Cortical neurons multiplex reward-related signals along with sensory and motor information.

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2017-06-13

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Ramakrishnan, Arjun
Byun, Yoon Woo
Rand, Kyle
Pedersen, Christian E
Lebedev, Mikhail A
Nicolelis, Miguel AL

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Abstract

Rewards are known to influence neural activity associated with both motor preparation and execution. This influence can be exerted directly upon the primary motor (M1) and somatosensory (S1) cortical areas via the projections from reward-sensitive dopaminergic neurons of the midbrain ventral tegmental areas. However, the neurophysiological manifestation of reward-related signals in M1 and S1 are not well understood. Particularly, it is unclear how the neurons in these cortical areas multiplex their traditional functions related to the control of spatial and temporal characteristics of movements with the representation of rewards. To clarify this issue, we trained rhesus monkeys to perform a center-out task in which arm movement direction, reward timing, and magnitude were manipulated independently. Activity of several hundred cortical neurons was simultaneously recorded using chronically implanted microelectrode arrays. Many neurons (9-27%) in both M1 and S1 exhibited activity related to reward anticipation. Additionally, neurons in these areas responded to a mismatch between the reward amount given to the monkeys and the amount they expected: A lower-than-expected reward caused a transient increase in firing rate in 60-80% of the total neuronal sample, whereas a larger-than-expected reward resulted in a decreased firing rate in 20-35% of the neurons. Moreover, responses of M1 and S1 neurons to reward omission depended on the direction of movements that led to those rewards. These observations suggest that sensorimotor cortical neurons corepresent rewards and movement-related activity, presumably to enable reward-based learning.

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10.1073/pnas.1703668114

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Ramakrishnan, Arjun, Yoon Woo Byun, Kyle Rand, Christian E Pedersen, Mikhail A Lebedev and Miguel AL Nicolelis (2017). Cortical neurons multiplex reward-related signals along with sensory and motor information. Proc Natl Acad Sci U S A, 114(24). pp. E4841–E4850. 10.1073/pnas.1703668114 Retrieved from https://hdl.handle.net/10161/15773.

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Nicolelis

Miguel Angelo L. Nicolelis

Professor Emeritus of Neurobiology

Miguel Nicolelis, M.D., Ph.D., is the Duke School of Medicine Distinguished Professor of Neuroscience, Duke University Professor of Neurobiology, Biomedical Engineering and Psychology and Neuroscience, and founder of Duke's Center for Neuroengineering. He is the founder and Scientific Director of the Edmond and Lily Safra International Institute for Neuroscience of Natal.  Dr. Nicolelis is also founder of the Walk Again Project, an international consortium of scientists and engineers, dedicated to the development of an exoskeleton device to assist severely paralyzed patients in regaining full body mobility.

Dr. Nicolelis has dedicated his career to investigate how the brains of freely behaving animals encode sensory and motor information. As a result of his studies, Dr. Nicolelis was first to propose and demonstrate that animals and human subjects can utilize their electrical brain activity to directly control neuroprosthetic devices via brain-machine interfaces (BMI).

Over the past 25 years, Dr. Nicolelis pioneered and perfected the development of a new neurophysiological method, known today as chronic, multi-site, multi-electrode recordings. Using this approach in a variety of animal species, as well as in intra-operative procedures in human patients, Dr. Nicolelis launched a new field of investigation, which aims at measuring the concurrent activity and interactions of large populations of single neurons throughout the brain. Through his work, Dr. Nicolelis has discovered a series of key physiological principles that govern the operation of mammalian brain circuits.

Dr. Nicolelis pioneering BMI studies have become extremely influential since they offer new potential therapies for patients suffering from severe levels of paralysis, Parkinson’s disease, and epilepsy. Today, numerous neuroscience laboratories in the US, Europe, Asia, and Latin America have incorporated Dr. Nicolelis' experimental paradigm to study a variety of mammalian neuronal systems. His research has influenced basic and applied research in computer science, robotics, and biomedical engineering. 


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