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  4. HOW THE BRAIN CONTROLS THE TONGUE

HOW THE BRAIN CONTROLS THE TONGUE

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Ito_cornellgrad_0058F_14738.pdf (32.65 MB)
Supp. Video 2.1 Cue-evoked licks and water retrieval licks exhibited distinct kinematics.mp4 (17.91 MB)
Supp. Video 2.2 Spout contact altered kinematics of subsequent licks.mp4 (40.13 MB)
Supp. Video 2.3 ALM inactivation at cue onset abolished the generation of corrective submovements.mp4 (7.18 MB)
Supp. Video 2.4 Example cue-evoked and water retrieval licks from a session with left spout position.mp4 (15.66 MB)
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Permanent Link(s)
http://doi.org/10.7298/vev3-2z16
https://hdl.handle.net/1813/117203
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Cornell Theses and Dissertations
Author
Ito, Brendan
Abstract

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.

Description
200 pages
Supplemental file(s) description: latSC photostimulation reveals a topographic map for lick aiming. Example trials with unilateral latSC photostimulation at 4 sites along the AP axis in latSC. Note that more posterior stimulations in the latSC evoked more lateral protrusions. , Recentering task decouples contact site from spout position. Example recentering trial. On left/right L2 displacement trials, the spout is also moved back to the center position between L3 and L4, evoking right/left nicks at center spout positions., Unilateral latSC inactivation impairs contralateral touch-guided re-aiming. Example trial in the touch-guided lick task with unilateral latSC photoinactivation. , Unilateral ALM or TJM1 inactivation biases licks ipsilaterally, but preserves touch-guided re-aiming. Example trial in the touch-guided lick task with unilateral ALM or TJM1 photoinactivation from L2 contact onset for 250 ms. , Bilateral latSC inactivation halts ongoing licking. Example trial in the touch-guided lick task with bilateral latSC photoinactivation from L2 contact onset for 250 ms. , Lesions of all three lingual cortical areas at once impair lick kinematics while preserving touch-guided re-aiming. Example pre-lesion and post-lesion trial in the touch-guided lick task from a mouse with ALM, TJM1, and TJS1 lesioned. , Bilateral ALM, TJM1, or TJS1 inactivation does not impair touch-guided re-aiming. Example trial in the touch-guided lick task with bilateral ALM, TJM1, or TJS1 photoinactivation from L2 contact onset for 250 ms. , Mice use tactile feedback to re-aim licks. Side and bottom views of the mouse tongue for L1-L5 at full speed and slowed 1/40x, for left, center and right spout displacement trials., Video from a double-step trial in which ALM was inactivated at the moment of L1 spout contact offset. ALM inactivation impaired the generation of corrective submovements and spout contact., Video from a double-step trial, in which the spout was retracted by 1 mm immediately after the offset of the first lick’s spout contact. Note both within-lick and across lick corrections. , ALM inactivation at protrusion (not cue) onset impaired spout contact but not the probability of generating a corrective submovement., Example cue-evoked lick from a session with left spout position in an ALM-inactivated trial. Note that ALM inhibition at cue onset abolished the generation of corrective submovements but did not affect aiming of protrusions., Example cue-evoked and water retrieval licks from a session with left spout position., ALM inactivation at cue onset abolished the generation of corrective submovements. Example of a cue-evoked lick from the same behavioral session as Video 1 with ALM bilaterally photoinhibited. Note absence of CSMs in the tongue tip trajectory. , Spout contact altered kinematics of subsequent licks. Representative example showing the absence of corrective submovements on a water retrieval lick following successful spout contact. , Cue-evoked licks and water retrieval licks exhibited distinct kinematics. Left to right: Raw video, video with tongue labeled by a convolutional neural network, and the estimated tongue tip trajectory during a cue-evoked lick and water retrieval lick..
Date Issued
2024-12
Keywords
Cortex
•
Mechanosensory
•
Motor Control
•
Superior Colliculus
•
Tactile
•
Tongue
Committee Chair
Goldberg, Jesse
Committee Member
Sheehan, Michael
Fetcho, Joseph
Degree Discipline
Neurobiology and Behavior
Degree Name
Ph. D., Neurobiology and Behavior
Degree Level
Doctor of Philosophy
Rights
Attribution-NonCommercial-NoDerivatives 4.0 International
Rights URI
https://creativecommons.org/licenses/by-nc-nd/4.0/
Type
dissertation or thesis
Link(s) to Catalog Record
https://newcatalog.library.cornell.edu/catalog/16921911

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