Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-21T23:55:32.013Z Has data issue: false hasContentIssue false
  • English
  • Français

A relationship between behavioral choice and the visual responses of neurons in macaque MT

Published online by Cambridge University Press:  02 June 2009

K. H. Britten ,
W. T. Newsome ,
M. N. Shadlen ,
S. Celebrini  and
J. A. Movshon
K. H. Britten
Affiliation:
Department of Neurobiology, Stanford University School of Medicine, Stanford
W. T. Newsome
Affiliation:
Department of Neurobiology, Stanford University School of Medicine, Stanford
M. N. Shadlen
Affiliation:
Department of Neurobiology, Stanford University School of Medicine, Stanford
S. Celebrini
Affiliation:
Department of Neurobiology, Stanford University School of Medicine, Stanford
J. A. Movshon
Affiliation:
Howard Hughes Medical Institute and Center for Neural Science, New York University, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

We have previously documented the exquisite motion sensitivity of neurons in extrastriate area MT by studying the relationship between their responses and the direction and strength of visual motion signals delivered to their receptive fields. These results suggested that MT neurons might provide the signals supporting behavioral choice in visual discrimination tasks. To approach this question from another direction, we have now studied the relationship between the discharge of MT neurons and behavioral choice, independently of the effects of visual stimulation. We found that trial-to-trial variability in neuronal signals was correlated with the choices the monkey made. Therefore, when a directionally selective neuron in area MT fires more vigorously, the monkey is more likely to make a decision in favor of the preferred direction of the cell. The magnitude of the relationship was modest, on average, but was highly significant across a sample of 299 cells from four monkeys. The relationship was present for all stimuli (including those without a net motion signal), and for all but the weakest responses. The relationship was reduced or eliminated when the demands of the task were changed so that the directional signal carried by the cell was less informative. The relationship was evident within 50 ms of response onset, and persisted throughout the stimulus presentation. On average, neurons that were more sensitive to weak motion signals had a stronger relationship to behavior than those that were less sensitive. These observations are consistent with the idea that neuronal signals in MT are used by the monkey to determine the direction of stimulus motion. The modest relationship between behavioral choice and the discharge of any one neuron, and the prevalence of the relationship across the population, make it likely that signals from many neurons are pooled to form the data on which behavioral choices are based.

Keywords

Visual cortexExtrastriateMiddle temporalMotion sensitivityPsychophysicsDiscriminationBehaviorMonkey
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 1 , January 1996 , pp. 87 - 100
Copyright
Copyright © Cambridge University Press 1996

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

Albright, T.D. (1984). Direction and orientation selectivity of neurons in visual area MT of the macaque. Journal of Neurophysiology 52, 1106–1130.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1971). A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Research 31, 85–105.CrossRefGoogle ScholarPubMed
Allman, J.M., Meizin, F. & McGuinness, E. (1985). Direction and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14, 105–126.CrossRefGoogle ScholarPubMed
Bamber, D. (1975). The area above the ordinal dominance graph and the area below the receiver operating characteristic graph. Journal of Mathematical Psychology 12, 387–415.CrossRefGoogle Scholar
Barlow, H.B., Levick, W.R. & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research (Suppl.) 3, 87–101.CrossRefGoogle Scholar
Bradley, A., Skottun, B.C., Ohzawa, I., Sclar, G. & Freeman, R.D. (1987). Visual orientation and spatial frequency discrimination: A comparison of single cells and behavior. Journal of Neurophysiology 57, 755–772.CrossRefGoogle ScholarPubMed
Britten, K.H., Newsome, W.T. & Movshon, J.A. (1988). Association between cortical unit activity and psychophysical response in alert monkeys. Society for Neuroscience Abstracts 14, 458.Google Scholar
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. (1992). The analysis of visual motion: A comparison of neuronal and psychophysical performance. The Journal of Neuroscience 12, 4745–4765.CrossRefGoogle Scholar
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. (1993). Responses of neurons in macaque MT to stochastic motion signals. Visual Neuroscience 10, 1157–1169.Google Scholar
Celebrini, S. & Newsome, W.T. (1994). Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. Journal of Neuroscience 14, 4109–4124.CrossRefGoogle ScholarPubMed
Cohn, T.E., Green, D.G. & Tanner, W.P. (1971). Receiver operating characteristic analysis. Application to the study of quantum fluctuation in optic nerve of Rana pipiens. Journal of General Physiology 66, 583–616.CrossRefGoogle Scholar
Dubner, R., Kenshalo, D.R., Maixner, W., Bushnell, M.C. & Oliveras, J.L. (1989). The correlation of monkey medullary dorsal horn neuronal activity and the perceived intensity of noxious heat stimuli. Journal of Neurophysiology 62, 450–457.CrossRefGoogle ScholarPubMed
Efron, B. & Tibshirani, R.J. (1993). An Introduction to the Bootstrap. New York: Chapman and Hall.Google Scholar
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurological Research 1, 203–209.CrossRefGoogle ScholarPubMed
Green, D.M. & Swets, J.A. (1966). Signal Detection Theory and Psy-chophysics. New York: John Wiley and Sons, Inc.Google Scholar
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, 535–538.CrossRefGoogle ScholarPubMed
Logothetis, N.K. & Schall, J.D. (1989). Neuronal correlates of subjective visual perception. Science 245, 761.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1983). Functional properties of neurons in the middle temporal visual area (MT) of the macaque monkey: I. Selectivity for stimulus direction, speed and orientation. Journal of Neurophysiology 49, 1127–1147.CrossRefGoogle ScholarPubMed
Moran, J. & Desimone, R. (1985). Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784.CrossRefGoogle ScholarPubMed
Mountcastle, V.B., Steinmetz, M.A. & Romo, R. (1990). Frequency discrimination in the sense of flutter: Psychophysical measurements correlated with postcentral events in behaving monkeys. Journal of Neuroscience 10, 3032–3044.CrossRefGoogle ScholarPubMed
Movshon, J.A., Adelson, E.H., Gizzi, M.S. & Newsome, W.T. (1985). The analysis of moving visual patterns. In Pattern Recognition Mechanisms, ed. Chagas, C., Gattass, R. & Gross, C., pp. 117–151. New York: Springer-Verlag.CrossRefGoogle Scholar
Newsome, W.T., Britten, K.H., Movshon, J.A. & Shadlen, M. (1989). Single neurons and the perception of visual motion. In Neural Mechanisms of Visual Perception. Proceedings of the Retina Research Foundation, ed. Lam, D.M.-K. & Gilbert, C.D., pp. 171–198. The Woodlands, Texas: Portfolio Publishing Company.Google Scholar
Newsome, W.T. & Paré, E.B. (1988). A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience 8, 2201–2211.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H. & Komatsu, H. (1988). Relation of cortical areas MT and MST to pursuit eye movements. 11. Differentiation of retinal from extraretinal inputs. Journal of Neurophysiology 60, 604–620.Google Scholar
Salzman, C.D., Murasuoi, C.M., Britten, K.H. & Newsome, W.T. (1992). Microstimulation in visual area MT: Effects on direction discrimination performance. Journal of Neuroscience 12, 2331–2355.CrossRefGoogle ScholarPubMed
Schiller, P. (1993). The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey. Visual Neuroscience 10, 717–746.CrossRefGoogle ScholarPubMed
Shadlen, M.N., Britten, K.H., Newsome, W.T. & Movshon, J.A. (1996). A computational analysis of the relationship between neuronal and behavioral responses to visual motion. Journal of Neuroscience (accepted pending revisions).CrossRefGoogle ScholarPubMed
Sinclair, R.J. & Burton, H. (1991). Tactile discrimination of gratings: Psychophysical and neural correlates in human and monkey. Somatosensory and Motor Research 8, 241–248.CrossRefGoogle Scholar
Tolhurst, D.J., Movshon, J.A. & Dean, A.F. (1983). The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Research 23, 775–785.CrossRefGoogle Scholar
Ungerleider, L.G. & Mishkin, M. (1979). The striate projection in the superior temporal sulcus of Macaca mulatta: Location and topographic organization. Journal of Comparative Neurology 188, 347–366.CrossRefGoogle ScholarPubMed
Vallbo, A.B. & Johannson, R.S. (1976). Skin mechanoreceptors in the human hand: Neural and psychophysical thresholds. In Active Touch: The Mechanisms of Recognition of Objects by Manipulation, ed. Gordon, G., pp. 29–54. New York: Oxford.Google Scholar
Van Essen, D.C., Maunsell, J.H.R. & Bixby, J.L. (1981). The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic representation. Journal of Comparative Neurology 199, 293–326.CrossRefGoogle Scholar
Vogels, R. & Orban, G.A. (1991). Quantitative study of striate single unit responses in monkeys performing an orientation discrimination task. Experimental Brain Research 84, 1–11.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. Journal of Physiology 236, 549–573.CrossRefGoogle ScholarPubMed
Zohary, E., Celebrini, S., Britten, K.H., Newsome, W.T. (1994). Neuronal plasticity that underlies improvement in perceptual performance. Science 263, 1289–1292.Google Scholar