Modulation of neuronal activity by target uncertainty

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Access through your institution Buy or subscribe Visual scenes are composed of many elements and although we can appreciate a scene as a whole, we can only move our eyes to one element of


the scene at a time. As visual scenes become more complex, the number of potential targets in the scene increases, and the uncertainty that any particular one will be selected for an eye


movement also increases. How motor systems accommodate this target uncertainty remains unknown. The activities of neurons in both the cerebral cortex1,2,3,4,5 and superior colliculus6,7,8


are modulated by this selection process. We reasoned that activity associated with target uncertainty should be evident in the saccadic motor system at the final stages of neural processing,


in the superior colliculus9,10. By systematically changing the number of stimuli from which a selection must be made and recording from superior colliculus neurons, we found that as the


target uncertainty increased, the neural activity preceding target selection decreased. These results indicate that neurons within the final common pathway for movement generation are active


well in advance of the selection of a particular movement. This early activity varies with the probability that a particular movement will be selected. The intermediate layers of the


superior colliculus receive input from extensive regions of the cerebral cortex and may be regarded as a virtual readout of the cerebral cortex for the control of eye movements. Moreover,


prelude burst neurons and buildup neurons in the superior colliculus increase their activity with the selection and preparation of a movement long before the activity closely related to


saccade generation6,7,8. We determined the effect of target uncertainty on buildup neurons in awake monkeys in two ways. In the first experiment, we manipulated target uncertainty by


presenting a different number of possible targets to monkeys on different trials. In a second experiment, we manipulated target uncertainty by presenting the same visual array of possible


targets on every trial and varying the probability that any one of the stimuli would be selected for a saccadic eye movement. In both experiments we found that buildup neurons decreased


their activity as uncertainty increased. This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal


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REFERENCES * Maunsell, J. H. R. The brain's visual world: representation of visual targets in cerebral cortex. _Science_ 270, 764–769 (1995). Google Scholar  * Schall, J. D. &


Hanes, D. P. Neural basis of saccade target selection in frontal eye field during visual search. _Nature_ 366, 467–469 (1993). Article  ADS  CAS  Google Scholar  * Schall, J. D., Hanes, D.


P., Thompson, K. G. & King, D. J. Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation. _J. Neurosci._ 15, 6905–6918 (1995). Google Scholar  *


Kusunoki, M. & Goldberg, M. E. Responses of parietal visual neurons to attentionally significant stable objects. _Soc. Neurosci. Abstr._ 21, 665 (1995). Google Scholar  * Shadlen, M. N.


& Newsome, W. T. Motion perception: Seeing and deciding. _Proc. Natl Acad. Sci. USA_ 93, 628–633 (1996). Google Scholar  * Glimcher, P. W. & Sparks, D. L. Movement selection in


advance of action in the superior colliculus. _Nature_ 355, 542–545 (1992). Article  ADS  CAS  Google Scholar  * 7. Munoz, D. P. & Wurtz, R. H. Saccade-related activity in monkey


superior colliculus. I. Characteristics of burst and buildup cells. _J. Neurophysiol._ 73, 2313–2333 (1995). Google Scholar  * Kustov, A. A. & Robinson, D. L. Shared neural control of


attentional shifts and eye movements. _Nature_ 384, 74–77 (1996). Article  ADS  CAS  Google Scholar  * Sparks, D. L. & Hartwich-Young, R. in _The Neurobiology of Saccadic Eye Movements,


Reviews of Oculomotor Research_, VOL. III(eds Wurtz, R. H. &Goldberg, M. E.) 213–256 (Elsevier, Amsterdam, (1989)). Google Scholar  * Miyashita, N. & Hikosaka, O. Minimal synaptic


delay in the saccadic output pathway of the superior colliculus studied in awake monkey. _Exp. Brain Res._ 112, 187–196 (1996). Google Scholar  * Moran, J. & Desimone, R. Selective


attention gates visual processing in extrastriate cortex. _Science_ 229, 782–784 (1985). Google Scholar  * Treue, S. & Maunsell, J. H. Attentional modulation of visual motion processing


in cortical areas MT and MST. _Nature_ 382, 539–541 (1996). Article  ADS  CAS  Google Scholar  * Motter, B. C. Focal attention produces spatially selective processing in visual cortical


areas V1, V2, and V4 in the presence of competing stimuli. _J. Neurophysiol._ 70, 909–919 (1993). Google Scholar  * Treisman, A. M. & Gelade, G. Afeature-integration theory of attention.


_Cogn. Psych._ 12, 97–136 (1980). Google Scholar  * Bravo, M. J. & Makayama, K. The role of attention in different visual-search tasks. _Percept. Psychophys._ 51, 465–472 (1992). Google


Scholar  * Goldberg, M. E. & Wurtz, R. H. Activity of superior colliculus in behaving monkeys. II. Effect of attention on neuronal responses. _J. Neurophysiol._ 35, 560–574 (1972).


Google Scholar  Download references ACKNOWLEDGEMENTS We thank the Laboratory of Diagnostic Radiology Research for magnetic resonance images. We thank J. Steinberg for secretarial assistance


preparing the manuscript. We gratefully acknowledge the critical comments made on previous versions by J. Gottlieb and M. A. Sommer. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Laboratory


of Sensorimotor Research, National Eye Institute, Bethesda, 20892-4435, Maryland, USA Michele A. Basso & Robert H. Wurtz Authors * Michele A. Basso View author publications You can also


search for this author inPubMed Google Scholar * Robert H. Wurtz View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to


Michele A. Basso. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Basso, M., Wurtz, R. Modulation of neuronal activity by target uncertainty. _Nature_


389, 66–69 (1997). https://doi.org/10.1038/37975 Download citation * Received: 30 January 1997 * Accepted: 17 June 1997 * Issue Date: 04 September 1997 * DOI: https://doi.org/10.1038/37975


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