Congruent neuronal modulation across competing actions challenges the role of the substantia nigra in action selection

Abstract

The basal ganglia are involved in the control of movement, but their exact role is unclear. Paradoxically, most of the inhibitory projection neurons in the main output nuclei increase firing around the time of movement; only a small fraction decrease firing. This antagonistic activity pattern could subserve action selection, with the small "decrease" population selectively disinhibiting the desired movement, and the larger "increase" population inhibiting competing movements. The action-selection hypothesis makes an implicit assumption: neurons that decrease firing to disinhibit a specific action should increase firing to inhibit that action when a different action is desired. To test this hypothesis, we recorded projection neurons in the substantia nigra pars reticulata (SNr) of mice trained to alternate between two different types of movements. Many SNr neurons showed a "ramping" pattern of pre-movement firing-rate modulation, with most neurons increasing firing, consistent with previous findings. However, contrary to the action-selection model, the overwhelming majority of SNr neurons exhibited congruent modulation between the competing actions, either increasing or decreasing their firing rates for both actions; only a small fraction of neurons exhibited opposite signs of modulation. Similar results were observed among SNr neurons identified as projecting to the arm or orofacial zones of motor superior colliculus. In addition, brief pauses in SNr firing outside explicit operant tasks were not accompanied by stereotyped movements. Our results are not easily reconciled with simple antagonistic mechanisms for action selection in the basal ganglia output nuclei. We also found that ramping activity in SNr neurons typically began hundreds of ms before self-timed and spontaneous movements, in contrast to previous findings suggesting that basal ganglia output is modulated too late to be involved in movement initiation. Our findings suggest constraints - and raise new questions - about the role of the basal ganglia in movement initiation and action selection.