Understanding the phenomena of adult brain plasticity, triggered either by injury to the nervous system or by learning new skills, will likely provide a fundamental step towards establishing newtherapies for treating neurological disorders. However, the circuit mechanisms underlying neural plasticity remain mostly unknown. Elucidating this question is the central focus of our research program. During the previous funding period, we demonstrated that corticothalamic (CT) projections, originating in the rat primary somatosensory cortex (S1), significantly contribute to the definition of the spatiotemporal structure of the receptive fields of neurons in the ventroposterior medial nucleus (VPM) of the thalamus. Our data also revealed that, following a peripheral deafferentation, CT projections contribute to the ability of VPM neurons to exhibit plastic reorganization. Interestingly, we also found that both the magnitude and duration of tactile responses of S1 and VPM neurons change according to the animal's behavioral state. Together, these results indicate that sensory representations within the thalamocortical loop (TCL) are plastic, dynamically modulated constructs, which emerge from the asynchronous convergence of multiple ascending and descending excitatory and inhibitory afferents. Most recently, we have reported that tactile signal processing across S1 layers is fundamentally different during active versus passive tactile stimulation. For example, task-related modulation of firing rates can begin before tactile stimulation. To date, however, the circuit mechanisms to account for such gross changes in response properties remain largely unknown. Here we propose to test the hypothesis that, during active tactile exploration, multiple corticocortical and corticothalamic projections dynamically modulate the magnitude and duration of tactile responses of S1 and VPM neurons respectively, in order to optimize the discrimination of tactile stimuli. We also propose that learning of a new tactile discrimination task enhances the effects of these "top-down" projections on the TCL. In this project we propose to focus on two major inputs to S1: primary motor cortex (M1) and contralateral S1. Focal reversible inactivation of M1 or S1 would reveal their contribution to TCL responses during motivated discrimination behavior. Chronic recording methods would allow us to follow changes in response statistics over the course of learning the discrimination task. Moveable electrode technology, pioneered in our lab, enables us to correlate the layer structure of S1 responses with anatomically known projections. These experiments offer a window into the nervous system as it dynamically integrates widely distributed neural signals to carry out a non-trivial sensory-motor task, and promise significant revisions to current models of sensation based predominantly on electrophysiological responses to passively delivered stimuli.

Agency
National Institute of Health (NIH)
Institute
National Institute of Dental & Craniofacial Research (NIDCR)
Type
Research Project (R01)
Project #
5R01DE011451-14
Application #
7994836
Study Section
Somatosensory and Chemosensory Systems Study Section (SCS)
Program Officer
Kusiak, John W
Project Start
1994-09-01
Project End
2012-12-31
Budget Start
2011-01-01
Budget End
2012-12-31
Support Year
14
Fiscal Year
2011
Total Cost
$359,285
Indirect Cost
Name
Duke University
Department
Biology
Type
Schools of Medicine
DUNS #
044387793
City
Durham
State
NC
Country
United States
Zip Code
27705
Hartmann, Konstantin; Thomson, Eric E; Zea, Ivan et al. (2016) Embedding a Panoramic Representation of Infrared Light in the Adult Rat Somatosensory Cortex through a Sensory Neuroprosthesis. J Neurosci 36:2406-24
Pais-Vieira, Miguel; Chiuffa, Gabriela; Lebedev, Mikhail et al. (2015) Building an organic computing device with multiple interconnected brains. Sci Rep 5:11869
Pais-Vieira, Miguel; Kunicki, Carolina; Tseng, Po-He et al. (2015) Cortical and thalamic contributions to response dynamics across layers of the primary somatosensory cortex during tactile discrimination. J Neurophysiol 114:1652-76
Thomson, Eric; Lou, Jason; Sylvester, Kathryn et al. (2014) Basal forebrain dynamics during a tactile discrimination task. J Neurophysiol 112:1179-91
Pais-Vieira, Miguel; Lebedev, Mikhail A; Wiest, Michael C et al. (2013) Simultaneous top-down modulation of the primary somatosensory cortex and thalamic nuclei during active tactile discrimination. J Neurosci 33:4076-93
Thomson, Eric E; Carra, Rafael; Nicolelis, Miguel A L (2013) Perceiving invisible light through a somatosensory cortical prosthesis. Nat Commun 4:1482
Pais-Vieira, Miguel; Lebedev, Mikhail; Kunicki, Carolina et al. (2013) A brain-to-brain interface for real-time sharing of sensorimotor information. Sci Rep 3:1319
Vasconcelos, Nivaldo; Pantoja, Janaina; Belchior, Hindiael et al. (2011) Cross-modal responses in the primary visual cortex encode complex objects and correlate with tactile discrimination. Proc Natl Acad Sci U S A 108:15408-13
Freire, Marco Aurelio M; Morya, Edgard; Faber, Jean et al. (2011) Comprehensive analysis of tissue preservation and recording quality from chronic multielectrode implants. PLoS One 6:e27554
Zhang, Hao; Lin, Shih-Chieh; Nicolelis, Miguel A L (2011) A distinctive subpopulation of medial septal slow-firing neurons promote hippocampal activation and theta oscillations. J Neurophysiol 106:2749-63

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