Spatiotemporal Tuning of Motor Cortical Neurons for Hand Position and Velocity

• Published in: Journal of neurophysiology 2004-01, Vol.91 (1), p.515-532
• Main Authors: Paninski, Liam, Fellows, Matthew R, Hatsopoulos, Nicholas G, Donoghue, John P
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Behavior, Animal; Electrophysiology; Hand - physiology; Kinesthesis; Macaca; Models, Neurological; Motion Perception - physiology; Motor Cortex - cytology; Motor Cortex - physiology; Motor Neurons - physiology; Motor Skills; Movement - physiology; Primates; Psychomotor Performance - physiology; Pursuit, Smooth - physiology; Reaction Time - physiology; Space Perception - physiology; Time Factors
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00587.2002

1 Center for Neural Science, New York University, New York, New York 10003; 2 Department of Neuroscience, Brown University, Providence, Rhode Island 02912; and 3 Committee on Computational Neuroscience, University of Chicago, Chicago, Illinois 60637 Submitted 22 July 2003; accepted in final form 8 September 2003 A pursuit-tracking task (PTT) and multielectrode recordings were used to investigate the spatiotemporal encoding of hand position and velocity in primate primary motor cortex (MI). Continuous tracking of a randomly moving visual stimulus provided a broad sample of velocity and position space, reduced statistical dependencies between kinematic variables, and minimized the nonstationarities that are found in typical "step-tracking" tasks. These statistical features permitted the application of signal-processing and information-theoretic tools for the analysis of neural encoding. The multielectrode method allowed for the comparison of tuning functions among simultaneously recorded cells. During tracking, MI neurons showed heterogeneity of position and velocity coding, with markedly different temporal dynamics for each. Velocity-tuned neurons were approximately sinusoidally tuned for direction, with linear speed scaling; other cells showed sinusoidal tuning for position, with linear scaling by distance. Velocity encoding led behavior by about 100 ms for most cells, whereas position tuning was more broadly distributed, with leads and lags suggestive of both feedforward and feedback coding. Individual cells encoded velocity and position weakly, with comparable amounts of information about each. Linear regression methods confirmed that random, 2-D hand trajectories can be reconstructed from the firing of small ensembles of randomly selected neurons (3-19 cells) within the MI arm area. These findings demonstrate that MI carries information about evolving hand trajectory during visually guided pursuit tracking, including information about arm position both during and after its specification. However, the reconstruction methods used here capture only the low-frequency components of movement during the PTT. Hand motion signals appear to be represented as a distributed code in which diverse information about position and velocity is available within small regions of MI. Address for reprint requests and other correspondence: M. R. Fellows, Department of Neuroscience, Brown University, Box 1953, Providence, RI 02912 (E-mail: mrf{at}brown.edu ).