Abstract
We examined how the relationship between neuronal activity and behavior evolved over time during a motion-detection task. Recording from two regions of visual cortex that process motion, the middle temporal (MT) and ventral intraparietal (VIP) areas, we used the time it took subjects to detect a motion stimulus to evaluate the dynamics of the underlying neuronal signals. Single-neuron activity was correlated with stimulus detection and reaction time (RT) in both areas. The rising edge of the population response from both areas was highly predictive of RT using a simple threshold-detection model. The time course of the population responses, however, differed between MT and VIP. For MT, the onset of the neuronal response was relatively constant, whereas for VIP the onset of the neuronal responses increased with RT. In contrast to previous studies, we found that single neurons were not reliable detectors of the motion signal when constrained by realistic detection times.
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References
Tolhurst, D.J., Movshon, J.A. & Dean, A.F. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res. 23, 775–785 (1983).
Parker, A. & Hawken, M. Capabilities of monkey cortical cells in spatial resolution tasks. J. Opt. Soc. Am. A 2, 1101–1114 (1985).
Geisler, W.S. & Albrecht, D.G. Visual cortex neurons in monkeys and cats: detection, discrimination, and identification. Vis. Neurosci. 14, 897–919 (1997).
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745–4765 (1992).
Croner, L.J. & Albright, T.D. Segmentation by color influences responses of motion-sensitive neurons in the cortical middle temporal visual area. J. Neurosci. 19, 3935–3951 (1999).
Prince, S.J.D., Pointon, A.D., Cumming, B.G. & Parker, A.J. The precision of single neuron responses in cortical area V1 during stereoscopic depth judgments. J. Neurosci. 20, 3387–3400 (2000).
Mountcastle, V.B., Steinmetz, M.A. & Romo, R. Frequency discrimination in the sense of flutter: psychophysical measurements correlated with post-central events in behaving monkeys. J. Neurosci. 10, 3032–3044 (1990).
Parker, A.J. & Newsome, W.T. Sense and the single neuron: probing the physiology of perception. Annu. Rev. Neurosci. 21, 227–277 (1998).
Meyer, D.E., Osman, A.M., Irwin, D.E. & Yantis, S. Modern mental chronometry. Biol. Psychol. 26, 3–67 (1988).
Luce, R.D. Response Times: Their Role in Inferring Elementary Mental Organization (eds. Broadbent, D. E. et al.) (Clarendom Press, Oxford, 1986).
Thompson, K.G., Hanes, D.P., Bichot, N.P. & Schall, J.D. Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. J. Neurophysiol. 76, 4040–4055 (1996).
Cook, E.P. & Maunsell, J.H.R. Attentional modulation of behavioral performance and neuronal responses in middle temporal and ventral intraparietal areas of macaque monkey. J. Neurosci. 22, 1994–2004 (2002).
Celebrini, S. & Newsome, W.T. Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. J. Neurosci. 14, 4109–4124 (1994).
Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996).
Dodd, J.V., Krug, K., Cumming, B.G. & Parker, A.J. Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT. J. Neurosci. 21, 4809–4821 (2001).
Shadlen, M.N. & Newsome, W.T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916–1936 (2001).
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. Responses of neurons in macaque MT to stochastic motion signals. Vis. Neurosci. 10, 1157–1169 (1993).
Bair, W. & Koch, C. Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput. 8, 1185–1202 (1996).
Buracas, G.T., Zador, A.M., DeWeese, M.R. & Albright, T.D. Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20, 959–969 (1998).
Hanes, D.P. & Schall, J.D. Neural control of voluntary movement initiation. Science 274, 427–430 (1996).
Reddi, B.A. & Carpenter, R.H. The influence of urgency on decision time. Nat. Neurosci. 3, 827–830 (2000).
Schall, J.D. & Thompson, K.G. Neural selection and control of visually guided eye movements. Annu. Rev. Neurosci. 22, 241–259 (1999).
Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).
Shadlen, M.N. & Newsome, W.T. Motion perception: seeing and deciding. Proc. Natl. Acad. Sci. USA 93, 628–633 (1996).
Gratton, G., Coles, M.G., Sirevaag, E.J., Eriksen, C.W. & Donchin, E. Pre- and post-stimulus activation of response channels: a psychophysiological analysis. J. Exp. Psychol. Hum. Percept. Perform. 14, 331–344 (1988).
Schmolesky, M.T. et al. Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272–3278 (1998).
Raiguel, S.E., Lagae, L., Gulyas, B. & Orban, G.A. Response latencies of visual cells in macaque areas V1, V2 and V5. Brain Res. 493, 155–159 (1989).
Shadlen, M.N., Britten, K.H., Newsome, W.T. & Movshon, J.A. A computational analysis of the relationship between neuronal and behavioral responses to visual motion. J. Neurosci. 16, 1486–1510 (1996).
Bair, W., Zohary, E. & Newsome, W.T. Correlated firing in macaque visual area MT: time scales and relationship to behavior. J. Neurosci. 21, 1676–1697 (2001).
Mazurek, M.E. & Shadlen, M.N. Limits to the temporal fidelity of cortical spike rate signals. Nat. Neurosci. 5, 463–471 (2002).
Lamarre, Y., Spidalieri, G. & Lund, J.P. Patterns of muscular and motor cortical activity during a simple arm movement in the monkey. Can. J. Physiol. Pharmacol. 59, 748–756 (1981).
Townsend, J.T. & Ashby, F.G. The Stochastic Modeling of Elementary Psychological Processes (Cambridge University Press, Cambridge, 1983).
Usher, M. & McClelland, J.L. The time course of perceptual choice: the leaky, competing accumulator model. Psychol. Rev. 108, 550–592 (2001).
Maunsell, J.H.R. & Van Essen, D.C. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J. Neurosci. 3, 2563–2586 (1983).
Colby, C.L., Duhamel, J.R. & Goldberg, M.E. Ventral intraparietal area of the macaque: anatomic location and visual response properties. J. Neurophysiol. 69, 902–914 (1993).
Gibson, J.R. & Maunsell, J.H.R. Sensory modality specificity of neural activity related to memory in visual cortex. J. Neurophysiol. 78, 1263–1275 (1997).
Robinson, D.A. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Eng. 10, 137–145 (1963).
Judge, S.J., Richmond, B.J. & Chu, F.C. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision. Res. 20, 535–538 (1980).
Van Essen, D.C., Maunsell, J.H.R. & Bixby, J.L. The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties and topographic organization. J. Comp. Neurol. 199, 293–326 (1981).
Efron, B. & Tibshirani, R. An Introduction to the Bootstrap (Chapman and Hall, New York, 1993).
Acknowledgements
This work is supported by the National Institutes of Health Grant R01 EY05911. J.H.R.M. is an Investigator with the Howard Hughes Medical Institute. We thank W. Bosking, C. Boudreau, J. DiCarlo, G. Ghose, C. Hocker and T. Yang for helpful discussions on all aspects of this project, and D. Murray and T. Williford for expert technical assistance.
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Cook, E., Maunsell, J. Dynamics of neuronal responses in macaque MT and VIP during motion detection. Nat Neurosci 5, 985–994 (2002). https://doi.org/10.1038/nn924
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DOI: https://doi.org/10.1038/nn924
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