Koch, C., & Fried, I. (2000b). Imagery neurons in the human brain. Nature, 408, 357–361.Google Scholar
Kronbichler, M., Hutzler, F., Wimmer, H., Mair, A., Staffen, W., & Ladurner, G. (2004). The visual word form area and the frequency with which words are encountered: Evidence from a parametric fMRI study. Neuroimage, 21, 946–953.Google Scholar
Mahon, B.Z. & Caramazza, A. (2003). Constraining questions about the organisation and representation of conceptual knowledge. Cognitive Neuropsychology, 20, 433–450.Google Scholar
Martin, A. (1998). Organization of semantic knowledge and the origin of words in the brain. In N.G. Jablonski & L.C. Aiello (Eds.), The origins and diversification of language (pp. 69–88). San Francisco, CA: California Academy of Sciences.
Martin, A. (2007). Neural foundations for conceptual representations: Evidence from functional brain imaging. In J. Hart & M. Kraut (Eds.), Neural basis of semantic memory. Cambridge, UK: Cambridge University Press.
Martin, A. & Chao, L.L. (2001). Semantic memory and the brain: Structure and processes. Current Opinion in Neurobiology, 11, 194–201.Google Scholar
Martin, A., Ungerleider, L.G., & Haxby, J.V. (2000). Category-specificity and the brain: The sensory-motor model of semantic representations of objects. In M.S. Gazzaniga (Ed.), The new cognitive neurosciences (pp. 1023–1036). Cambridge, MA: MIT Press.
Martin, A., Wiggs, C.L., Ungerleider, L.G., & Haxby, J.V. (1996). Neural correlates of category-specific knowledge. Nature, 379, 649–652.Google Scholar
McKenna, P. & Parry, R. (1994). Category-specificity in the naming of natural and manmade objects: Normative data from adults and children. Neuropsychological Rehabilitation, 4, 225–281.Google Scholar
Miceli, G., Fouch, E., Capasso, R., Shelton, J., Tomaiuolo, F., & Caramazza, A. (2001). The dissociation of color from form and function knowledge. Nature Neuroscience, 4, 662–667.Google Scholar
Moss, H.E., Rodd, J.M., Stamatakis, E.A., Bright, P., & Tyler, L.K. (2005). Anteromedial temporal cortex supports fine-grained differentiation among objects. Cerebral Cortex, 15, 616–627.Google Scholar
Moss, H.E., Tyler, L.K., & Devlin, J. (2002). The emergence of category specific deficits in a distributed semantic system. In E. Forde & G.W. Humphreys (Eds.), Category-specificity in brain and mind (pp. 115–148). Sussex: Psychology Press.
Polk, T.A. & Farah, M.J. (1998). The neural development and organization of letter recognition: Evidence from functional neuroimaging, computational modeling, and behavioral studies. Proceedings of the National Academy of Science United States of America, 95, 847–852.Google Scholar
Pulvermuller, F. (2005). Brain mechanisms linking language and action. Nature Reviews, Neuroscience, 6, 576–582.Google Scholar
Pulvermuller, F., Shtyrov, Y., & Ilmoniemi, R. (2005). Brain signatures of meaning access in action word recognition. Journal of Cognitive Neuroscience, 17, 884–892.Google Scholar
Rademacher, J., Morosan, P., Schormann, T., Schleicher, A., Werner, C., Freund, H.J., & Zilles, K. (2001). Probabilistic mapping and volume measurement of human primary auditory cortex. Neuroimage, 13, 669–683.Google Scholar
Rapp, B., Hillis, A., & Caramazza, A. (1993). The role of representations in cognitive theory: More on multiple semantics and the agnosias. Cognitive Neuropsychology, 10, 235–249.Google Scholar
Saffran, E.M. & Schwartz, M.F. (1994). Of cabbages and things: Semantic memory from a neuropsychological perspective—A tutorial review. Attention and Performance, 25, 507–536.Google Scholar
Sartori, G. & Job, R. (1988). The oyster with four legs: A neuropsychological study on the interaction of visual and semantic information. Cognitive Neuropsychology, 5, 105–132.Google Scholar
Sartori, G., Job, R., Miozzo, M., Zago, S., & Marchiori, G. (1993). Category-specific form-knowledge deficit in a patient with herpes simplex virus encephalitis. Journal of Clinical and Experimental Neuropsychology, 15, 280–299.Google Scholar
Schier, M.A. (2000). Changes in EEG alpha power during simulated driving: A demonstration. International Journal of Psychophysiology, 37, 155–162.Google Scholar
Segal, J.B., Williams, R., Kraut, M.A., & Hart, Jr., J. (2003). Semantic memory deficit with a left thalamic infarct. Neurology, 61, 252–254.CrossRefGoogle Scholar
Simmons, W.K. & Barsalou, W. (2003). The similarity-in-topography principle: Reconciling theories of conceptual deficits. Cognitive Neuropsychology, 20, 451–486.CrossRefGoogle Scholar
Slotnick, S., Moo, L., Kraut, M., Lesser, R., & Hart, J. (2002). Thalamic modulation of cortical rhythms during semantic memory recall in humans. Proceedings of the National Academy of Sciences United States of America, 99, 6440–6443.CrossRefGoogle Scholar
Tanaka, K. (1997). Inferotemporal cortex and object recognition. In J.W. Donahoe & V.P. Dorsel (Eds.), Neural-network models of cognition: Biobehavioral foundations (Vol. 121, pp. 160–188). Amsterdam: North-Holland/Elsevier Science Publishers.
Taylor, K., Moss, H., & Tyler, L. (2007). The conceptual structure account: A cognitive model of semantic memory and its neural instantiation. In J. Hart & M. Kraut (Eds.), Neural basis of semantic memory. London: Cambridge University Press.
Tulving, E. (1983). Elements of episodic memory. Oxford: Oxford University Press.
Tyler, L.K. & Moss, H.E. (2001). Towards a distributed account of conceptual knowledge. Trends in Cognitive Sciences, 5, 244–252.CrossRefGoogle Scholar
Tyler, L.K., Moss, H.E., Durrant-Peatfield, M.R., & Levy, J.P. (2000). Conceptual structure and the structure of concepts: A distributed account of category-specific deficits. Brain and Language, 75, 195–231.CrossRefGoogle Scholar
Tyler, L.K., Stamatakis, E.A., Dick, E., Bright, P., Fletcher, P., & Moss, H. (2003). Objects and their actions: Evidence for a neurally distributed semantic system. Neuroimage, 18, 542–557.CrossRefGoogle Scholar
Warrington, E.K. & McCarthy, R.A. (1987). Categories of knowledge: Further fractionation and an attempted integration. Brain, 110, 1273–1296.CrossRefGoogle Scholar
Warrington, E.K. & Shallice, T. (1984). Category specific semantic impairments. Brain, 107, 829–854.Google Scholar
Yang, J.J., Francis, N., Bellgowan, P.S.F., & Martin, A. (2005). Object concepts and the human amygdala: Enhanced activity for identifying animals independent of in-put modality and stimulus format. Journal of Cognitive Neuroscience, Supplement, 176.Google Scholar
Zola-Morgan, S., Cohen, N.J., & Squire, L.R. (1983). Recall of remote episodic memory in amnesia. Neuropsychologia, 21, 487–500.Google Scholar