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)].”

“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) (…”

“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).”

“…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).”

“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…”

“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 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…”

“We fit the parameters of these models on electrophysiological recordings obtained previously (18).”

“At the somatosensory periphery, the intensity of skin vibrations is encoded in the strength of the response of populations of mechanoreceptive afferents (Muniak et al. 2007), while their frequency composition is encoded in millisecond-precision temporal patterning in afferent responses (Mackevicius et al.”

“In the intact nerve, increases in pressure result in both an increase in the number of recruited fibers and an increase in the firing rates of those fibers already recruited (Muniak et al., 2007), which explains why changes in either the delivered charge or the stimulation frequencies result in changes in perceived pr…”

“Indeed, while changes in stimulus amplitude affect perceived intensity (Talbot et al., 1968; Johnson, 1974; Muniak et al., 2007), they have little effect on perceived frequency content over a range of amplitudes (Hernández et al.”

“At the somatosensory periphery, the intensity of both simple and complex vibrations is encoded in the strength of the response these elicit in populations of mechanoreceptive afferents [5,6].”

“Depending on the temporal frequency of the stimulation, either rapidly adapting (RA) or Pacinian (PC) systems are thought to encode these vibrations (Muniak et al., 2007).”

“Previous work in animals (Bensmaïa et al. 2005; Muniak et al. 2007; Phillips and Johnson 1981; Pubols et al. 1971; Werner and Mountcastle 1965) and the human hand (Condon et al. 2014; Hallin et al. 2002; Johansson and Vallbo 1979a; Johansson et al. 1982; Knibestöl and Vallbo 1970) has led to the…”

“The mapping between pressure and perceived intensity could in principle be derived by combining models that characterize the relationship between perceived intensity and afferent responses (46) with models that simulate populations’ responses to arbitrary spatiotemporal skin deformations (47–50).”

“where m and s represent the (known) mean and slope of the sigmoid (estimated in a previous study [13]).”

“…a logarithmic function in different sensory systems likely represents an evolutionary adaptation of the nervous system to respond over a working intensity range, and implies that firing activity of certain types of sensory neurons follows a similar intensity/response ratio (Muniak et al., 2007).”

“These findings are consistent with more recently reported neuroimaging and neurophysiological studies (Chen et al., 2007; Muniak et al., 2007).”

“This is also true for mechanical stimuli where perceived intensity increased with increasing vibration frequency in able-bodied human participants using tactile input to the hand ( Hollins and Roy, 1996 ; Muniak et al., 2007 ; Verrillo et al., 1969 ).”

“The response of a mechanoreceptive afferent to a vibratory stimulus is typically a piece-wise linear function of its amplitude (Figure 1)[12;14;20]: As the amplitude of the stimulus increases beyond the afferent’s absolute threshold (I0), its response increases until the afferent produces one spike per stimulus cycle…”

“Their responses to sinusoids, for example, are restricted to a small fraction of each stimulus cycle over the range of tangible frequencies [7,8,9 ,10 ,11].”

“04) than were the word selections from which they were derived (One‐ way ANOVA, F(3,42) = 35.”

“Appendage mechanosensation is different from these sensory modalities in that the appendages of animals are integrated sensorimotor structures that perform dual roles, acting as both sensory and motor structures during a given behavior (16, 30).”

“Although SA1 and RA afferents become increasingly insensitive beyond this range, PC afferents in fact increase in sensitivity with increases in frequency up to 250–300 Hz (Freeman and Johnson 1982; Muniak et al. 2007; Talbot et al. 1968).”

“The characteristic onion-like structure of the corpuscle confers to the fiber an exquisite sensitivity to rapid transients (9) and submicron-scale vibrations at high frequencies (40-400 Hz) (112, 186, 252).”

“We have previously reported the responses of 35 afferent fibers [15 SA1, 13 RA, and 7 PC, characterized by using standard criteria based on their response properties (63)] to 55 different texture stimuli (see ref.”

“Experimental procedures have been previously described (Muniak et al., 2007).”

“It has been shown that the neural coding of stimulus intensity is best accounted for by the fi ring rate evoked in afferent neurons located within the proximity of stimulation (Muniak et al., 2007; Ray et al., 2008), with increased fi ring rate as stimulus strength is increased.”

“The fact that the amplitude of 400-Hz stimulus was lower than that of the 300-Hz stimulus is somewhat surprising given that thresholds of Pacinian afferents (the mechanoreceptor population sensitive to vibration) are higher at 400 Hz than at 300 Hz (Muniak et al., 2007).”

“The model was developed and tested on the responses of 5 SA1, 5 RA, and 5 PC fibers (recorded from two anesthetized Rhesus macaques) to a variety of vibratory stimuli, including diharmonic stimuli (superimposed sinusoids) and bandpass noise stimuli varying in amplitude and frequency content (for details, see [13]).”

“Note that gluing the probe to the skin has little effect on the perception of these vibrations (Muniak et al. 2007).”

“investigated how the primary afferent responses related specifically to the subjective sensation of stimulus intensity reported by human subjects (20).”

“All three classes of touch receptors respond to textures (Muniak et al. 2007; Phillips et al. 1990, 1992; Saal et al. 2017; Yoshioka et al. 2007) but at different rates; their inputs are weighted differently depending upon the fine structure of the material palpated.”

“This size-dependent recruitment order phenomenon has also been observed in sensory neurons [53–55].”

“Units were classified as SA1, RA, or PC using standard methods (Muniak et al. 2007).”

“The stimulus patterns are similar to the activities of rapidly adapting (RA) and Pacinian (PC) receptors on inputting sinusoidal mechanical stimuli [43].”

“…amplitude and frequency, hoping to capitalize on the fact that different afferent classes exhibit different frequency sensitivity: SA1 fibers peak in sensitivity at low frequencies, PC fibers at high frequencies, and RA fibers at intermediate frequencies (Muniak et al., 2007; Talbot et al., 1968).”

“encoding [36]–[38], reduced habituation of percepts from”

“To explore intensity coding, Muniak et al. (2007) compared magnitude estimates from human participants with physiological responses recorded from primary afferents in anesthetized monkeys.”

“However, response properties also vary within afferent type [7], [ 8 ].”

“For humans and monkeys, it was found that estimation of touch intensity requires the integration of several afferents (Johnson, 1974; Muniak et al., 2007; Bensmaia, 2008; but see Arabzadeh et al., 2014).”

“956 H. E. WHEAT, L. M. SALO, AND A. W. GOODWIN Muniak et al. 2007 ) and in only a few cases has normal force been controlled directly (Cohen and Vierck 1993; Goodwin et al. 1997).”

“…in the task, the optimum level of noise did not activate Pacinian corpuscles with their lowest absolute threshold for frequencies of 250–300 Hz (Muniak et al., 2007; Johansson and Flanagan, 2009) but had activated Merkel disks (and to some extent Meissner receptors) responsive to low…”

“In addition, the frequencies eliciting the highest rates are higher for FA afferents than for either SA class.(23)”

“Tactile stimuli, regardless of difference in modality or quality, can all be judged on a single intensive continuum [10].”

“Vibratory responses have been extensively characterized in the periphery and cortex of rhesus macaques (Harvey et al. 2013; Johnson and Lamb 1981; Mountcastle et al. 1967; Muniak et al. 2007), as have responses to passive and active limb movements.”

“It has been well documented that perceived intensity is a function of, among other things, population recruitment patterns [40].”

“Even a rather elementary property such as perceived vibrotactile intensity is derived from signals arising in all four types of mechanoreceptor found in glabrous skin [12], [13].”

“More recently, by using the same idea of consistency, Muniak et al. (2007) found that stimulus magnitude was best represented by total firing rate of afferents located under or near the stimulus contactor, weighted by afferent type.”

“), one of these covaries more strongly than the others with the perceived magnitude of the stimulus (population firing rate weighted by afferent type), which strongly bolsters its claim as the neural code for intensity (Muniak et al. 2007).”

“Although similar thresholds were observed in those experiments, population models present a more reliable and realistic interpretation for linking physiology and psychophysics (Johnson 1974; Johansson and Vallbo 1980; Goodwin and Wheat 1999; Güçlü and Bolanowski 1999, 2002, 2004, 2005; Güçlü 2007; Muniak et al. 2007).”

“Extracellular single-unit recordings were obtained from the median and ulnar nerves innervating the distal fingertips of 4 Rhesus macaques (Macaca mulatta) as described previously (Muniak et al., 2007; Weber et al., 2013).”

“This hierarchical structure facilitates rapid and efficient tactile encoding, resulting in a dynamic sense of touch ( 4 , 19 ).”

“In the absence of injury, the perceived increase in intensity of a tactile stimulus is encoded by an increased firing of A LTMs (Muniak et al. 2007).”