Skip to main content Accessibility help
×
Home

Extraretinal representations in area V4 in the macaque monkey

  • John H. R. Maunsell (a1), Gary Sclar (a1), Tara A. Nealey (a1) and Derryl D. DePriest (a1)

Abstract

Several neurophysiological studies have shown that the visual cerebral cortex of macaque monkeys performing delayed match-to-sample tasks contains individual neurons whose levels of activity depend on the sample the animal is required to remember. Haenny et al. (1988) reported that the activity of neurons in area V4 of monkeys performing an orientation matching task depends on the orientation for which the animal is searching. It was proposed that these neurons contribute to a representation of the orientation being sought.

We have further characterized these neurons by recording visual responses from individual neurons during multiple behavioral tasks. Animals were trained to perform an orientation match-to-sample task using either a visual or a tactile orientation sample. In a set of 89 neurons examined using both types of sample, 25% showed statistically significant effects of sample orientation regardless of whether the sample was visual or tactile. Most of these preferred the same sample orientation in both conditions. These results allow us to specify the nature of the information signaled by these neurons more precisely than has previously been possible.

For 193 units tested using one of the matching tasks, responses were also recorded while the animal performed a simple fixation task. In this task the animal was not required to attend to the visual stimuli that were presented. A few neurons that were responsive during the matching task were silent during fixation, but a comparable number was much more responsive during fixation. Across the whole population there was no systematic change in either responsivity or selectivity for orientation under the two conditions.

Copyright

References

Hide All
Andersen, R.A. & Mountcastle, V.B. (1983). The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex. Journal of Neuroscience 3, 532548.
Bruce, C.J. & Goldberg, M.E. (1985). Cerebral cortical activity associated with the orientation of visual attention in the rhesus monkey. Vision Research 25, 471481.
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.
Desimone, R., Albright, T.D., Gross, C.G. & Bruce, C. (1984). Stimulus-selective properties of inferior temporal neurons in the macaque. Journal of Neuroscience 4, 20512062.
Fuster, J.M. & Jervey, J.P. (1982). Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task. Journal of Neuroscience 2, 361375.
Gnadt, W. & Andersen, R.A. (1988). Memory related motor planning activity in posterior parietal cortex of macaque. Experimental Brain Research 70, 216220.
Goldberg, M.E. & Bushnell, M.C. (1981). Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation infrontal eye fields specifically related to saccades. Journal of Neurophysiology 46, 773787.
Goldberg, M.E. & Wurtz, R.H. (1972). Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. Journal of Neurophysiology 35, 560–559.
Haenny, P.E., Maunsell, J.H.R. & Schiller, P.H. (1988). State dependent activity in monkey visual cortex. II. Extraretinal factors in V4. Experimental Brain Research 69, 245259.
Haenny, P.E. & Schiller, P.H. (1988). State dependent activity in monkey visual cortex. I. Single cell activity in V1 and V4 on visual tasks. Experimental Brain Research 69, 225244.
Hikosaka, O. & Wurtz, R.H. (1983). Visual and oculomotor functions of monkey substantia nigra par reticulata: III. Memory-contingent visual and saccade responses. Journal of Neurophysiology 49, 12681284.
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.
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.
Maunsell, J.H.R. & Schiller, P.H. (1984). Evidence for the segregation of parvo- and magnocellular channels in the visual cortex of the macaque monkey. Society for Neuroscience Abstracts 10, 520.
Maunsell, J.H.R. & Sclar, G. (1988). Neurons in area V4 of the macaque monkey signal task-specific information. Investigative Ophthalmology and Visual Science 29, 22.
Maunsell, J.H.R., Sclar, G. & Nealey, T.A. (1988). Task-specific signals in area V4 of monkey visual cortex. Society for Neuroscience Abstracts 14, 10.
Mays, L.E. & Sparks, D.L. (1980). Dissociation of visual and saccade-related responses in superior colliculus neurons. Journal of Neurophysiology 43, 207232.
Miyashita, Y. (1988). Neuronal correlate of visual associative long-term memory in the primate visual cortex. Nature 335, 817820.
Miyashita, Y. & Chang, H.S. (1988). Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331, 6870.
Moran, J. & Desimone, R. (1985). Selective attention gates visual processing in the extrastriate cortex. Science 229, 782784.
Mountcastle, V.B., Motter, B.C., Steinmetz, M.A. & Sestokas, A.K. (1987). Common and differential effects of attentive fixation on the excitability of parietal and prestriate (V4) cortical visual neurons in the macaque monkey. Journal of Neuroscience 7, 22392255.
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.
Remmel, R.S. (1984). An inexpensive eye movement monitor using the scleral search coil technique. IEEE Transactions in Biomedical Engineering 31, 388390.
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, 132146.
Richmond, B.J., Wurtz, R.H. & Sato, T. (1983). Visual responses of inferior temporal neurons in awake rhesus monkey. Journal of Neurophysiology 50, 1415.
Robinson, D.A. (1963). A method of measuring eye movements using a scleral search coil in a magnetic field. IEEE Transactions in Biomedical Engineering 101, 131145.
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.
Spitzer, H., Desimone, R. & Moran, J. (1988). Increased attention enhances both behavioral and neuronal performance. Science 240, 338340.
Wolbarsht, M.L., McNichol, E.G. & Wagner, H.G. (1960). Glass insulated platinum microelectrode. Science 132, 13091310.
Wurtz, R.H. & Goldberg, M.E. (1972). The primate superior colliculus and the shift of visual attention. Investigative Ophthalmology 11, 441449.
Wurtz, R.H. & Mohler, C.W. (1976). Organization of monkey superior colliculus: Enhanced visual response of superficial layer cells. Journal of Neurophysiology 39, 745762.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed