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Modulation of neuronal activity by target uncertainty

Nature volume 389, pages 66–69 (1997)Cite this article

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.

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Figure 1: Behavioural task used for separating target uncertainty from target selection.
Figure 2: Decreased neuronal activity with increased uncertainty.
Figure 3: All neurons showed decreased activity with increased uncertainty.
Figure 4: Uncertainty effects persist with individual visual stimuli.

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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.

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  1. Laboratory of Sensorimotor Research, National Eye Institute, Bethesda, 20892-4435, Maryland, USA

    Michele A. Basso & Robert H. Wurtz

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  1. Michele A. Basso
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  2. Robert H. Wurtz
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Correspondence to Michele A. Basso.

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Basso, M., Wurtz, R. Modulation of neuronal activity by target uncertainty. Nature 389, 66–69 (1997). https://doi.org/10.1038/37975

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