Hostname: page-component-7c8c6479df-p566r Total loading time: 0 Render date: 2024-03-28T16:01:30.785Z Has data issue: false hasContentIssue false

Single neurons with both form/color differential responses and saccade-related responses in the nonretinotopic pulvinar of the behaving macaque monkey

Published online by Cambridge University Press:  02 June 2009

Louis A. Benevento
Affiliation:
University of Maryland at Baltimore, Baltimore and University of Illinois at Chicago, Chicago
John D. Port
Affiliation:
University of Maryland at Baltimore, Baltimore and University of Illinois at Chicago, Chicago

Abstract

The nonretinotopic portion of the macaque pulvinar complex is interconnected with the occipitoparietal and occipitotemporal transcortical visual systems where information about the location and motion of a visual object or its form and color are modulated by eye movements and attention. We recorded from single cells in and about the border of the dorsal portion of the lateral pulvinar and the adjacent medial pulvinar of awake behaving Macaca mulatta in order to determine how the properties of these two functionally dichotomous cortical systems were represented. We found a class of pulvinar neurons that responded differentially to ten different patterns or broadband wavelengths (colors). Thirty-four percent of cells tested responded to the presentation of at least one of the pattern or color stimuli. These cells often discharged to several of the patterns or colors, but responded best to only one or two of them, and 86% were found to have statistically significant pattern and/or color preferences. Pattern/color preferential cells had an average latency of 79.1 ± 46.0 ms (range 31–186 ms), responding well before most inferotemporal cortical cell responses. Visually guided and memory-guided saccade tasks showed that 58% of pattern/color preferential cells also had saccade-related properties e.g. directional presaccadic and postsaccadic discharges, and inhibition of activity during the saccade. In the pulvinar, the mean presaccadic response latency was earlier, and the mean postsaccadic response latency was later, than those reported for parietal cortex. We also discovered that the strength of response to patterns or colors changed depending upon the behavioral setting. In comparison to trials in which the monkey fixated dead ahead during passive presentations of pattern and color stimuli, 92% of the cells showed attenuated responses to the same passive presentation of patterns and colors during fixation when these trials were interleaved with trials which also required active saccades to pattern and color targets in the periphery. We conclude that properties which represent the functionally dichotomous object and spatial visual systems are found together in single pulvinar neurons and that the responses of these cells to pattern or color stimuli are influenced by the focus of spatial attention. The pulvinar is the first structure in the brain shown to have neurons which integrate both object and spatial properties and the response latencies indicate that this information is processed before that in cortex. These results are discussed in terms of role of the pulvinar in visual attention as well as its unique role in providing both object feature and spatial location information to the inferotemporal cortex.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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

Acuña, C., Gonzalez, F. & Dominquez, R. (1983). Sensorimotor unit activity related to intention in the pulvinar of behaving Cebus appela monkeys. Experimental Brain Research 52, 411421.CrossRefGoogle Scholar
Andersen, R.A., Asanuma, C., Essick, G. & Siegel, R.M. (1990). Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobe. Journal Comparative Neurology 296, 65113.CrossRefGoogle Scholar
Andersen, R.A. & Gnadt, J.W. (1989). Role of the posterior parietal cortex in saccadic eye movements. In Reviews in Oculomotor Research, Volume III, ed. Wurtz, R.H. & Goldberg, M.E., pp. 315335. Amsterdam: Elsevier.Google Scholar
Andersen, R.A., Essick, G.K. & Siegel, R.M. (1987). Neurons of area 7 activated by both visual stimuli and oculomotor behavior. Experimental Brain Research 67, 316322.CrossRefGoogle ScholarPubMed
Baizer, J.S., Desimone, R. & Ungerleider, L.G. (1993). Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys. Visual Neuroscience 10, 5972.CrossRefGoogle ScholarPubMed
Baleydier, C. & Morel, A. (1992). Segregated thalamocortical pathways to inferior parietal and inferotemporal cortex in macaque monkey. Visual Neuroscience 8, 391405.CrossRefGoogle ScholarPubMed
Barash, S., Gracewell, R.M., Fogassi, L., Gnadt, J.W. & Andersen, R.A. (1991 a). Saccade-related activity in the lateral intraparietal area. I. Temporal properties: Comparison with area 7a. Journal Neurophysiology 66, 10951108.CrossRefGoogle Scholar
Barash, S., Gracewell, R.M., Fogassi, L., Gnadt, J.W. & Andersen, R.A. (1991 b). Saccade-related activity in the lateral intraparietal area. II. Spatial properties. Journal Neurophysiology 66, 11091124.CrossRefGoogle ScholarPubMed
Baylis, G.C., Rolls, E.T. & Leonard, C.M. (1987). Functional subdivisions of the temporal lobe neocortex. Journal for Neuroscience 7, 330342.CrossRefGoogle ScholarPubMed
Bender, D.B. (1981). Retinotopic organization of macaque pulvinar. Journal Neurophysiology 46, 672693.Google Scholar
Bender, D.B. (1982). Receptive-field properties of neurons in the macaque inferior pulvinar. Journal of Neurophysiology 48, 117.Google Scholar
Bender, D.B. & Baizer, J.S. (1990). Saccadic eye movements following kainic acid lesions of the pulvinar in monkeys. Experimental Brain Research 79, 467478.Google Scholar
Benevento, L.A. & Davis, B. (1977). Topographical projections of the prestriate cortex to the pulvinar in the macaque monkey: An autoradiographic study. Experimental Brain Research 30, 405424.Google Scholar
Benevento, L.A. & Fallon, J. (1975). The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). Journal of Comparative Neurology 160, 339362.CrossRefGoogle ScholarPubMed
Benevento, L.A. & McCleary, L.B. (1992). An immunocytochemical method for marking microelectrode tracks following single-unit recordings in long surviving awake monkeys. Journal Neuroscience Methods 41, 199204.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Miller, J. (1981). Visual responses of single neurons in the caudal lateral pulvinar of the macaque monkey. Journal of Neuroscience 1, 12681278.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Rezak, M. (1976). The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca mulatta): An autoradiographic study. Brain Research 108, 124.Google Scholar
Benevento, L.A. & Standage, G.P. (1983). The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 217, 307336.CrossRefGoogle Scholar
Benevento, L.A. & Yoshida, K. (1981). The afferent and efferent organization of lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 203, 455474.CrossRefGoogle ScholarPubMed
Boussaoud, D., Desimone, R. & Ungerleider, L.G. (1992). Subcortical connections of visual areas MST and FST in Macaques. Visual Neuroscience 9, 291302.CrossRefGoogle ScholarPubMed
Bushnell, M.C., Goldberg, M.E. & Robinson, D.L. (1981). Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. Journal of Neurophysiology 46, 755772.CrossRefGoogle ScholarPubMed
Chalupa, L.M. (1991). Visual function of the pulvinar. In Vision and Visual Dysfunction, Vol. 4: Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 140159. Boston, MA: CRC Press.Google Scholar
Chelazzi, L., Miller, E.K., Duncan, J. & Desimone, R. (1993). A neural basis for visual search in inferior temporal cortex. Nature 363, 345347.CrossRefGoogle ScholarPubMed
Desimone, R., Wessinger, M., Thomas, L. & Scheinder, W. (1990). Attentional control of visual perception: Cortical and subcortical mechanisms. Cold Spring Harbor Symposium Quantitative Biology 55, 963971.CrossRefGoogle ScholarPubMed
Desimone, R., Albright, T.D., Gross, C.G. & Bruce, C.J. (1984). Stimulus selective properties of inferior temporal neurons in the macaque. Journal of Neuroscience 4, 20512062.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219226.CrossRefGoogle ScholarPubMed
Dow, B.M. (1991). Colour Vision. In Vision and Visual Dysfunction, Vol. 4: Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 316338. Boston, MA: CRC Press.Google Scholar
Goldberg, M.E. & Wurtz, R.H. (1972). Activity of superior colliculus in behaving monkey. II. Effects of attention on neuronal responses. Journal of Neurophysiology 35, 560574.CrossRefGoogle ScholarPubMed
Gross, C.G., Rocha-Miranda, C.E. & Bender, D.B. (1972). Visual properties of neurons in inferotemporal cortex of the macaque. Journal of Neurophysiology 35, 96111.CrossRefGoogle ScholarPubMed
Hardy, S.G. & Lynch, J.C. (1992). The spatial distribution of pulvinar neurons that project to two subregions of the inferior parietal lobule in the macaque. Cerebral Cortex 2, 217230.CrossRefGoogle ScholarPubMed
Hikosaka, O. & Wurtz, R.H. (1983). Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memorycontingent visual and saccade responses. Journal Neurophysiology 49, 12681284.CrossRefGoogle ScholarPubMed
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position: An improved method. Vision Research 20, 535538.CrossRefGoogle ScholarPubMed
Komatsu, H., Ideura, Y., Shinji, K. & Yamane, S. (1992). Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey. Journal of Neuroscience 12, 408424.CrossRefGoogle ScholarPubMed
LaBerge, D. & Buchsbaum, M.S. (1990). Positron emission tomographic measurements of pulvinar activity during an attention task. Journal of Neuroscience 10, 613619.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740749.CrossRefGoogle ScholarPubMed
Lynch, J.C., Mountcastle, V.B., Talbot, W.H. & Yin, T.C.T. (1977). Parietal lobe mechanisms for directed visual attention. Journal of Neurophysiology 40, 362389.CrossRefGoogle ScholarPubMed
Lysakowski, A., Standage, G.P. & Benevento, L.A. (1986). Histological and architectonic differentiation of zones of pretectal and collicular inputs to the pulvinar and dorsal lateral geniculate nuclei in the macaque. Journal of Comparative Neurology 250, 431448.CrossRefGoogle Scholar
Mauguiere, F. & Baleydier, C. (1978). Topographical organization of medial pulvinar neurons sending fibers to Brodmann's areas 7, 21 and 22 in the monkey. Experimental Brain Research 31, 605607.CrossRefGoogle Scholar
Mikami, A. & Kubota, K. (1980). Inferotemporal neuron activities and color discrimination. Brain Research 182, 6578.CrossRefGoogle ScholarPubMed
Mishkin, M., Lewis, M.E. & Ungerleider, L. (1982). Equivalence of parieto-preoccipital subareas for visuospatial ability in monkeys. Behavioral Brain Research 6, 4155.CrossRefGoogle ScholarPubMed
Moran, J. & Desimone, R. (1985). Selective attention gates visual processing in extrastriate cortex. Science 229, 792794.Google Scholar
Morecraft, R.J., Guela, C. & Mesulam, M.M. (1993). Architecture of connectivity within a cingulo-fronto-parietal neurocognitive network for directed attention. Archives of Neurology 50, 279284.Google Scholar
Morel, A. & Bullier, J. (1990). Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience 4, 555578.CrossRefGoogle ScholarPubMed
Mountcastle, V.B. (1982). An organizing principle for cerebral function: The unit module and the distributed system. The Mindful Brain, pp. 750. Cambridge, MA: MIT Press.Google Scholar
Mountcastle, V.B., Motter, B.C., Steinmetz, M.A. & Sestokas, K.A. (1987). Common and differential effects of attentive fixation on the excitability of the parietal and prestriate (V4) cortical visual neurons in the macaque. Journal of Neuroscience 7, 22392255.Google Scholar
Perryman, K.M., Lindsley, D.F. & Lindsley, D.B. (1980). Pulvinar neuron responses to spontaneous and trained eye movements and to light flashes in squirrel monkeys. Electroencephalography and Clinical Neurology 49, 152161.Google Scholar
Petersen, S.E., Robinson, D.L. & Keys, W. (1985). Pulvinar nuclei of the behaving rhesus monkey: Visual responses and their modulation. Journal of Neurophysiology 54, 867886.CrossRefGoogle ScholarPubMed
Petersen, S.E., Robinson, D.L. & Morris, J.D. (1987). Contribution of the pulvinar to visual spatial attention. Neuropsychologia 25, 97105.CrossRefGoogle ScholarPubMed
Port, J. & Benevento, L.A. (1991). Form and Location properties of single units in the pulvinar of awake monkeys. Society for Neuroscience 17, 711.Google Scholar
Port, J., Castillo, E. & Benevento, L.A. (1992). Pattern and color encoding neurons with oculomotor properties in the macaque pulvinar. Society of Neuroscience 18, 1417.Google Scholar
Port, J. & Benevento, L.A. Saccade-dependent responses in dorsal pulvinar neurons of the awake behaving macaque (in preparation).Google Scholar
Posner, M.I. & Petersen, S.E. (1990). The attention system of the human brain. Annual Review of Neuroscience 13, 2542.CrossRefGoogle ScholarPubMed
Rafal, R.D. & Posner, M.I. (1987). Deficits in human spatial attention following thalamic lesions. Proceedings of the National Academy of Sciences of the U.S.A. 84, 73497353.CrossRefGoogle ScholarPubMed
Raiguel, S.E., Lieven, L., Balazs, G. & Orban, G.A. (1989). Response latencies of visual cells in macaque areas V1, V2 and V5. Brain Research 493, 155159.Google Scholar
Rezak, M. & Benevento, L.A. (1979). A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey. Brain Research 167, 1940.CrossRefGoogle ScholarPubMed
Richmond, B.J., Wurtz, R.H. & Sato, T. (1983). Visual responses of inferior temporal neurons in awake rhesus monkey. Journal of Neurophysiology 50, 14151432.Google Scholar
Richmond, B.J. & Sato, T. (1987). Enhancement of inferior temporal neurons during visual discrimination. Journal of Neurophysiology 58, 12921306.CrossRefGoogle ScholarPubMed
Richmond, B.J., Optican, L.M., Podell, M. & Spitzer, H. (1987). Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. Journal of Neurophysiology 57, 132.Google Scholar
Rizzolati, G. (1983). Mechanisms of selective attention in mammals. In Advances in Vertebrate Neuroethiology, ed. Ewert, J.P. et al. , London: Plenum Press.Google Scholar
Robinson, D.L., Goldberg, M.E. & Stanton, G.B. (1978). Parietal association cortex in the primate: Sensory mechanisms and behavioral modulations. Journal of Neurophysiology 41, 910932.Google Scholar
Robinson, D.L. & McClurkin, J.W. (1989). The visual superior colliculus and pulvinar. In Reviews in Oculomotor Research, Vol. III., ed. Wurtz, R.H. & Goldberg, M.E., pp. 337360. Amsterdam: Elsevier.Google Scholar
Robinson, D.L., McClurkin, J.W. & Kertzman, C. (1990). Orbital position and eye movement influences on visual responses in the pulvinar nuclei of the behaving macaque. Experimental Brain Research 82, 235246.CrossRefGoogle ScholarPubMed
Robinson, D.L., McClurkin, J.W., Kertzman, C. & Petersen, S.E. (1991). Visual responses of pulvinar and collicular neurons during eye movements of awake, trained macaques. Journal of Neurophysiology 66, 485496.CrossRefGoogle ScholarPubMed
Robinson, D.L. & Petersen, S.E. (1985). Responses of pulvinar neurons to real and self-induced stimulus movement. Brain Research 338, 392394.CrossRefGoogle ScholarPubMed
Robinson, D.L. & Petersen, S.E. (1992). The pulvinar and visual salience. Trends in Neuroscience 15, 127132.Google Scholar
Robinson, D.L., Petersen, S.E. & Keys, W. (1986). Saccade-related and visual activity in the pulvinar nuclei of the behaving rhesus monkey. Experimental Brain Research 62, 625634.Google Scholar
Robinson, D.L. (1993). Functional contributions of the primate pulvinar. Program in Brain Research 95, 371380.CrossRefGoogle ScholarPubMed
Robinson, D. L. & Petersen, S.E. (1992). The pulvinar and visual salience. Trends in Neuroscience 15, 127132.Google Scholar
Rolls, E.T., Judge, S.J. & Sanghera, M. (1977). Activity of neurons in the inferotemporal cortex of the alert monkey. Brain Research 130, 229238.Google Scholar
Sakata, H., Shibutani, H., Kawano, K. & Harrington, T.L. (1985). Neural mechanisms of space vision in the parietal association cortex of the monkey. Vision Research 25, 453463.Google Scholar
Sato, T. (1988). Effects of attention and stimulus interaction on visual responses of inferior temporal neurons in macaque. Journal of Neurophysiology 60, 344364.Google Scholar
Sato, T. (1990). Neuronal mechanisms of visual selective attention in monkey inferior temporal cortex. In Vision, Memory, and the Temporal Lobe, pp. 111121. NY: Elsevier Science Publishing Co.Google Scholar
Sato, T., Kawamura, T. & Iwai, E. (1980). Responsiveness or inferotemporal single units to visual pattern stimuli in monkeys performing discrimination. Experimental Brain Research 38, 313319.CrossRefGoogle ScholarPubMed
Schein, S.J. & Desimone, R. (1990). Spectral properties of V4 neurons in the macaque. Journal of Neuroscience 10, 33693389.Google Scholar
Selemon, L.D. & Goldman-Rakic, P.S. (1988). Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: Evidence for a distributed neural network subserving spatially guided behavior. Journal of Neuroscience 8, 40494068.Google Scholar
Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. NY: McGraw Hill.Google Scholar
Spitzer, H. & Richmond, B.J. (1991). Task difficulty: Ignoring, attending to, and discriminating a visual stimulus yield progressively more activity in inferior temporal neurons. Experimental Brain Research 83, 340348.CrossRefGoogle ScholarPubMed
Ungerleider, L.G., Galkin, T.W. & Mishkin, M. (1983). Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey. Journal of Comparative Neurology 217, 137157.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Analysis of Visual Behavior, ed. Ingle, D.J., pp. 549586. Cambridge, MA: MIT Press.Google Scholar
Webster, M.J., Bachevalier, J. & Ungerleider, L.G. (1993). Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. Journal of Comparative Neurology 335, 7391.Google Scholar
Wilson, F.A.W., Scalaidhe, S.P.O. & Goldman-Rakic, P.S. (1993). Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 19551957.Google Scholar
Wurtz, R.H. (1969). Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. Journal Neurophysiology 32, 975986.CrossRefGoogle ScholarPubMed
Zeki, S. (1977). Colour coding in the superior temporal sulcus of the rhesus monkey visual cortex. Proceedings of the Royal Society B (London) 277, 195223.Google Scholar