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Neural coding mechanisms underlying perceived roughness of finely textured surfaces
T Yoshioka1, B Gibb, A K Dorsch
1Zanvyl Krieger Mind/Brain Institute, Departments of Neuroscience and Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21218, USA. takashi@jhu.edu
Summary
Perceived surface roughness, whether from coarse or fine elements, is consistently signaled by spatial variations in slowly adapting type 1 (SA1) afferent nerve firing rates. This neural mechanism explains human judgments across different element spacings.
Area of Science:
- Neuroscience
- Psychophysics
- Somatosensation
Background:
- Previous research established that perceived roughness for surfaces with element spacings greater than 1 mm relies on spatial variations in slowly adapting type 1 (SA1) afferent firing rates.
- The neural basis for roughness perception with element spacings less than 1 mm remained less understood.
Purpose of the Study:
- To investigate whether the SA1 afferent spatial firing rate variation mechanism explains the perceived roughness of surfaces with element spacings smaller than 1 mm.
- To compare the neural responses of SA1, rapidly adapting (RA), and Pacinian (PC) afferents to various surface textures.
Main Methods:
- Human psychophysical experiments were conducted using 20 gratings and a smooth surface with varying spatial periods, groove widths (GWs), and ridge widths (RWs).
- Neurophysiological recordings were performed on SA1, RA, and PC afferents in anesthetized macaque monkeys as surfaces were scanned across their receptive fields.
- Correlation analysis was used to compare psychophysical roughness magnitude estimates with neural firing rate variations.
Main Results:
- Human roughness magnitude estimates were accurately described by the equation: 0.2 + 1.6GW - 0.5RW - 0.25GW(2) (R=0.99).
- Spatial variation in SA1 afferent firing rates showed a high correlation (R=0.97) with human roughness judgments across all tested surfaces.
- Pacinian (PC) afferent responses did not correlate with roughness perception, showing strong and uniform responses to all patterns.
Conclusions:
- Spatial variation in SA1 afferent firing rates is the sole neural code responsible for perceived surface roughness, irrespective of element spacing (fine or coarse).
- For finely spaced elements, stochastic variations in SA1 firing rates contribute to the perceived roughness, complementing pattern-driven variations seen with coarser elements.