The Neural Coding of Stimulus Intensity: Linking the Population Response of Mechanoreceptive Afferents with Psychophysical Behavior

“…flutter and motion perception; and PC in the perception of microtextures (Hollins and Bensmaia, 2007) and of textures explored through a tool (Yoshioka et al., 2007) (for review, see Johnson, 2001)], all three populations of afferents respond to most natural stimuli, albeit to different degrees.”

“The frequency dependence of threshold parameter conformed with previous measurements of absolute threshold (Talbot et al., 1968; Freeman and Johnson, 1982a; Johansson et al., 1982): PC afferents yielded a characteristic U-shaped threshold-frequency relationship; the RA threshold-frequency function was also U-shaped (f…”

“However, there is little direct evidence that it contributes to vibrotaction [for a counterargument, see Bolanowski et al. (1988)].”

“The perceived intensity of sinusoids in the low- to intermediatefrequency range has been shown to increase linearly with stimulus intensity (Stevens, 1968; Franzén, 1969; Verrillo et al., 1969) whereas the firing rates evoked in individual peripheral afferents do not (Mountcastle et al., 1969).”

“For instance, microstimulation of single SA2 afferents does not produce any conscious sensation, much less a vibratory percept, whereas microstimulation of the other three afferent types yields sensations ranging from pressure, to taps, to vibrations, the nature of which depends both on the frequency of the electrical…”

“The frequency dependence of threshold parameter conformed with previous measurements of absolute threshold (Talbot et al., 1968; Freeman and Johnson, 1982a; Johansson et al., 1982): PC afferents yielded a characteristic U-shaped threshold-frequency relationship; the RA threshold-frequency function was also U-shaped (f…”

“The coarse spatial structure of SA1 and RA RFs is similar (Johansson, 1978), and the model is likely applicable to both afferent types.”

“Perceived intensity was modeled as a simple power function of stimulus intensity (Stevens, 1968; Franzén, 1969) or as a two-branched function, with the second branch a power function (Verrillo et al., 1969; Hollins and Roy, 1996).”

“that the perception of frequency is simply based on the mean firing rates of mechanoreceptive afferents, although frequency may be coded with a mean rate code in primary somatosensory cortex (Salinas et al., 2000).”

“Moreover, how stimulus intensity is represented in cortex is unclear [but see de Lafuente and Romo (2005, 2006)].”

“Moreover, how stimulus intensity is represented in cortex is unclear [but see de Lafuente and Romo (2005, 2006)].”

“Next, we assessed whether the recruitment of afferents could serve as a code for intensity [following Johnson (1974)].”

“First, their RFs are an order of magnitude larger (mean area 101 mm 2 vs 11 and 13 mm 2 for SA1 and RA afferents, respectively) (Johansson and Vallbo, 1980).”

“Although the three afferent types have been implicated in different aspects of tactile perception [SA1 in form and texture perception; RA in microslip, flutter and motion perception; and PC in the perception of microtextures (Hollins and Bensmaia, 2007) and of textures explored through a tool (Yoshioka et al., 2007) (…”

“…A fourth type of afferent, slowly adapting type 2 (SA2), traditionally believed to terminate in Ruffini corpuscles (although see Pare et al., 2003), is found in the glabrous skin of humans but not macaques and responds to vibratory stimulation (Merzenich and Harrington, 1969; Gynther et al., 1992).”

“That simple coding mechanisms such as the ones proposed here can account for perception is particularly striking given the nonlinear and dynamic nature of cortical processing (Moore et al., 1999; Kohn and Whitsel, 2002; Sripati et al., 2006).”

“…tactile perception [SA1 in form and texture perception; RA in microslip, flutter and motion perception; and PC in the perception of microtextures (Hollins and Bensmaia, 2007) and of textures explored through a tool (Yoshioka et al., 2007) (for review, see Johnson, 2001)], all three populations…”

“Furthermore, the discriminability of sinusoidal, diharmonic, and triharmonic waveforms cannot be predicted on the basis of intensity cues alone but rather is a function of both the intensive and temporal properties of the stimuli (Bensmaia et al., 2005a).”

“Furthermore, the discriminability of sinusoidal, diharmonic, and triharmonic waveforms cannot be predicted on the basis of intensity cues alone but rather is a function of both the intensive and temporal properties of the stimuli (Bensmaia et al., 2005a).”

“DOI:10.1523/JNEUROSCI.1486-07.2007 Copyright © 2007 Society for Neuroscience 0270-6474/07/2711687-13$15.00/0 exists between the aspect of the neural activity that is relevant to the subjective experience (in this case, perceived intensity) and the subjective experience itself (Johnson et al., 2002).”

“The frequency dependence of threshold parameter conformed with previous measurements of absolute threshold (Talbot et al., 1968; Freeman and Johnson, 1982a; Johansson et al., 1982): PC afferents yielded a characteristic U-shaped threshold-frequency relationship; the RA threshold-frequency function…”

“The tip of the stylus was flat and had a diameter of 1 mm (cf. Freeman and Johnson, 1982b).”

“…is explained only in part by adaptation in the responses of peripheral afferents (Bensmaia et al., 2005b) [however, given the time course of the spatial funneling and of peripheral and central adaptation (Leung et al., 2005), the degree to which these phenomena influenced our results is not clear].”

“For instance, lowfrequency diharmonic stimuli varying only in the phase of the high-frequency component relative to that of the low-frequency component have been shown to be discriminable (Bensmaia and Hollins, 2000), although these evoke identical firing rates in the three afferent types (Fig.”

“That simple coding mechanisms such as the ones proposed here can account for perception is particularly striking given the nonlinear and dynamic nature of cortical processing (Moore et al., 1999; Kohn and Whitsel, 2002; Sripati et al., 2006).”

“The phenomenon of central adaptation also constitutes a dynamic change in the responses of cortical neurons to vibratory stimuli: indeed, cortical responses to extended suprathreshold vibratory stimulation decrease over time (O’Mara et al., 1988; Whitsel et al., 2003), a phenomenon that is explained only in part by ad…”

“…type 2 afferents A fourth type of afferent, slowly adapting type 2 (SA2), traditionally believed to terminate in Ruffini corpuscles (although see Pare et al., 2003), is found in the glabrous skin of humans but not macaques and responds to vibratory stimulation (Merzenich and Harrington, 1969;…”

“The perceived intensity of sinusoids in the low- to intermediatefrequency range has been shown to increase linearly with stimulus intensity (Stevens, 1968; Franzén, 1969; Verrillo et al., 1969) whereas the firing rates evoked in individual peripheral afferents do not (Mountcastle et al., 1969).”

“For instance, vibratory stimulation has been shown to evoke a pattern of activation in primary somatosensory cortex that becomes more spatially restricted over time (Simons et al., 2007).”

“Perceived intensity was modeled as a simple power function of stimulus intensity (Stevens, 1968; Franzén, 1969) or as a two-branched function, with the second branch a power function (Verrillo et al., 1969; Hollins and Roy, 1996).”

“That simple coding mechanisms such as the ones proposed here can account for perception is particularly striking given the nonlinear and dynamic nature of cortical processing (Moore et al., 1999; Kohn and Whitsel, 2002; Sripati et al., 2006).”

“The phenomenon of central adaptation also constitutes a dynamic change in the responses of cortical neurons to vibratory stimuli: indeed, cortical responses to extended suprathreshold vibratory stimulation decrease over time (O’Mara et al., 1988; Whitsel et al., 2003), a phenomenon that is explained only in part by ad…”

“Johnson (1974) set out to elucidate the neural code of perceived intensity by reconstructing the response evoked in a population of RA afferents by 40 Hz vibrations at various intensities (also see Cohen and Vierck, 1993b).”

“The perceived intensity of sinusoids in the low- to intermediatefrequency range has been shown to increase linearly with stimulus intensity (Stevens, 1968; Franzén, 1969; Verrillo et al., 1969) whereas the firing rates evoked in individual peripheral afferents do not (Mountcastle et al., 1969).”

“Johnson (1974) set out to elucidate the neural code of perceived intensity by reconstructing the response evoked in a population of RA afferents by 40 Hz vibrations at various intensities (also see Cohen and Vierck, 1993b).”

“Second, because the three populations of mechanoreceptive afferents have different frequency sensitivity profiles, the relative activation of each population of afferents could carry information about the frequency content of the stimulus (Roy and Hollins, 1998).”

“…A fourth type of afferent, slowly adapting type 2 (SA2), traditionally believed to terminate in Ruffini corpuscles (although see Pare et al., 2003), is found in the glabrous skin of humans but not macaques and responds to vibratory stimulation (Merzenich and Harrington, 1969; Gynther et al., 1992).”

“Extracellular single-unit recordings were collected from the median and ulnar nerves innervating the distal fingertips of six Rhesus macaques (Macaca mulatta) using established procedures (11, 12).”

“…in populations of slowly adapting mechanoreceptors (SAI units: Blake et al., 1997; Connor et al., 1990; Connor and Johnson, 1992; see also Muniak et al., 2007, for vibrotactile intensity coding) except for very smooth surfaces, where activity in the Pacinian (RAII) channel appears more…”