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Neural hybrid model of semantic object memory: Implications from event-related timing using fMRI

Published online by Cambridge University Press:  12 February 2004

MICHAEL A. KRAUT
Affiliation:
Dept. of Radiology, Division of Neuroradiology, The Johns Hopkins University School of Medicine, Baltimore, MD
VINCE CALHOUN
Affiliation:
Dept. of Psychiatry, Yale University, New Haven, CT
JEFFERY A. PITCOCK
Affiliation:
Depts. of Geriatrics, Neurology, and Radiology, Donald. W. Reynolds Center on Aging, University of Arkansas for Medical Science, Little Rock, AR
CATHERINE CUSICK
Affiliation:
Dept. of Structural and Cellular Biology, Neuroscience Program, Tulane University, New Orleans, LA
JOHN HART
Affiliation:
Depts. of Geriatrics, Neurology, and Radiology, Donald. W. Reynolds Center on Aging, University of Arkansas for Medical Science, Little Rock, AR

Abstract

Previous studies by our group have demonstrated fMRI signal changes and synchronized gamma rhythm EEG oscillations between thalamus and cortical regions as subjects recall objects from visually presented features. Here, we extend this work by estimating the time course of fMRI signal changes in the cortical and subcortical regions found to exhibit evidence for task-related activation. Our results indicate that there are separate loci of signal changes in the thalamus (dorsomedial and pulvinar) that exhibit notable differences in times of onset, peak and return to baseline of signal changes. The signal changes in the pulvinar demonstrate the slowest transients of all the cortical and subcortical regions we examined. Evaluation of cortical regions demonstrated salient differences as well, with the signal changes in Brodmann area 6 (BA6) rising, peaking, and returning to baseline earlier than those detected in other regions. We conclude that BA6 mediates early designation or refinement of search criteria, and that the pulvinar may be involved in the binding of feature stimuli for an integrated object memory. (JINS, 2003, 9, 1031–1040.)

Type
THEMATIC ARTICLES
Copyright
© 2003 The International Neuropsychological Society

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References

REFERENCES

Binder, J.R., Swanson, S.J., Hammeke, T., Morris, G., Mueller, W., Fischer, M., Benbadis, S., Frost, J., Rao, S., & Haughton, V. (1996). Determination of language dominance using functional MRI: A comparison with the Wada test. Neurology, 46, 978984.CrossRefGoogle Scholar
Calhoun, V., Adali, T., Kraut, M., & Pearlson, G. (2000). A weighted least-squares algorithm for estimation and visualization of relative latencies in event-related functional MRI. Magnetic Resonance in Medicine, 44, 947954.3.0.CO;2-5>CrossRefGoogle Scholar
Caramazza, A. & Shelton, J.R. (1998). Domain-specific knowledge systems in the brain: The animate-inanimate distinction. Journal of Cognitive Neuroscience, 10, 134.Google Scholar
Chao, L.L., Haxby, J., & Martin, A. (1999). Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neuroscience, 2, 913919.CrossRefGoogle Scholar
Crosson, B., Sadek, J.R., Bobholz, J.A., Gokcay, D., Mohr, C., Leonard, C., Maron, L., Auerbach, E., Browd, S., Freeman, A., & Briggs, R. (1999). Activity in the paracingulate and cingulate sulci during word generation: An fMRI study of functional anatomy. Cerebral Cortex, 9, 307316.CrossRefGoogle Scholar
Devlin, J.T., Russell, R.P., Davis, M.H., Price, C., Moss, H., Fadili, M., & Tyler, L. (2002). Is there an anatomical basis for category-specificity? Semantic memory studies in PET and fMRI. Neuropsychologia, 40, 5475.CrossRefGoogle Scholar
Eichenbaum, H. & Bunsey, M. (1995). On the binding of associations in memory: Clues from studies on the role of hippocampal region in paired-associate learning. Current Directions in Psychological Science, 4, 1923.Google Scholar
Fiez, J.A. (1997). Phonology, semantics, and the role of the left inferior prefrontal cortex. Human Brain Mapping, 5, 7983.Google Scholar
Fodor, J.A. & Pylyshyn, Z.W. (1988). Connectionism and cognitive architecture: A critical analysis. Cognition, 28, 371.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, 539559.Google Scholar
Gray, C.M. (1999). The temporal correlation hypothesis of visual feature integration: Still alive and well. Neuron, 24, 3147.CrossRefGoogle Scholar
Guillery, R.W. (1995). Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. Journal of Anatomy, 187, 583592.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, 6186.3.0.CO;2-I>CrossRefGoogle Scholar
Hart, J. & Gordon, B. (1990). Delineation of single-word semantic comprehension deficits in aphasia, with anatomical correlation. Annals of Neurology, 27, 226231.Google Scholar
Hart, J. & Gordon, B. (1992). Neural subsystems for object knowledge. Nature, 359, 6064.Google Scholar
Hart, J., Moo, L., Segal, J.B., Adkins, E., & Kraut, M. (2002). Neural substrates of semantics. In A. Hillis (Ed.), Handbook of language disorders, (pp. 207227). Philadelphia: Psychology Press.
Haxby, J., Gobbini, M.I., Furey, M.L., Ishai, A., & Pietrini, P. (2001). Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science, 293, 24252430.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, 315330.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, 217227.CrossRefGoogle Scholar
Joliot, M., Ribary, U., & Llinas, R. (1994). Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proceedings of the National Academy of Sciences U.S.A., 91, 1174811751.Google Scholar
Kemmerer, D. & Tranel, D. (2000). Verb retrieval in brain-damaged subjects: 1. Analysis of stimulus, lexical, and conceptual factors. Brain and Language, 73, 347392.Google Scholar
Klimesch, W. (1996). Memory processes, brain oscillations and EEG synchronization. International Journal of Psychophysiology, 24, 61100.Google Scholar
Kounios, J., Smith, R.W., Yang, W., Bachman, P., & D'Esposito, N. (2001). Cognitive association formation in human memory revealed by spatiotemporal brain imaging. Neuron, 29, 297306.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, 2436.Google Scholar
Kraut, M.A., Kremen, S., Moo, L.R., Segal, J., Calhoun, V., & Hart, J. (2002b). Object activation in semantic memory from visual multimodal feature input. Journal of Cognitive Neuroscience, 14, 3747.Google Scholar
Kraut, M., Moo, L., Segal, J., & Hart, J. (2002c). Neural activation during an explicit categorization task: Category- or feature-specific effects? Brain Research Cognitive Brain Research, 13, 213220.Google Scholar
Llinas, R.R., Ribary, U., Jeanmonod, D., Kronberg, E., & Mitra, P. (1999). Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proceedings of the National Academy of Sciences USA, 96, 1522215227.CrossRefGoogle Scholar
Martin, A., Wiggs, C.L., Ungerleider, L.G., & Haxby, J.V. (1996). Neural correlates of category-specific knowledge. Nature, 379, 649652.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, 662667.Google Scholar
Moore, C.J. & Price, C.J. (1999). A functional neuroimaging study of the variables that generate category-specific object processing differences. Brain, 122, 943962.CrossRefGoogle Scholar
Nadeau, S.E. & Crosson, B. (1997). Subcortical aphasia. Brain and Language, 58, 355402.Google Scholar
Ojemann, J., Ojemann, G., & Lettich, E. (2002). Cortical stimulation mapping of language cortex by using a verb generation task: Effects of learning and comparison to mapping based on object naming. Journal of Neurosurgery, 97, 3338.CrossRefGoogle Scholar
Preuss, T.M. & Goldman-Rakic, P.S. (1987). Crossed corticothalamic and thalamocortical connections of macaque prefrontal cortex. Journal of Comparative Neurology, 257, 269281.Google Scholar
Ribary, U., Ioannides, A.A., Singh, K.D., Asno, R., Bolton, J., Lado, F., Mogilner, A., Llinas, R. (1991). Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proceedings of the National Academy of Sciences USA, 88, 1103711041.Google Scholar
Sherman, S.M. (2001). Thalamic relay functions. Progress in Brain Research, 134, 5169.Google Scholar
Singer, W. (1993). Synchronization of cortical activity and its putative role in information processing and learning. Annual Review of Physiology, 55, 349374.Google Scholar
Singer, W. & Gray, C.M. (1995). Visual feature integration and the temporal correlation hypothesis. Annual Review of Neuroscience, 18, 555586.Google 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 USA, 99, 64406443.CrossRefGoogle Scholar
Smith, E.E., Shoben, E.J., & Rips, L.J. (1974). Structure and process in semantic memory: A featural model for semantic decisions. Psychological Review, 81, 214241.Google Scholar
Steriade, M. (2000). Corticothalamic resonance, states of vigilance and mentation. Neuroscience, 101, 243276.Google Scholar
Talairach, J. & Tournoux, P. (1988). Co-planar sterotaxic atlas of the human brain: 3-dimensional proportional system: An approach to medical cerebral imaging. New York: Thieme.
Thompson-Schill, S., D'Esposito, M., Aguirre, G., & Farah, M. (1997). Role of left inferior prefrontal cortex in retrieval of semantic knowledge: A reevaluation. Proceedings of the National Academy of Sciences USA, 94, 1479214797.CrossRefGoogle Scholar
Thompson-Schill, S., Swick, D., Farah, M., D'Esposito, M., Kan, I., & Knight, R. (1998). Verb generation in patients with focal frontal lesions: A neuropsychological test of neuroimaging findings. Proceedings of the National Academy of Sciences USA, 95, 1585515860.Google Scholar
Tyler, L. & Moss, H. (2001). Towards a distributed account of conceptual knowledge. Trends in Cognitive Science, 5, 244252.CrossRefGoogle Scholar
Underwood, G. & Whitfield, A. (1985). Right hemisphere interactions in picture–word rocessing. Brain and Cognition, 4, 273286.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, 254256.Google Scholar
Ward, R., Danziger, S., Owen, V., & Rafal, R. (2002). Deficits in spatial coding and feature binding following damage to spatiotopic maps in the human pulvinar. Nature Neuroscience, 5, 99100.CrossRefGoogle Scholar
Warrington, E. & McCarthy, R.A. (1994). Multiple meaning systems in the brain: A case for visual semantics. Neuropsychología, 32, 14651473.Google Scholar
Wilson, F.A., Scalaidhe, S.P., & Goldman-Rakic, P.S. (1993). Dissociation of object and spatial processing domains in primate prefrontal cortex. Science, 260, 19551958.CrossRefGoogle Scholar
Yeterian, E.H. & Pandya, D.N. (1988). Corticothalamic connections of paralimbic regions in the rhesus monkey. Journal of Comparative Neurology, 269, 130146.Google Scholar