Neural correlates of conflict resolution between automatic and volitional actions by basal ganglia

Authors

  • Masayuki Watanabe,

    1. Centre for Neuroscience Studies, Queen’s University, Kingston, ON, Canada K7L3N6
    2. CIHR Group in Sensory-Motor Integration, Queen’s University, Kingston, ON, Canada
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  • Douglas P. Munoz

    1. Centre for Neuroscience Studies, Queen’s University, Kingston, ON, Canada K7L3N6
    2. CIHR Group in Sensory-Motor Integration, Queen’s University, Kingston, ON, Canada
    3. Department of Physiology, Queen’s University, Kingston, ON, Canada
    4. Department of Psychology, Queen’s University, Kingston, ON, Canada
    5. Department of Medicine, Queen’s University, Kingston, ON, Canada
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Dr D. P. Munoz, 1Centre for Neuroscience Studies, as above.
E-mail: doug_munoz@biomed.queensu.ca

Abstract

A dominant basal ganglia (BG) model consists of two functionally opposite pathways: one facilitates motor output and the other suppresses it. Although this idea was originally proposed to account for motor deficits, it has been extended recently also to explain cognitive deficits. Here, we employed the antisaccade paradigm (look away from a stimulus) to address the role of the caudate nucleus, the main BG input stage where the two pathways diverge, in conflict resolution. Using single neuron recordings in awake monkeys, we identified the following three groups of neurons. The first group of neurons showed activity consistent with sensory-driven (automatic) saccades toward a contralateral visual stimulus. The second group of neurons showed activity consistent with internally driven (volitional) saccades toward the contralateral side regardless of stimulus locations. The third group of neurons showed similar firing characteristics with the second group of neurons, except that their preferred saccade direction was ipsilateral. The activity of the three groups of neurons was correlated with behavioral outcome. Based on these findings, we suggest the following hypothesis: the first and second groups of neurons encoding automatic and volitional saccades, respectively, might give rise to the facilitation (direct) pathway and promote saccades toward the opposite directions, which creates a response conflict. This conflict could be resolved by the third group of caudate neurons, which might give rise to the suppression (indirect) pathway and attenuate inappropriate saccade commands toward the stimulus.

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