Self-Generated Movements with “Unexpected” Sensory Consequences

Abstract

SUMMARY The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6–10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep—a behavioral state that predominates in early infancy [12–16]—neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected.

Developmental Neuroscience: How Twitches Make Sense

“…In their simulations, each embryo 'developed' species-typical motor patterns without the need for any explicit instructions. Like the results of Tiriac et al [10], these simulations underscore the importance of spontaneous movements like twitches during development: they are critical developmental processes that allow for adaptive and precise circuit construction without the need for a blueprint.…”

“…Overall, the findings of Tiriac et al [10] suggest that twitches are a special form of self-generated movementthey are treated as unexpected movements from the outside and the neural signal produced by these movements are, thus, not cancelled out. This being the case, they could be used to guide the development of sensorimotor neural circuits, but there is little direct evidence to date that twitches per se are necessary for the formation of sensorimotor maps in the brain.…”

“…Critically, Tiriac et al [10] pharmacologically activated lumbar-spinal neurons to produce movements (regardless of state) and the same sensory-related M1 activity was evident as it was for sleep twitches. That is, when the movement was initiated locally to the spinal cord, there was no canceling of the sensory signal.…”

“…Tiriac et al [10] addressed this puzzle head on by investigating the sensory-related neural activity generated by sleep twitches. The authors recorded proprioceptive sensory responses -those related to joints and tendons -in the hindlimb region of primary motor cortex (M1) of 8-10-day-old rat pups.…”

The developmental origins of spatial navigation: Are we headed in the right direction?

“…These jerky movements of the limbs generate sensory feedback that, in turn, provides substantial activation to the developing nervous system. This twitch-related activity is ideally suited to participate in the self-organization of sensorimotor neural circuits [11,12]. Twitch-related feedback from skeletal muscles—including the nuchal muscle, which controls movements of the head—is conveyed successively to the spinal cord, medulla, thalamus, and sensorimotor cortex.…”