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The Journal of Neuroscience, September 26, 2007, 27(39):10608-10620; doi:10.1523/JNEUROSCI.5279-06.2007

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Behavioral/Systems/Cognitive
Neuronal Activity in the Primary Somatosensory Thalamocortical Loop Is Modulated by Reward Contingency during Tactile Discrimination

Janaina Pantoja,¹ Sidarta Ribeiro,² Michael Wiest,^1,5 Ernesto Soares,¹ Damien Gervasoni,⁶ Nelson A. M. Lemos,² and Miguel A. L. Nicolelis^1,2,3,4,5,7

¹Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710, ²Edmond and Lily Safra International Institute of Neuroscience of Natal, Natal, RN 59066-060, Brazil, Departments of ³Psychology and Neuroscience and ⁴Biomedical Engineering and ⁵Duke University Center for Neuroengineering, Duke University, Durham, North Carolina 27710, ⁶Centre National de la Recherche Scientifique, Université Claude Bernard, 69372 Lyon, France, and ⁷Brain and Mind Institute at École Polytechnique Féderale de Lausanne, 1015 Lausanne, Switzerland

Correspondence should be addressed to Miguel A. L. Nicolelis, Department of Neurobiology, Duke University Medical Center, Box 3209, Durham, NC 27710. Email: nicoleli{at}neuro.duke.edu

Delayed-response sensory discrimination is believed to require primary sensory thalamus and cortex for early stimulus identification and higher-order forebrain regions for the late association of stimuli with rewarded motor responses. Here we investigate neuronal responses in the rat primary somatosensory cortex (S1) and ventral posterior medial nucleus of the thalamus (VPM) during a tactile discrimination task that requires animals to associate two different tactile stimuli with two corresponding choices of spatial trajectory to be rewarded. To manipulate reward expectation, neuronal activity observed under regular reward contingency (CR) was compared with neuronal activity recorded during freely rewarded (FR) trials, in which animals obtained reward regardless of their choice of spatial trajectory. Across-trial firing rates of S1 and VPM neurons varied according to the reward contingency of the task. Analysis of neuronal ensemble activity by an artificial neural network showed that stimulus-related information in S1 and VPM increased from stimulus sampling to reward delivery in CR trials but decreased to chance levels when animals performed FR trials, when stimulus discrimination was irrelevant for task execution. Neuronal ensemble activity in VPM was only correlated with task performance during stimulus presentation. In contrast, S1 neuronal activity was highly correlated with task performance long after stimulus removal, a relationship that peaked during the 300 ms that preceded reward delivery. Together, our results indicate that neuronal activity in the primary somatosensory thalamocortical loop is strongly modulated by reward contingency.

Key words: somatosensory; tactile; reward; memory; thalamus; ANN; behavior; cortex

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Received June 26, 2006; revised Aug. 10, 2007; accepted Aug. 14, 2007.

Correspondence should be addressed to Miguel A. L. Nicolelis, Department of Neurobiology, Duke University Medical Center, Box 3209, Durham, NC 27710. Email: nicoleli{at}neuro.duke.edu

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