Cutaneous Mechanoreceptive Afferents: Neural Coding of Texture
KeywordsSurface Texture Spatial Layout Perceptual Judgment Pacinian Corpuscle Afferent Response
We can identify objects by the way they feel. As we move our fingers over objects in our pocket or purse, we can easily distinguish between our keys and our phone or between two different fabrics in our dresser drawer. The tactile perception of the surface texture of objects, i.e., of their microstructure and material properties, contributes to our ability to identify them by touch. Signals in the nerve convey information that allows us to identify different textures, as well as attribute different perceptual properties (e.g., roughness or hardness) to them.
Spatial and Temporal Mechanisms
When we run our fingers across a textured surface, a characteristic pattern of deformations is produced in the skin (Sripati et al. 2006), and the resulting stresses and strains are transduced by multiple populations of mechanoreceptors embedded in the skin. The spatial layout and timing of the consequent spatiotemporal patterns of afferent activation convey information about surface texture (Weber et al. 2013).
In summary, then, coarse textural features are encoded in the spatial pattern of activity evoked in one population of afferents – SA1 fibers – while fine textural features are encoded in the temporal patterns of activity evoked in the other two, RA and PC fibers.
Multidimensionality of Texture Perception
The sensation of exploring a surface can be described along a number of perceptual dimensions: things may feel rough or smooth, hard or soft, sticky or slippery, and warm or cool (Hollins et al. 2000). The dominant dimension, and the most studied one, is roughness.
Sensitivity to peripheral variability is a common feature of sensory processing. Indeed, when stimuli do not change in time, central sensory neurons across all modalities adapt toward their baseline level of activity (Wark et al. 2007). In this way, adaptation serves to increase neural sensitivity to variations in the sensory input. Furthermore, sensory neurons in both visual and somatosensory cortex exhibit both excitatory and inhibitory components and thus show sensitivity to spatial differences in activation across the sensory sheet.
Information from both spatial and temporal mechanisms is combined to reconstruct judgments of hardness. Surfaces with different compliance lead to different spatial patterns of deformation of the skin: soft surfaces deform around the skin, while hard surfaces change the shape of the skin. These spatial patterns of skin deformations are reflected in the spatial patterns of activation elicited in populations of SA1 afferents (Franzén et al. 1996).
Precisely timed information can also be used to determine hardness. When judged through a probe, hardness is most effectively perceived using rapid tapping motions (LaMotte 2000), which elicit dynamic force profiles that most effectively recruit RA and PC afferents. Indeed, while SA1 responses to statically indented stimuli are informative about surface compliance, RA responses only convey hardness information during the dynamic loading phase (Fig. 4b; Condon et al. 2013).
Perceptual judgments of stickiness are often closely correlated with perceptual judgments of roughness (Hollins et al. 2000). When exploring the stickiness of a surface, subjects tend to apply a set amount of force normal to the surface. The resulting range of force tangential to the surface covaries closely with measurements of perceived stickiness (Smith and Scott 1996). Tangential forces stretch the skin, which excites Ruffini cylinders (innervated by slowly adapting type II (SAII) afferents) (Knibestol 1975) as well as SA1 and RA afferents (Birznieks et al. 2001, 2010).
Perception of a surface’s temperature is clearly used for object identification (Katz and Krueger 1989) and is incorporated into the multidimensional percept of texture (Bensmaia and Hollins 2005; Hollins et al. 2000). Because everyday objects tend to be colder than skin temperature, surface temperature is determined by the rate of heat flow out of the skin (Ho and Jones 2006). This heat flow is almost certainly transduced by thermoreceptive afferents in the skin (Darian-Smith et al. 1973, 1979; Johnson et al. 1973, 1979).
Spatiotemporal patterns of activation across the four main populations of afferents that innervate the glabrous skin of the hand – SA1, RA, PC, and SAII – as well as thermoreceptors, convey exquisite and multidimensional information about surface texture. Different information about surface texture is conveyed in different aspects of afferent responses, with spatial patterns mediating the perception of coarse features and compliance and temporal patterns mediating the perception of fine features. Importantly, the perception of texture reflects the integration of different types of signals from multiple different tactile submodalities.
- Franzén O, Johansson R, Terenius LY (1996) Somesthesis and the neurobiology of the somatosensory cortex. In: Advances in life sciences. Birkhäuser Verlag, Basel/Boston, xx, 421 ppGoogle Scholar
- Katz D, Krueger LE (1989) The world of touch. Erlbaum, Hillsdale. xii 260 ppGoogle Scholar
- Manfredi LR et al (2014) Natural scenes in tactile texture. J Neurophysiol. (doi:10.1152/jn.00680.2013)Google Scholar