Journal of Neurophysiology, Vol 56, Issue 3 598-622, Copyright © 1986 by APS

ARTICLES

Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys

S. Warren, H. A. Hamalainen and E. P. Gardner

In order to classify movement-sensitive neurons in SI cortex, and to estimate their relative distribution, we have developed a new simple method for controlled motion of textured surfaces across the skin, as well as a set of objective criteria for determining direction selectivity. Moving stimuli were generated using 5 mm thick precision gear wheels, whose teeth formed a grafting. They were mounted on the shafts of low-torque potentiometers (to measure the speed and direction of movement) and rolled manually across the skin using the potentiometer shaft as an axle. As the grafting wheel was advanced, its ridges sequentially contacted a specific set of points on the skin, leaving gaps of defined spacing that were unstimulated. This stimulus was reproducible from trial to trial and produced little distention of the skin. Three objective criteria were used to categorize responses: the ratio of responses to motion in the most and least preferred directions [direction index (DI)], the difference between mean firing rates in the two directions divided by the average standard deviation [index of discriminability (delta'e)], and statistical tests. Neurons were classified as direction sensitive if DI greater than 35, delta's greater than or equal to 1.35 (equivalent to 75% correct discrimination by an unbiased observer), and firing rates in most- and least-preferred directions were significantly different (P less than 0.05). Good agreement was found between the three classification schemes. Recordings were made from 1,020 cortical neurons in the hand and forearm regions of primary somatosensory cortex (areas 3b, 1 and 2) of five macaque monkeys. Tangential motion across the skin was found to be an extremely effective stimulus for SI cortical neurons. Two hundred eighty six of 757 tactile neurons (38%) responded more vigorously to moving stimuli than to pressure or tapping the skin. One hundred twenty-one cells were tested with moving gratings and were classified according to their ability to differentiate movement in longitudinal and transverse directions. Responses to the moving gratings resembled those observed when stroking the skin with brushed, edges, or blunt probes. Three major types of firing patterns were found: motion sensitive, direction sensitive, and orientation sensitive. Motion-sensitive neurons (37%) responded to movement in both longitudinal and transverse directions with only slight difference in firing rates and interval distributions. Responses throughout the field were fairly uniform, and no clear point of maximum sensitivity was apparent. Direction-sensitive neurons (60%) displayed clear preferences for movement in one or more directions.4

This article has been cited by other articles:

				S. J. Bensmaia, P. V. Denchev, J. F. Dammann III, J. C. Craig, and S. S. Hsiao The Representation of Stimulus Orientation in the Early Stages of Somatosensory Processing J. Neurosci., January 16, 2008; 28(3): 776 - 786. [Abstract] [Full Text] [PDF]

				E. P. Gardner, K. S. Babu, S. D. Reitzen, S. Ghosh, A. S. Brown, J. Chen, A. L. Hall, M. D. Herzlinger, J. B. Kohlenstein, and J. Y. Ro Neurophysiology of Prehension. I. Posterior Parietal Cortex and Object-Oriented Hand Behaviors J Neurophysiol, January 1, 2007; 97(1): 387 - 406. [Abstract] [Full Text] [PDF]

				P. J. Fitzgerald, J. W. Lane, P. H. Thakur, and S. S. Hsiao Receptive field properties of the macaque second somatosensory cortex: representation of orientation on different finger pads. J. Neurosci., June 14, 2006; 26(24): 6473 - 6484. [Abstract] [Full Text] [PDF]

				P. J. Fitzgerald, J. W. Lane, P. H. Thakur, and S. S. Hsiao Receptive field (RF) properties of the macaque second somatosensory cortex: RF size, shape, and somatotopic organization. J. Neurosci., June 14, 2006; 26(24): 6485 - 6495. [Abstract] [Full Text] [PDF]

				A. P. Sripati, T. Yoshioka, P. Denchev, S. S. Hsiao, and K. O. Johnson Spatiotemporal Receptive Fields of Peripheral Afferents and Cortical Area 3b and 1 Neurons in the Primate Somatosensory System J. Neurosci., February 15, 2006; 26(7): 2101 - 2114. [Abstract] [Full Text] [PDF]

				E. Naito, P. E. Roland, C. Grefkes, H. J. Choi, S. Eickhoff, S. Geyer, K. Zilles, and H. H. Ehrsson Dominance of the Right Hemisphere and Role of Area 2 in Human Kinesthesia J Neurophysiol, February 1, 2005; 93(2): 1020 - 1034. [Abstract] [Full Text] [PDF]

				E. Gentaz and A. Streri An "Oblique Effect" in Infants' Haptic Perception of Spatial Orientations J. Cogn. Neurosci., February 1, 2004; 16(2): 253 - 259. [Abstract] [Full Text] [PDF]

				H. E. Wheat and A. W. Goodwin Tactile Discrimination of Gaps by Slowly Adapting Afferents: Effects of Population Parameters and Anisotropy in the Fingerpad J Neurophysiol, September 1, 2000; 84(3): 1430 - 1444. [Abstract] [Full Text] [PDF]

				J. J. DiCarlo and K. O. Johnson Spatial and Temporal Structure of Receptive Fields in Primate Somatosensory Area 3b: Effects of Stimulus Scanning Direction and Orientation J. Neurosci., January 1, 2000; 20(1): 495 - 510. [Abstract] [Full Text] [PDF]

				S. Roy and K. D. Alloway Synchronization of Local Neural Networks in the Somatosensory Cortex: A Comparison of Stationary and Moving Stimuli J Neurophysiol, March 1, 1999; 81(3): 999 - 1013. [Abstract] [Full Text] [PDF]

				J. J. DiCarlo, K. O. Johnson, and S. S. Hsiao Structure of Receptive Fields in Area 3b of Primary Somatosensory Cortex in the Alert Monkey J. Neurosci., April 1, 1998; 18(7): 2626 - 2645. [Abstract] [Full Text] [PDF]

				M. J. Dodson, A. W. Goodwin, A. S. Browning, and H. M. Gehring Peripheral Neural Mechanisms Determining the Orientation of Cylinders Grasped by the Digits J. Neurosci., January 1, 1998; 18(1): 521 - 530. [Abstract] [Full Text] [PDF]

				M Sur, P. Garraghty, and A. Roe Experimentally induced visual projections into auditory thalamus and cortex Science, December 9, 1988; 242(4884): 1437 - 1441. [Abstract] [PDF]