We address active sensation in the context of the tactile localization of objects, with an ultimate goal to decode how a perception is converted into a motor act. Our approach is to map the transformation of sensory input within the closed loops of the vibrissa sensorimotor system, in which animals sweep long hairs or vibrissae rhythmically through the space that surrounds their head,. The focus of the proposed new experiments are to delineate the control of brainstem nuclei, both sensory nuclei that transform input sensations and motor nuclei that direct the sensors, by descending cortical projections. Such control is of general relevance to all mammalian sensorimotor systems. The nested, closed loop structure of the rodent vibrissa system is a model for sensorimotor control in mammals up through primates. As a focus for scientific investigation and progress in both computational and health related issues, the vibrissa system enjoys a significant data base of anatomical and electrophysiological data, is compatible with standard molecular and physiological tools, and is amenable to a studies with awake behaving animals, albeit with a reduced behavioral repertoire compared to primates. The proposed experiments involve the cortical activation of brainstem nuclei electrical and optical based physiological and anatomical studies with awake, trained rodents. We begin at the sensory end. 1) Does feedback from primary sensory cortex to brainstem nuclei alter the sensory response? Centrifugal fibers from sensory cortex project to integrative sensory neurons in the brainstem. We will determine if and how this feedback path modulates the gain of the reafferent signal of sensor motion, a basic aspect of proprioception. This may be used, based on our past work, to code touch in terms of coordinates that are normalized to the region of interest. More generally, this work addresses """"""""gain of function"""""""" through high-level control. We next consider an essential missing module in the vibrissa sensorimotor circuit: Where are the brainstem nuclei that drive rhythmic whisking? We ask: 2) Does the rhythm pattern generator of breathing control whisking as well? We ask if the rhythmic generator for breathing acts as a central clock, or if breathing and whisking have independent rhythmic generators that phase-lock under different conditions. This query bears on the general coordination of orofacial behaviors. We then build on this effort and ask: 3) Does feedback from motor cortex control the region of interest of rhythmic whisking? The interpretation of touch in neural pathways depends on how the region of interest that shape vibrissa movements are regulated. We will determine how the slowly varying signals observed in motor cortex are used to guide the range of motion set by brainstem motor nuclei. This query bears on the general issue of coordinating motor output on multiple time-scales. Our data may lead to fundamental concepts in signaling and circuitry in the normal state as well as dysfunction states.

Public Health Relevance

We study how sensory input is processed when the sensors themselves are moving, as is common to feeling, through active touch, and seeing, through eye and head movements. Our investigations make use of the rodent vibrissa system: these animals sweep long hairs through space as they search for nearby objects and conspecifics. Our proposed studies hold two promises: One is to understand how mammals control motor output based on sensory input. The second is to understand how orofacial behaviors, such as chewing, swallowing, breathing, and, in the rodent, whisking, are synchronized. This is essential to well-being, as misplaced signaling leads to orofacial myofunctional disorders.

Agency
National Institute of Health (NIH)
Institute
National Institute of Neurological Disorders and Stroke (NINDS)
Type
Research Project (R01)
Project #
5R01NS058668-06
Application #
8653623
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Gnadt, James W
Project Start
2007-03-01
Project End
2018-04-30
Budget Start
2014-05-01
Budget End
2015-04-30
Support Year
6
Fiscal Year
2014
Total Cost
$325,343
Indirect Cost
$108,781
Name
University of California San Diego
Department
Type
Other Domestic Higher Education
DUNS #
804355790
City
La Jolla
State
CA
Country
United States
Zip Code
92093
McElvain, Lauren E; Friedman, Beth; Karten, Harvey J et al. (2018) Circuits in the rodent brainstem that control whisking in concert with other orofacial motor actions. Neuroscience 368:152-170
Kurnikova, Anastasia; Moore, Jeffrey D; Liao, Song-Mao et al. (2017) Coordination of Orofacial Motor Actions into Exploratory Behavior by Rat. Curr Biol 27:688-696
Bellavance, Marie-Andrée; Takatoh, Jun; Lu, Jinghao et al. (2017) Parallel Inhibitory and Excitatory Trigemino-Facial Feedback Circuitry for Reflexive Vibrissa Movement. Neuron 95:673-682.e4
Knutsen, Per M; Mateo, Celine; Kleinfeld, David (2016) Precision mapping of the vibrissa representation within murine primary somatosensory cortex. Philos Trans R Soc Lond B Biol Sci 371:
Deschênes, Martin; Kurnikova, Anastasia; Elbaz, Michael et al. (2016) Circuits in the Ventral Medulla That Phase-Lock Motoneurons for Coordinated Sniffing and Whisking. Neural Plast 2016:7493048
Deschênes, Martin; Takatoh, Jun; Kurnikova, Anastasia et al. (2016) Inhibition, Not Excitation, Drives Rhythmic Whisking. Neuron 90:374-87
Kleinfeld, David; Deschênes, Martin; Ulanovsky, Nachum (2016) Whisking, Sniffing, and the Hippocampal ?-Rhythm: A Tale of Two Oscillators. PLoS Biol 14:e1002385
Aljadeff, Johnatan; Lansdell, Benjamin J; Fairhall, Adrienne L et al. (2016) Analysis of Neuronal Spike Trains, Deconstructed. Neuron 91:221-59
Haidarliu, Sebastian; Kleinfeld, David; Deschênes, Martin et al. (2015) The Musculature That Drives Active Touch by Vibrissae and Nose in Mice. Anat Rec (Hoboken) 298:1347-58
Deschênes, Martin; Haidarliu, Sebastian; Demers, Maxime et al. (2015) Muscles involved in naris dilation and nose motion in rat. Anat Rec (Hoboken) 298:546-53

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