Trends in Neurosciences

Trends in Neurosciences

Volume 37, Issue 12, December 2014, Pages 689-697
Journal home page for Trends in Neurosciences

Opinion
Touch is a team effort: interplay of submodalities in cutaneous sensibility

https://doi.org/10.1016/j.tins.2014.08.012Get rights and content

Highlights

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    Every tactile function is subserved by multiple afferent types.

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    Neurons in primary somatosensory cortex receive inputs from multiple afferent types.

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    Somatosensory responses should be categorized by function rather than by submodality.

Traditionally, different classes of cutaneous mechanoreceptive afferents are ascribed different and largely non-overlapping functional roles (for example texture or motion) stemming from their different response properties. This functional segregation is thought to be reflected in cortex, where each neuron receives input from a single submodality. We summarize work that challenges this notion. First, while it is possible to design artificial stimuli that preferentially excite a single afferent class, most natural stimuli excite all afferents and most tactile percepts are shaped by multiple submodalities. Second, closer inspection of cortical responses reveals that most neurons receive convergent input from multiple afferent classes. We argue that cortical neurons should be grouped based on their function rather than on their submodality composition.

Section snippets

The cutaneous submodalities

If one opens a neuroscience textbook to the somatosensory chapter, one is likely to find a table that ascribes a different function to each afferent: one afferent population mediates shape and texture perception, another motion perception, a further one skin stretch perception, and the last vibration perception (Figure 1A). This segregation of function was most eloquently articulated by Kenneth Johnson in a series of review papers 1, 2, 3, illustrating this point using results from his elegant

Multiple submodalities contribute to most tactile percepts

Three populations of mechanoreceptive afferents innervate the glabrous skin of the hand. Slowly adapting type 1 (SA1) afferents, which terminate in Merkel disks; rapidly adapting (RA) afferents, which innervate Meissner corpuscles; and PC afferents, which innervate Pacinian corpuscles. These three populations of afferents respond to different aspects of skin deformations. A fourth population of mechanoreceptors, Ruffini cylinders (innervated by slowly adapting type 2 or SA2 afferents), tend to

The convergence of submodality specific signals in primary somatosensory cortex

Two intermediate neural structures relay tactile signals from the periphery to cortex: the cuneate nucleus and the ventroposterior lateral nucleus of the thalamus. We describe the pathway in more detail in Box 1, together with the (rather sparse) results relevant to the question of submodality segregation in these nuclei. In the following we will focus on primary somatosensory cortex (S1), first laying out the evidence for the traditional view of submodality segregation, and then following up

Somatosensory neurons should be classified in terms of function, not presumed submodality

The traditional view posits that mechanoreceptive afferents play different functional roles stemming from their different response properties. Given this separation of function, submodality-specific signals would need to remain segregated as they ascend the somatosensory hierarchy to not interfere with each other's function. However, as discussed above, most natural tactile stimuli excite most afferent types, information about any one of their features is carried by multiple submodalities, and

Acknowledgments

We thank Drs James Craig, Mark Hollins, Andrew Pruszynski, and Jeffrey Yau for their comments on a previous version of this manuscript. This work was supported by National Science Foundation grant IOS-1150209.

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