Multimodal Interactions between Proprioceptive and Cutaneous Signals in Primary Somatosensory Cortex

Sung Soo Kim; Manuel Gomez-Ramirez; Pramodsingh H Thakur; Steven S Hsiao

doi:10.1016/j.neuron.2015.03.020

Multimodal Interactions between Proprioceptive and Cutaneous Signals in Primary Somatosensory Cortex

Neuron. 2015 Apr 22;86(2):555-66. doi: 10.1016/j.neuron.2015.03.020. Epub 2015 Apr 9.

Authors

Sung Soo Kim¹, Manuel Gomez-Ramirez², Pramodsingh H Thakur³, Steven S Hsiao⁴

Affiliations

¹ The Zanvyl Krieger Mind/Brain Institute, The Johns Hopkins University, Baltimore, MD 21218, USA; The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins School of Medicine, Baltimore, MD 21218, USA; Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147, USA. Electronic address: sungsoo@janelia.hhmi.org.
² The Zanvyl Krieger Mind/Brain Institute, The Johns Hopkins University, Baltimore, MD 21218, USA; The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins School of Medicine, Baltimore, MD 21218, USA. Electronic address: gomezramirezm@jhu.edu.
³ The Zanvyl Krieger Mind/Brain Institute, The Johns Hopkins University, Baltimore, MD 21218, USA; Department of Biomedical Engineering, The Johns Hopkins University, Baltimore, MD 21218, USA.
⁴ The Zanvyl Krieger Mind/Brain Institute, The Johns Hopkins University, Baltimore, MD 21218, USA; The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins School of Medicine, Baltimore, MD 21218, USA; Department of Biomedical Engineering, The Johns Hopkins University, Baltimore, MD 21218, USA.

Abstract

The classical view of somatosensory processing holds that proprioceptive and cutaneous inputs are conveyed to cortex through segregated channels, initially synapsing in modality-specific areas 3a (proprioception) and 3b (cutaneous) of primary somatosensory cortex (SI). These areas relay their signals to areas 1 and 2 where multimodal convergence first emerges. However, proprioceptive and cutaneous maps have traditionally been characterized using unreliable stimulation tools. Here, we employed a mechanical stimulator that reliably positioned animals' hands in different postures and presented tactile stimuli with superb precision. Single-unit recordings in SI revealed that most neurons responded to cutaneous and proprioceptive stimuli, including cells in areas 3a and 3b. Multimodal responses were characterized by linear and nonlinear effects that emerged during early (∼20 ms) and latter (> 100 ms) stages of stimulus processing, respectively. These data are incompatible with the modality specificity model in SI, and provide evidence for distinct mechanisms of multimodal processing in the somatosensory system.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Analysis of Variance
Animals
Brain Mapping*
Electric Stimulation
Kinesthesis
Macaca mulatta
Neurons / classification
Neurons / physiology*
Nonlinear Dynamics
Proprioception / physiology*
Skin / innervation*
Somatosensory Cortex / physiology*
Touch / physiology*

Abstract

Publication types

MeSH terms

Grants and funding