Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-17T14:59:41.828Z Has data issue: false hasContentIssue false
  • English
  • Français

Neural substrates of object identification: Functional magnetic resonance imaging evidence that category and visual attribute contribute to semantic knowledge

Published online by Cambridge University Press:  01 March 2009

CHRISTINA E. WIERENGA ,
WILLIAM M. PERLSTEIN ,
MICHELLE BENJAMIN ,
CHRISTIANA M. LEONARD ,
LESLIE GONZALEZ ROTHI ,
TIM CONWAY ,
M. ALLISON CATO ,
KAUNDINYA GOPINATH ,
RICHARD BRIGGS  and
BRUCE CROSSON
CHRISTINA E. WIERENGA*
Affiliation:
Department of Veterans Affairs Rehabilitation Research and Development, Brain Rehabilitation Research Center at the Malcom Randall VA Medical Center, Gainesville, Florida Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida McKnight Brain Institute, University of Florida, Gainesville, Florida
WILLIAM M. PERLSTEIN
Affiliation:
Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida McKnight Brain Institute, University of Florida, Gainesville, Florida
MICHELLE BENJAMIN
Affiliation:
Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida McKnight Brain Institute, University of Florida, Gainesville, Florida
CHRISTIANA M. LEONARD
Affiliation:
McKnight Brain Institute, University of Florida, Gainesville, Florida Department of Neuroscience, University of Florida, Gainesville, Florida
LESLIE GONZALEZ ROTHI
Affiliation:
Department of Veterans Affairs Rehabilitation Research and Development, Brain Rehabilitation Research Center at the Malcom Randall VA Medical Center, Gainesville, Florida Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida McKnight Brain Institute, University of Florida, Gainesville, Florida Department of Neurology, University of Florida, Gainesville, Florida
TIM CONWAY
Affiliation:
Department of Veterans Affairs Rehabilitation Research and Development, Brain Rehabilitation Research Center at the Malcom Randall VA Medical Center, Gainesville, Florida Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida McKnight Brain Institute, University of Florida, Gainesville, Florida
M. ALLISON CATO
Affiliation:
Division of Neurology, Nemours Children’s Clinic, Jacksonville, Florida
KAUNDINYA GOPINATH
Affiliation:
Department of Nuclear and Radiological Engineering, University of Florida, Gainesville, Florida Department of Radiology, University of Texas Southwestern Medical School, Dallas, Texas
RICHARD BRIGGS
Affiliation:
Department of Radiology, University of Texas Southwestern Medical School, Dallas, Texas Department of Radiology, University of Florida, Gainesville, Florida
BRUCE CROSSON
Affiliation:
Department of Veterans Affairs Rehabilitation Research and Development, Brain Rehabilitation Research Center at the Malcom Randall VA Medical Center, Gainesville, Florida Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida McKnight Brain Institute, University of Florida, Gainesville, Florida
*
*Correspondence and reprint requests to: Christina E. Wierenga, UCSD Department of Psychiatry, VA San Diego Healthcare System, Psychology Service (151B), 3350 La Jolla Village Drive, San Diego, California 92161. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent findings suggest that neural representations of semantic knowledge contain information about category, modality, and attributes. Although an object’s category is defined according to shared attributes that uniquely distinguish it from other category members, a clear dissociation between visual attribute and category representation has not yet been reported. We investigated the contribution of category (living and nonliving) and visual attribute (global form and local details) to semantic representation in the fusiform gyrus. During functional magnetic resonance imaging (fMRI), 40 adults named pictures of animals, tools, and vehicles. In a preliminary study, identification of objects in these categories was differentially dependent on global versus local visual feature processing. fMRI findings indicate that activation in the lateral and medial regions of the fusiform gyrus distinguished stimuli according to category, that is, living versus nonliving, respectively. In contrast, visual attributes of global form (animals) were associated with higher activity in the right fusiform gyrus, while local details (tools) were associated with higher activity in the left fusiform gyrus. When both global and local attributes were relevant to processing (vehicles), cortex in both left and right medial fusiform gyri was more active than for other categories. Taken together, results support distinctions in the role of visual attributes and category in semantic representation. (JINS, 2009, 15, 169–181.)

Keywords

Semantic organizationFunctional MRIRecognitionTemporal lobeLanguageVisual perception
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 15 , Issue 2 , March 2009 , pp. 169 - 181
Copyright
Copyright © INS 2009

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.)

References

REFERENCES

Alathari, L., Trinh Ngo, C., & Dopkins, S. (2004). Loss of distinctive features and a broader pattern of priming in Alzheimer’s disease. Neuropsychology, 18, 603–612.CrossRefGoogle Scholar
Barry, C. & McHattie, J.V. (1995). Problems naming animals: Category-specific anomia or a misnomer? In Campbell, R. & Conway, M.A. (Eds.), Broken memories: Case studies in memory impairment, 237–248. New York: Blackwell.Google Scholar
Beauchamp, M.S., Lee, K.E., Haxby, J.V., & Martin, A. (2003). fMRI responses to video and point-light displays of moving humans and manipulable objects. Journal of Cognitive Neuroscience, 15, 991–1001.CrossRefGoogle ScholarPubMed
Belger, A., Puce, A., Krystal, J.H., Gore, J.C., Goldman-Rakic, P., & McCarthy, G. (1998). Dissociation of mnemonic and perceptual processes during spatial and nonspatial working memory using fMRI. Human Brain Mapping, 6, 14–32.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Birn, R.M., Saad, Z.S., & Bandettini, P.A. (2001). Spatial heterogeneity of the nonlinear dynamics in the fMRI BOLD response. NeuroImage, 14, 817–826.CrossRefGoogle ScholarPubMed
Boronat, C.B., Buxbaum, L.J., Coslett, H.B., Tang, K., Saffran, E.M., Kimberg, D.Y., & Detre, J.A. (2005). Distinctions between manipulation and function knowledge of objects: Evidence from functional magnetic resonance imaging. Cognitive Brain Research, 23, 361–373.CrossRefGoogle ScholarPubMed
Carter, C., Macdonald, A.M., Botvinick, M., Ross, L., Stenger, V.A., Noll, D., & Cohen, J.D. (2000). Parsing executive processes: Strategic vs. evaluative functions of the anterior cingulated cortex. Proceedings of the National Academy of Sciences of the United States of America, 97, 1944–1948.CrossRefGoogle Scholar
Chao, L., Haxby, J., & Martin, A. (1999). Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neuroscience, 2, 913–919.CrossRefGoogle ScholarPubMed
Chao, L. & Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. NeuroImage, 12, 478–484.CrossRefGoogle ScholarPubMed
Coltheart, M. (1981). The MRC psycholinguistic database. Quarterly Journal of Experimental Psychology, 33A, 497–505.CrossRefGoogle Scholar
Coltheart, M., Inglis, L., Cupples, L., Michie, P., & Budd, W. (1998). A semantic subsystem of visual attributes. Neurocase, 4, 353–370.CrossRefGoogle Scholar
Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers in Biomedical Research, 29, 162–173.CrossRefGoogle ScholarPubMed
Crosson, B., Cato, M.A., Sadek, J.R., & Lu, L. (2000). Organization of semantic knowledge in the human brain: Toward a resolution in the next millennium. Brain and Cognition, 42, 146–148.CrossRefGoogle Scholar
Crosson, B., Moberg, P.J., Boone, J.R., Gonzalez Rothi, L.J., & Raymer, A. (1997). Category-specific naming deficit for medical terms after dominant thalamic/capsular hemorrhage. Brain and Language, 60, 407–442.CrossRefGoogle ScholarPubMed
Damasio, H., Grabowski, T.J., Tranel, D., Hichwa, R.D., & Damasio, A.R. (1996). A neural basis for lexical retrieval. Nature, 380, 499–505.CrossRefGoogle ScholarPubMed
De Renzi, E. & Lucchelli, F. (1994). Are semantic systems separately represented in the brain? The case of living category impairment. Cortex, 30, 3–25.CrossRefGoogle ScholarPubMed
Delis, D., Massman, P., Butters, N., Salmon, D., Shear, P., Demadura, T., & Filoteo, J. (1992). Spatial cognition in Alzheimer’s disease: Subtypes of global-local impairment. Journal of Clinical and Experimental Neuropsychology, 14, 463–477.CrossRefGoogle ScholarPubMed
Devlin, J.T., Moore, C.J., Mummery, C.J., Gorno-Tempini, M.L., Phillips, J.A., Noppeney, U., Frackowiak, R.S., Friston, K.J., & Price, C.J. (2002). Anatomic constraints on cognitive theories of category specificity. NeuroImage, 15, 675–685.CrossRefGoogle ScholarPubMed
Done, D.J. & Hajilou, B.B. (2005). Loss of high-level perceptual knowledge of object structure in DAT. Neuropsychologia, 43, 60–68.CrossRefGoogle ScholarPubMed
Doyon, J. & Milner, B. (1991). Right temporal-lobe contribution to global visual processing. Neuropsychologia, 29, 343–360.CrossRefGoogle ScholarPubMed
Farah, M.J. & Wallace, M.A. (1992). Semantically-bounded anomia: Implications for the neural implementation of naming. Neuropsychologia, 30, 609–621.CrossRefGoogle Scholar
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). ‘Mini-mental State’. A practical method for grading the cognitive status of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.CrossRefGoogle Scholar
Gainotti, G. & Silveri, M.C. (1996). Cognitive and anatomical locus of lesion in a patient with a category-specific semantic impairment for living beings. Cognitive Neuropsychology, 13, 357–389.CrossRefGoogle Scholar
Gerlach, C., Law, I., Gade, A., & Paulson, O.B. (2000). Categorization and category effects in normal object recognition: A PET study. Neuropsychologia, 38, 1693–1703.CrossRefGoogle ScholarPubMed
Gerlach, C., Law, I., Gade, A., & Paulson, O.B. (2002). The role of action knowledge in the comprehension of artifacts: A PET study. NeuroImage, 15, 143–152.CrossRefGoogle Scholar
Goodglass, H. & Wingfield, A. (1993). Selective preservation of a lexical category in aphasia: Dissociations in comprehension of body parts and geographical place names following focal brain lesion. Memory, 1, 313–328.CrossRefGoogle ScholarPubMed
Harley, T.A. & Grant, F. (2004). The role of functional and perceptual attributes: Evidence from picture naming in dementia. Brain and Language, 91, 223–234.CrossRefGoogle ScholarPubMed
Hart, J. & Gordon, B. (1992). Neural subsystems for object knowledge. Nature, 359, 60–64.CrossRefGoogle ScholarPubMed
Hauk, O., Johnsrude, I., & Pulvermüller, F. (2004). Somatotopic representation of action words in human motor and premotor cortex. Neuron, 41, 301–307.CrossRefGoogle ScholarPubMed
Heilman, K.M. & Valenstein, E. (1993). Clinical Neuropsychology (3rd ed.). New York: Oxford University Press.CrossRefGoogle Scholar
Hillis, A.E. & Caramazza, A. (1991). Category-specific naming and comprehension impairment: A double dissociation. Brain, 114, 2081–2094.CrossRefGoogle ScholarPubMed
Hillis, A.E., Rapp, B., Romani, C., & Caramazza, A. (1990). Selective impairments of semantics in lexical processing. Cognitive Neuropsychology, 7, 191–243.CrossRefGoogle Scholar
Humphreys, G.W., Riddoch, M.J., & Quinlan, P.T. (1988). Cascade processes in picture identification. Cognitive Neuropsychology, 5, 67–103.CrossRefGoogle Scholar
Ishai, A., Ungerleider, L., Martin, A., Schouten, J., & Haxby, J. (1999). Distributed representation of objects in the human ventral visual pathway. Proceedings of the National Academy of Sciences of the United States of America, 96, 9379–9384.CrossRefGoogle ScholarPubMed
Kellenbach, M.L., Brett, M., & Patterson, K. (2003). Actions speak louder than functions: The importance of manipulability and action in tool representation. Journal of Cognitive Neuroscience, 15, 30–46.CrossRefGoogle ScholarPubMed
Kraut, M.A., Moo, L.R., Segal, J.B., & Hart, J. (2002). Neural activation during an explicit categorization task: Category- or feature-specific effects? Brain Research Cognitive Brain Research, 13, 213–220.CrossRefGoogle ScholarPubMed
Kucera, H. & Francis, W. (1967). Computational analysis of present-day American English. Providence, RI: Brown University Press.Google Scholar
Laws, K., Evans, J., Hodges, J., & McCarthy, R. (1995). Naming without knowing and appearance without associations: Evidence for constructive processes in semantic memory? Memory, 3, 409–433.CrossRefGoogle ScholarPubMed
Martin, A., Haxby, J., Lalonde, F., Wiggs, S., & Ungerleider, L. (1995). Discrete cortical regions associated with knowledge of color and knowledge of action. Science, 270, 102–105.CrossRefGoogle ScholarPubMed
Martin, A., Wiggs, C.L., Ungerleider, L.G., & Haxby, J.V. (1996). Neural correlates of category-specific knowledge. Nature, 379, 649–652.CrossRefGoogle ScholarPubMed
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97–113.CrossRefGoogle ScholarPubMed
Pulvermüller, F. (2001). Brain reflections of words and their meaning. Trends in Cognitive Sciences, 5, 517–524.CrossRefGoogle ScholarPubMed
Pulvermüller, F., Harle, M., & Hummel, F. (2001). Walking or talking? Behavioral and neurophysiological correlates of action verb processing. Brain and Language, 78, 143–168.CrossRefGoogle ScholarPubMed
Sacchett, C. & Humphreys, G. (1992). Calling a squirrel a squirrel, but a canoe a wigwam: A category-specific deficit for artefactual objects and body parts. Cognitive Neuropsychology, 9, 73–86.CrossRefGoogle Scholar
Shapiro, A.M., Benedict, R.H., Schretlen, D., & Brandt, J. (1999). Construct and concurrent validity of the Hopkins Verbal Learning Test-revised. Clinical Neuropsychology, 13, 348–358.CrossRefGoogle ScholarPubMed
Sheridan, J. & Humphreys, G. (1993). A verbal-semantic category-specific recognition impairment. Cognitive Neuropsychology, 10, 143–184.CrossRefGoogle Scholar
Silveri, M. & Gainotti, G. (1988). Interaction between vision and language in category-specific semantic impairment. Cognitive Neuropsychology, 5, 677–709.CrossRefGoogle Scholar
Talairach, J. & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thiem Medical Publishers.Google Scholar
Taylor, K.I., Moss, H.E., & Tyler, L.K. (2007). Cognitive model of semantic memory. In Hart, J. Jr & Kraut, M.A. (Eds.), Neural basis of semantic memory (pp. 265–301). New York: Cambridge University Press.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 ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Ingle, D.J., Goodale, M.A., & Mansfield, R.J.W. (Eds.), Analysis of visual behavior (pp. 549–586). Cambridge, MA: MIT Press.Google Scholar
Vandenberghe, R., Price, C., Wise, R., Josephs, O., & Frackowiak, R. (1996). Functional anatomy of a common semantic system for words and pictures. Nature, 383, 254–256.CrossRefGoogle ScholarPubMed
Vannucci, M., Viggiano, M.P., & Argenti, F. (2001). Identification of spatially filtered stimuli as function of the semantic category. Cognitive Brain Research, 12, 475–478.CrossRefGoogle ScholarPubMed
Warrington, E. & Shallice, T. (1984). Category specific semantic impairments. Brain, 107, 829–854.CrossRefGoogle ScholarPubMed
Weisberg, J., van Turennout, M., & Martin, A. (2007). A neural system for learning about object function. Cerebral Cortex, 17, 513–521.CrossRefGoogle Scholar
Whatmough, C., Chertkow, H., Murtha, S., & Hanratty, K. (2002). Dissociable brain regions process object meaning and object structure during picture naming. Neuropsychologia, 40, 174–186.CrossRefGoogle ScholarPubMed
Wierenga, C.E., Benjamin, M., Gopinath, K., Perlstein, W.M., Leonard, C.M., Gonzalez Rothi, L.J., Conway, T., Cato, M.A., Briggs, R., & Crosson, B. (2008). Age-related changes in word retrieval: Role of bilateral frontal and subcortical networks. Neurobiology of Aging, 29, 436–451.CrossRefGoogle ScholarPubMed
Wilson, F.A., Scalaidhe, S.P., & Goldman-Rakic, P.S. (1993). Dissociation of object and spatial processing domains in primate prefrontal cortex. Science, 260, 1955–1958.CrossRefGoogle ScholarPubMed