Conventional theories assume that control of visually-guided movements occurs primarily in the cerebral cortex, and involves target detection in visual cortex, integration of target location and body configuration in parietal cortex, and command signal generation in motor cortex that drives motoneurons and thereby muscles. Here we present an alternative perspective on human visually-guided movement, inspired by the fact that the capacity to produce fast and accurate visually-guided movements emerged at a primitive stage of animal evolution [Cisek P (2020), Philos Trans R Soc Lond B Biol Sci 377]. Indeed, despite lacking a cerebral cortex, vertebrates such as frogs and archerfish can produce impressive feats of spatially accurate, visually-guided targeting of prey. Critically, the core subcortical brain structures used for prey capture by lower vertebrates have been phylogenetically conserved in humans.
This presentation will describe our recent work that documents reaching behaviour that is strikingly suggestive of subcortical control. We show that target-directed and coordinated activation of multiple muscles can occur within 100 ms of target presentation, that this rapid muscle activation is enhanced by multisensory inputs and task predictability, and that the activity is associated with modulation of corticospinal excitability within 70 ms of target presentation. We propose that these observations are the signature of a fast, subcortical visuomotor pathway through the superior colliculus and brainstem reticular formation that bypasses motor cortex. The functional properties of the responses suggest the possibility that subcortical circuits represent the core hub of the reach control system, which integrates cortical and sensory sensory inputs to generate control outputs to the spinal interneurons and motoneurons. These ideas have important implications for development of neuroprostheses, neuro-rehabilitiation, and design of human-machine interfaces.