Convergence of Submodality-Specific Input Onto Neurons in Primary Somatosensory Cortex

• Published in: Journal of neurophysiology 2009-09, Vol.102 (3), p.1843-1853
• Main Authors: Pei, Yu-Cheng, Denchev, Peter V, Hsiao, Steven S, Craig, James C, Bensmaia, Sliman J
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Adaptation, Physiological - physiology; Afferent Pathways - physiology; Animals; Linear Models; Macaca mulatta; Neurons - classification; Neurons - physiology; Peripheral Nerves - physiology; Physical Stimulation - methods; Somatosensory Cortex - cytology
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00235.2009

1 Krieger Mind/Brain Institute and 2 Department of Neuroscience, Johns Hopkins University, Baltimore, Maryland; 3 Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital and Chang Gung University, Taoyuan County, Taiwan; and 4 Department of Psychological and Brain Sciences, Indiana University, Indiana Submitted 20 March 2009; accepted in final form 14 June 2009 Abstract At the somatosensory periphery, slowly adapting type 1 (SA1) and rapidly adapting (RA) afferents respond very differently to step indentations: SA1 afferents respond throughout the entire stimulus interval ( SUSTAINED response), whereas RA afferents respond only at stimulus onset ( ON response) and offset ( OFF response). We recorded the responses of cortical neurons to step indentations and found many neurons in areas 3b and 1 to exhibit properties that are intermediate between these two extremes: These neurons responded during the sustained portion of the stimulus and also at the offset of the stimulus. Several lines of evidence indicate that these neurons, which exist in large proportions even at these early stages of somatosensory cortical processing, receive input from both populations of afferents. First, we show that many cortical neurons have both a significant SUSTAINED response and a significant OFF response. Second, the strength of the OFF response is uncorrelated with that of the SUSTAINED response, which is to be expected if SUSTAINED and OFF responses stem from different populations of afferent fibers. Third, the bulk of the variance in cortical responses to step indentations can be accounted for using a linear combination of both SA1 and RA responses. Finally, we show that the OFF response in cortical neurons does not reflect rebound from inhibition. We conclude that the convergence of modality specific input onto individual neurons is common in primary somatosensory cortex and discuss how this conclusion might be reconciled with previous findings. Address for reprint requests and other correspondence: S. J. Bensmaia, Krieger 338, Johns Hopkins University, 3400 N. Charles St., Baltimore, MD 21218 (E-mail: sliman{at}jhu.edu )