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The Journal of Neuroscience, February 15, 2006, 26(7):2101-2114; doi:10.1523/JNEUROSCI.3720-05.2006

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Behavioral/Systems/Cognitive
Spatiotemporal Receptive Fields of Peripheral Afferents and Cortical Area 3b and 1 Neurons in the Primate Somatosensory System

Arun P. Sripati,^1,2 Takashi Yoshioka,^1,3 Peter Denchev,¹ Steven S. Hsiao,^1,3,4 and Kenneth O. Johnson^1,3,4

¹Zanvyl Krieger Mind/Brain Institute and Departments of ²Electrical and Computer Engineering, ³Neuroscience, and ⁴Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21218

Correspondence should be addressed to Steven S. Hsiao, Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218. Email: Steven.Hsiao{at}jhu.edu

Neurons in area 3b have been previously characterized using linear spatial receptive fields with spatially separated excitatory and inhibitory regions. Here, we expand on this work by examining the relationship between excitation and inhibition along both spatial and temporal dimensions and comparing these properties across anatomical areas. To that end, we characterized the spatiotemporal receptive fields (STRFs) of 32 slowly adapting type 1 (SA1) and 21 rapidly adapting peripheral afferents and of 138 neurons in cortical areas 3b and 1 using identical random probe stimuli. STRFs of peripheral afferents consist of a rapidly appearing excitatory region followed by an in-field (replacing) inhibitory region. STRFs of SA1 afferents also exhibit flanking (surround) inhibition that can be attributed to skin mechanics. Cortical STRFs had longer time courses and greater inhibition compared with peripheral afferent STRFs, with less replacing inhibition in area 1 neurons compared with area 3b neurons. The greater inhibition observed in cortical STRFs point to the existence of underlying intracortical mechanisms. In addition, the shapes of excitatory and inhibitory lobes of both peripheral and cortical STRFs remained mostly stable over time, suggesting that their feature selectivity remains constant throughout the time course of the neural response. Finally, the gradual increase in the proportion of surround inhibition from the periphery to area 3b to area 1, and the concomitant decrease in response linearity of these neurons indicate the emergence of increasingly feature-specific response properties along the somatosensory pathway.

Key words: receptive field; somatosensory cortex; macaque; spatial transformations; peripheral nerve; tactile

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Received Sept. 2, 2005; revised Jan. 5, 2005; accepted Jan. 6, 2006.

Correspondence should be addressed to Steven S. Hsiao, Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218. Email: Steven.Hsiao{at}jhu.edu

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