Early vestibular processing does not discriminate active from passive self-motion if there is a discrepancy between predicted and actual proprioceptive feedback

Abstract

Most of our sensory experiences are gained by active exploration of the world. While the ability to distinguish sensory inputs resulting of our own actions (termed reafference) from those produced externally (termed exafference) is well established, the neural mechanisms underlying this distinction are not fully understood. We have previously proposed that vestibular signals arising from self-generated movements are inhibited by a mechanism that compares the internal prediction of the proprioceptive consequences of self-motion to the actual feedback. Here we directly tested this proposal by recording from single neurons in monkey during vestibular stimulation that was externally produced and/or self-generated. We show for the first time that vestibular reafference is equivalently canceled for self-generated sensory stimulation produced by activation of the neck musculature (head-on-body motion), or axial musculature (combined head and body motion), when there is no discrepancy between the predicted and actual proprioceptive consequences of self-motion. However, if a discrepancy does exist, central vestibular neurons no longer preferentially encode vestibular exafference. Specifically, when simultaneous active and passive motion resulted in activation of the same muscle proprioceptors, neurons robustly encoded the total vestibular input (i.e., responses to vestibular reafference and exafference were equally strong), rather than exafference alone. Taken together, our results show that the cancellation of vestibular reafference in early vestibular processing requires an explicit match between expected and actual proprioceptive feedback. We propose that this vital neuronal computation, necessary for both accurate sensory perception and motor control, has important implications for a variety of sensory systems that suppress self-generated signals.