HOW THE BRAIN CONTROLS THE TONGUE
Effective goal directed behavior requires ongoing movements to be modified in response to unexpected sensory events. For example, if your pinky nicks your coffee cup as you extend your arm to reach for it, you immediately reposition your fingers to grasp and lift it. What are the neural circuits that govern these ‘on-the-fly’ corrections when we make mistakes in our ongoing movements? Traditionally, the neural mechanisms underlying ‘on-the-fly’ corrections have been studied in primates performing forelimb reach tasks. However, many other animal species including giraffes, frogs, chameleons, and rodents, do not reach with their limbs, but rather ‘reach’ with their tongues to achieve similar behavioral goals. What are the neural circuits that guide the control of tongue movements? Despite the importance of the tongue for eating, drinking, and vocalizing, the neural mechanisms underlying precise and accurate tongue control remain poorly understood. The two studies presented in this dissertation are among the first to investigate the neural mechanisms of tongue control in mice, and more broadly, reveal conserved neural circuit principles underlying the control of lingual movements in mice and the control of limb and eye movements in primates and other species. In Chapter 2, I describe the development of the first ever system to track lingual kinematics in 3D with deca-micron millisecond-timescale spatiotemporal precision as mice licked for water from a spout. Inspired by primate reach tasks, I developed a novel behavioral paradigm in which, on randomly interleaved trials, the water spout unexpectedly retracted in the middle of a mouse’s lick bout, causing the tongue to miss the spout on the next lick in the bout. Mice rapidly reacted to spout misses with ‘on-the-fly’ corrective submovements, analogous to those previously observed when primates miss targets during reaching. Remarkably, corrections were implemented within single licks, revealing extremely fast sensorimotor feedback control of the tongue for the first-time. Interestingly, I found that corrective lingual movements in rodents – just like corrective forelimb movements in primates – depended on the motor cortex. Thus, corrective movements during licking in mice resemble, both behaviorally and mechanistically, corrective movements observed in primates performing forelimb reach tasks, revealing a general principle for the role of the motor cortex in reacting to an absence of a predicted event. While Chapter 2 focuses on corrections after misses, Chapter 3 describes how touch is used to guide tongue movements. I created a new behavioral paradigm that elicited unexpected touch events on the tongue surface by subtly moving the spout to the left or right, such that the spout nicked the left or right side of the tongue. Mice used the precise location of these touch events to re-aim the tongue on the next lick in a bout. Surprisingly, I found that touch-guided lingual movements in mice did not depend on the cortex, unlike touch-guided reaching and grasping in primates, but rather the superior colliculus – a brain region known to contain multiple topographic maps of sensory space that is used to orient the head, eyes, and body towards salient sensory stimuli. Incredibly, collicular neurons exhibited spatially precise receptive fields for touch events on different parts of the tongue surface, and tactile representations followed an orderly map of tongue space, with neurons in more posterior collicular areas exhibiting selectivity for more contralateral touch events. Moreover, spatiotemporally precise photoactivations of collicular neurons showed that this map had a motor component, with more posterior photoactivation sites resulting in more contralaterally aimed licks. Thus, just as the superior colliculus is involved in orienting to sensory stimuli in primates and other species, the superior colliculus is involved in ‘orienting’ the tongue to tactile lingual stimuli in mice. Together, through careful decomposition of behavior, these studies reveal general principles for the neural control of movement that are both species- and effector-independent. The motor cortex is critical for reacting to misses – the absence of predicted events. Meanwhile, the superior colliculus is important for orienting effectors to salient sensory events.