The Neural Coding of Stimulus Intensity: Linking the Population Response of Mechanoreceptive Afferents with Psychophysical Behavior
TL;DR: The neural code underlying the perception of stimulus intensity in the somatosensory system is investigated and it is concluded that stimulus intensity is best accounted for by the firing rate evoked in afferents located under or near the locus of stimulation, weighted by afferent type.
Abstract: How specific aspects of a stimulus are encoded at different stages of neural processing is a critical question in sensory neuroscience. In the present study, we investigated the neural code underlying the perception of stimulus intensity in the somatosensory system. We first characterized the responses of SA1 (slowly adapting type 1), RA (rapidly adapting), and PC (Pacinian) afferents of macaque monkeys to sinusoidal, diharmonic, and bandpass noise stimuli. We then had human subjects rate the perceived intensity of a subset of these stimuli. On the basis of these neurophysiological and psychophysical measurements, we evaluated a series of hypotheses about which aspect(s) of the neural activity evoked at the somatosensory periphery account for perception. We evaluated three types of neural codes. The first consisted of population codes based on the firing rate of neurons located directly under the probe. The second included population codes based on the firing rate of the entire population of active neurons. The third included codes based on the number of active afferents. We found that the response evoked in the localized population is logarithmic with stimulus amplitude (given a constant frequency composition), whereas the population response across all neurons is linear with stimulus amplitude. We conclude that stimulus intensity is best accounted for by the firing rate evoked in afferents located under or near the locus of stimulation, weighted by afferent type.
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TL;DR: In this paper, a combination of spatial and temporal mechanisms, mediated by all three populations of afferents, accounts for perceptual judgments of texture in Rhesus macaques using a custom-made rotating drum stimulator.
Abstract: When we run our fingers over the surface of an object, we acquire information about its microgeometry and material properties. Texture information is widely believed to be conveyed in spatial patterns of activation evoked across one of three populations of cutaneous mechanoreceptive afferents that innervate the fingertips. Here, we record the responses evoked in individual cutaneous afferents in Rhesus macaques as we scan a diverse set of natural textures across their fingertips using a custom-made rotating drum stimulator. We show that a spatial mechanism can only account for the processing of coarse textures. Information about most natural textures, however, is conveyed through precise temporal spiking patterns in afferent responses, driven by high-frequency skin vibrations elicited during scanning. Furthermore, these texture-specific spiking patterns predictably dilate or contract in time with changes in scanning speed; the systematic effect of speed on neuronal activity suggests that it can be reversed to achieve perceptual constancy across speeds. The proposed temporal coding mechanism involves converting the fine spatial structure of the surface into a temporal spiking pattern, shaped in part by the mechanical properties of the skin, and ascribes an additional function to vibration-sensitive mechanoreceptive afferents. This temporal mechanism complements the spatial one and greatly extends the range of tangible textures. We show that a combination of spatial and temporal mechanisms, mediated by all three populations of afferents, accounts for perceptual judgments of texture.
293 citations
TL;DR: This work proposes that the timing of contact events can be signaled through phasic intracortical microstimulation at the onset and offset of object contact that mimics the ubiquitous on and off responses observed in primary somatosensory cortex to complement slowly varying pressure-related feedback.
Abstract: Our ability to manipulate objects dexterously relies fundamentally on sensory signals originating from the hand. To restore motor function with upper-limb neuroprostheses requires that somatosensory feedback be provided to the tetraplegic patient or amputee. Given the complexity of state-of-the-art prosthetic limbs and, thus, the huge state space they can traverse, it is desirable to minimize the need for the patient to learn associations between events impinging on the limb and arbitrary sensations. Accordingly, we have developed approaches to intuitively convey sensory information that is critical for object manipulation—information about contact location, pressure, and timing—through intracortical microstimulation of primary somatosensory cortex. In experiments with nonhuman primates, we show that we can elicit percepts that are projected to a localized patch of skin and that track the pressure exerted on the skin. In a real-time application, we demonstrate that animals can perform a tactile discrimination task equally well whether mechanical stimuli are delivered to their native fingers or to a prosthetic one. Finally, we propose that the timing of contact events can be signaled through phasic intracortical microstimulation at the onset and offset of object contact that mimics the ubiquitous on and off responses observed in primary somatosensory cortex to complement slowly varying pressure-related feedback. We anticipate that the proposed biomimetic feedback will considerably increase the dexterity and embodiment of upper-limb neuroprostheses and will constitute an important step in restoring touch to individuals who have lost it.
287 citations
TL;DR: Questions are raised as to whether the body surface can be mapped affectively in a meaningful manner with a single stimulus and indeed whether pleasantness-to-touch can be viewed as a unidimensional construct.
266 citations
Cites background from "The Neural Coding of Stimulus Inten..."
...…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…...
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TL;DR: This work compared the naturalness and efficacy of different encoding strategies to deliver neural stimulation to trans-radial amputees implanted with intraneural electrodes and found that hybrid strategies are able to provide highly sensitive and natural percepts and should be preferred.
230 citations
TL;DR: It is argued that cortical neurons should be grouped based on their function rather than on their submodality composition, as most natural stimuli excite all afferents and most tactile percepts are shaped by multiple submodalities.
207 citations
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TL;DR: The Open Society and Its Enemies as mentioned in this paper is regarded as one of Popper's most enduring books and contains insights and arguments that demand to be read to this day, as well as many of the ideas in the book.
Abstract: Described by the philosopher A.J. Ayer as a work of 'great originality and power', this book revolutionized contemporary thinking on science and knowledge. Ideas such as the now legendary doctrine of 'falsificationism' electrified the scientific community, influencing even working scientists, as well as post-war philosophy. This astonishing work ranks alongside The Open Society and Its Enemies as one of Popper's most enduring books and contains insights and arguments that demand to be read to this day.
3,178 citations
TL;DR: The spatial distribution of densities supports the idea that the RA and SA I units account for spatial acuity in psychophysical tests, which is known to increase in distal direction along the hand.
Abstract: 1. Single unit impulses were recorded with percutaneously inserted tungsten needle electrodes from the median nerve in conscious human subjects. 2. A sample of 334 low threshold mechanoreceptive units innervating the glabrous skin area of the hand were studied. In accordance with earlier investigations, the units were separated into four groups on the basis of their adaptation and receptive field properties: RA, PC, SA I and SA II units. 3. The locations of the receptive fields of individual units were determined and the relative unit densities within various skin regions were calculated. The over-all density was found to increase in the proximo-distal direction. There was a slight increase from the palm to the main part of the finger and an abrupt increase from the main part of the finger to the finger tip. The relative densities in these three regions were 1, 1.6, 4.2. 4. The differences in over-all density were essentially accounted for by the two types of units characterized by small and well defined receptive fields, the RA and SA I units, whereas the PC and SA II units were almost evenly distributed over the whole glabrous skin area. 5. The spatial distribution of densities supports the idea that the RA and SA I units account for spatial acuity in psychophysical tests. This capacity is known to increase in distal direction along the hand. 6. On the basis of histological data regarding the number of myelinated fibres in the median nerve, a model of the absolute unit density was proposed. It was estimated that the density of low threshold mechanoreceptive units at the finger tip is as high as 241 u./cm2, whereas in the palm it is only 58 u./cm2.
1,148 citations
TL;DR: The results support the idea that each of the four mechanoreceptive afferent systems innervating the hand serves a distinctly different perceptual function, and that tactile perception can be understood as the sum of these functions.
942 citations
"The Neural Coding of Stimulus Inten..." refers background in this paper
...…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....
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TL;DR: This paper combines two experimental of the first importance for sensory neurophysdesigns which differ remarkably in method, iology, for they establish the dynamic and in their historical and conceptual derange required of the input on the afferent side of the system to account for the output-the measured sensory capacities.
Abstract: IT WAS OUR PURPOSE in the studies described in the intact, behaving organism are therefore this paper to combine two experimental of the first importance for sensory neurophysdesigns which differ remarkably in method, iology, for they establish: 7) the dynamic and in their historical and conceptual derange required of the input on the afferent side of the system to account for the output-the measured sensory capacities; 2) the information about the stimulus which must be preserved in the initial encoding to account for the over-all information transmitting capacity of the nervous system in a particular sensory sphere; and 3) a basis for determining which of the many codes available to the pulse-operated input sys tern may be of functional significance in the sensory performance measured. It is thought that a continued correlation of the results of these two types of studies will set the limits and establish some of the parameters to be expected of that higher order neural mechanism intervening between initial cortical display and sensory experience, referred to above. mechanisms (30). Electrophysiological studies, particularly with the method of singleunit analysis, can now provide precise measures of the neural encoding in first-order nerve fibers of the parameters of peripheral stimuli, and of the successive relay and transformation of that neural replication from periphery to cerebral cortex. They have so far provided little understanding of those cerebral mechanisms which, operating upon the transformed replication of the peripheral event in the primary receiving areas of the cerebral cortex, are thought to lead to subjective sensory experience and its overt behavioral counterparts. Psychophysical studies, on the other hand, seek to establish Ideally, the two types of observation should be made in the same organism at the same lawful relations between those experiences time. Given the demands of the single-unit and certain physical aspects of the stimuli method when applied in its quantitative which evoke them. The results of these quantiform, and particularly the desired level of tative measures of the sensory performance of control of stimulus parameters, this is not vet possible for somesthesis. For the present Received for publication August 24, 1967. l This study was supported by Public Health &e Ahave made the assumption thai what Service Grants NB-1045 and NB-06828, Air Force monkeys and humans feel with their hands Contract no. 49 (638) 1305. is in principle the same, and that neuro2 Visiting Lecturer in Physiology, 1966, from the physiological observations made in the one School of Physiology, University of New South Wales, New South Wales, Australia. may with some validity be correlated with 3 Foreign Fellow of the Public Health Service, psychophysical measures in the other, given 1965-1966, from the University of Freiburg im Breisa precise identity of experimental design in gau, Germany. the two cases.
933 citations
"The Neural Coding of Stimulus Inten..." refers background or methods or result in this paper
...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 (for frequencies through 400 Hz), although considerably shallower....
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...Mechanoreceptive afferents often exhibit entrained responses to sinusoidal stimuli (i.e., an integral number of impulses per cycle) over wide ranges of amplitudes (Talbot et al., 1968; Johnson, 1974; Bensmaia et al., 2005b)....
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...Single-unit recordings were made from the ulnar and median nerves of two anesthetized macaque monkeys (Macaca mulatta) using standard methods (Talbot et al., 1968)....
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..., an integral number of impulses per cycle) over wide ranges of amplitudes (Talbot et al., 1968; Johnson, 1974; Bensmaia et al., 2005b)....
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...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…...
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TL;DR: It is concluded that the four channels work in conjunction at threshold to create an operating range for the perception of vibration that extends from at least 0.4 to greater than 500 Hz and may be determined by the combined inputs from four channels.
Abstract: Although previous physiological and anatomical experiments have identified four afferent fiber types (PC, RA, SA II, and SA I) in glabrous (nonhairy) skin of the human somatosensory periphery, only three have been shown to mediate tactile (mechanoreceptive) sensation. Psychophysical evidence that four channels (P, NP I, NP II, and NP III) do, indeed, participate in the perceptual process is presented. In a series of experiments involving selective masking of the various channels, modification of the skin‐surface temperature, and testing cutaneous sensitivity down to very low‐vibratory frequencies, the fourth psychophysical channel (NP III) is defined. Based on these experiments and previous work from our laboratory, it is concluded that the four channels work in conjunction at threshold to create an operating range for the perception of vibration that extends from at least 0.4 to greater than 500 Hz. Each of the four channels appears to mediate specific portions of the overall threshold‐frequency characteristic. Selection of appropriate neural‐response criteria from previously published physiological data and correlation of their derived frequency characteristics with the four psychophysical channels indicates that each channel has its own physiological substrate: P channel and PC fibers, NP I channel and RA fibers, NP II channel and SA II fibers, and NP III channel and SA I fibers. These channels partially overlap in their absolute sensitivities, making it likely that suprathreshold stimuli may activate two or more of the channels at the same time. Thus the perceptual qualities of touch may be determined by the combined inputs from four channels.
885 citations
"The Neural Coding of Stimulus Inten..." refers background in this paper
...However, there is little direct evidence that it contributes to vibrotaction [for a counterargument, see Bolanowski et al. (1988)]....
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