scholarly journals The neural code for tactile roughness in the somatosensory nerves

2017 ◽  
Vol 118 (6) ◽  
pp. 3107-3117 ◽  
Author(s):  
Justin D. Lieber ◽  
Xinyue Xia ◽  
Alison I. Weber ◽  
Sliman J. Bensmaia

Roughness is the most salient perceptual dimension of surface texture but has no well-defined physical basis. We seek to determine the neural determinants of tactile roughness in the somatosensory nerves. Specifically, we record the patterns of activation evoked in tactile nerve fibers of anesthetized Rhesus macaques to a large and diverse set of natural textures and assess what aspect of these patterns of activation can account for psychophysical judgments of roughness, obtained from human observers. We show that perceived roughness is determined by the variation in the population response, weighted by fiber type. That is, a surface will feel rough to the extent that the activity varies across nerve fibers and varies across time within nerve fibers. We show that this variation-based neural code can account not only for magnitude estimates of roughness but also for roughness discrimination performance. NEW & NOTEWORTHY Our sense of touch endows us with an exquisite sensitivity to the microstructure of surfaces, the most salient aspect of which is roughness. We analyze the responses evoked in tactile fibers of monkeys by natural textures and compare them to judgments of roughness obtained for the same textures from human observers. We then describe how texture signals from three populations of nerve fibers are integrated to culminate in a percept of roughness.

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Hannes P Saal ◽  
Michael A Harvey ◽  
Sliman J Bensmaia

The sense of touch comprises multiple sensory channels that each conveys characteristic signals during interactions with objects. These neural signals must then be integrated in such a way that behaviorally relevant information about the objects is preserved. To understand the process of integration, we implement a simple computational model that describes how the responses of neurons in somatosensory cortex—recorded from awake, behaving monkeys—are shaped by the peripheral input, reconstructed using simulations of neuronal populations that reproduce natural spiking responses in the nerve with millisecond precision. First, we find that the strength of cortical responses is driven by one population of nerve fibers (rapidly adapting) whereas the timing of cortical responses is shaped by the other (Pacinian). Second, we show that input from these sensory channels is integrated in an optimal fashion that exploits the disparate response behaviors of different fiber types.


2021 ◽  
Vol 2021 ◽  
pp. 1-13
Author(s):  
Jeanette M. Metzger ◽  
Helen N. Matsoff ◽  
Don Vu ◽  
Alexandra D. Zinnen ◽  
Kathryn M. Jones ◽  
...  

Minimal myelination is proposed to be a contributing factor to the preferential nigral neuronal loss in Parkinson’s disease (PD). Similar to nigral dopaminergic neurons, sympathetic neurons innervating the heart have long, thin axons which are unmyelinated or minimally myelinated. Interestingly, cardiac sympathetic loss in PD is heterogeneous across the heart, yet the spatial relationship between myelination and neurodegeneration is unknown. Here, we report the mapping of myelin basic protein (MBP) expression across the left ventricle of normal rhesus macaques (n = 5) and animals intoxicated with systemic 6-OHDA (50 mg/kg iv) to model parkinsonian cardiac neurodegeneration (n = 10). A subset of 6-OHDA-treated rhesus received daily dosing of pioglitazone (5 mg/kg po; n = 5), a PPARγ agonist with neuroprotective properties. In normal animals, MBP-immunoreactivity (-ir) was identified surrounding approximately 14% of axonal fibers within nerve bundles of the left ventricle, with more myelinated nerve fibers at the base level of the left ventricle than the apex p < 0.014 . Greater MBP-ir at the base was related to a greater number of nerve bundles at that level relative to the apex p < 0.05 , as the percent of myelinated nerve fibers in bundles was not significantly different between levels of the heart. Cardiac sympathetic loss following 6-OHDA was associated with decreased MBP-ir in cardiac nerve bundles, with the percent decrease of MBP-ir greater in the apex (84.5%) than the base (52.0%). Interestingly, cardiac regions and levels with more MBP-ir in normal animals showed attenuated sympathetic loss relative to areas with less MBP-ir in 6-OHDA + placebo (r = −0.7, p < 0.014 ), but not in 6-OHDA + pioglitazone (r = −0.1) subjects. Our results demonstrate that myelination is present around a minority of left ventricle nerve bundle fibers, is heterogeneously distributed in the heart of rhesus macaques, and has a complex relationship with cardiac sympathetic neurodegeneration and neuroprotection.


2019 ◽  
Author(s):  
Justin D. Lieber ◽  
Sliman J. Bensmaia

ABSTRACTA major function of sensory processing is to achieve neural representations of objects that are stable across changes in context and perspective. Small changes in exploratory behavior can lead to large changes in signals at the sensory periphery, thus resulting in ambiguous neural representations of objects. Overcoming this ambiguity is a hallmark of human object recognition across sensory modalities. Here, we investigate how the perception of tactile texture remains stable across exploratory movements of the hand, including changes in scanning speed, despite the concomitant changes in afferent responses. To this end, we scanned a wide range of everyday textures across the fingertips of Rhesus macaques at multiple speeds and recorded the responses evoked in tactile nerve fibers and somatosensory cortical neurons. We found that individual cortical neurons exhibit a wider range of speed-sensitivities than do nerve fibers. The resulting representations of speed and texture in cortex are more independent than are their counterparts in the nerve and account for speed-invariant perception of texture. We demonstrate that this separation of speed and texture information is a natural consequence of previously described cortical computations.


2015 ◽  
Vol 113 (7) ◽  
pp. 2934-2952 ◽  
Author(s):  
Brian J. Malone ◽  
Brian H. Scott ◽  
Malcolm N. Semple

The temporal coherence of amplitude fluctuations is a critical cue for segmentation of complex auditory scenes. The auditory system must accurately demarcate the onsets and offsets of acoustic signals. We explored how and how well the timing of onsets and offsets of gated tones are encoded by auditory cortical neurons in awake rhesus macaques. Temporal features of this representation were isolated by presenting otherwise identical pure tones of differing durations. Cortical response patterns were diverse, including selective encoding of onset and offset transients, tonic firing, and sustained suppression. Spike train classification methods revealed that many neurons robustly encoded tone duration despite substantial diversity in the encoding process. Excellent discrimination performance was achieved by neurons whose responses were primarily phasic at tone offset and by those that responded robustly while the tone persisted. Although diverse cortical response patterns converged on effective duration discrimination, this diversity significantly constrained the utility of decoding models referenced to a spiking pattern averaged across all responses or averaged within the same response category. Using maximum likelihood-based decoding models, we demonstrated that the spike train recorded in a single trial could support direct estimation of stimulus onset and offset. Comparisons between different decoding models established the substantial contribution of bursts of activity at sound onset and offset to demarcating the temporal boundaries of gated tones. Our results indicate that relatively few neurons suffice to provide temporally precise estimates of such auditory “edges,” particularly for models that assume and exploit the heterogeneity of neural responses in awake cortex.


2012 ◽  
Vol 229 (1) ◽  
pp. 273-279 ◽  
Author(s):  
Xavier Libouton ◽  
Olivier Barbier ◽  
Yorick Berger ◽  
Leon Plaghki ◽  
Jean-Louis Thonnard

2013 ◽  
Vol 100 (3) ◽  
pp. S101
Author(s):  
O.D. Slayden ◽  
J. Kawi ◽  
C. Hergert ◽  
L.D. Martin ◽  
L.A. Holden

1994 ◽  
Vol 72 (5) ◽  
pp. 498-505 ◽  
Author(s):  
Robert H. Lamotte ◽  
Mandayam A. Srinivasan ◽  
Charles Lu ◽  
Andreas Klusch-Petersen

In the pursuit of peripheral neural representations of shape for the sense of touch, a series of two- and three-dimensional objects were stroked across the fingerpad of the anesthetized monkey and responses evoked in cutaneous mechanoreceptive primary afferent nerve fibers recorded. Responses of slowly adapting fibers (SAs) and rapidly adapting fibers (RAs) were recorded to the stroking of a cylinder, a sphere, several ellipsoids, and a pattern of alternating convex and concave cylindrical bars. The compressional force was maintained constant during a stroke, and the stroke velocities as well as orientations of the objects and stroke trajectories were varied between separate sets of trials. The major geometrical properties of the shapes were well represented in the spatiotemporal responses of the afferent fiber populations, particularly those of the SAs. Intensive parameters of shapes, such as the magnitude of change in skin curvature produced as a result of contact with the object surface, were encoded in the discharge rates of SAs and RAs, but this neural code was also influenced by changes in stroke velocity. Spatial parameters of shapes such as the extent of contact and the changes in contour that characterize a shape as belonging to a particular category (such as a sphere as opposed to a cylinder) are encoded in the spatially distributed discharge rates of the SA population. This spatial response profile provides a neural code that is probably invariant with moderate changes in the way the object comes in contact with the skin, such as the contact force or the orientation of the object.Key words: shape, cutaneous mechanoreceptors, primates, touch.


2019 ◽  
Vol 121 (6) ◽  
pp. 2237-2255 ◽  
Author(s):  
Julia Dlugaiczyk ◽  
Kathrin D. Gensberger ◽  
Hans Straka

Galvanic vestibular stimulation (GVS) plays an important role in the quest to understand sensory signal processing in the vestibular system under normal and pathological conditions. It has become a highly relevant tool to probe neuronal computations and to assist in the differentiation and treatment of vestibular syndromes. Following its accidental discovery, GVS became a diagnostic tool that generates eye movements in the absence of head/body motion. With the possibility to record extracellular and intracellular spikes, GVS became an indispensable method to activate or block the discharge in vestibular nerve fibers by cathodal and anodal currents, respectively. Bernie Cohen, in his attempt to decipher vestibular signal processing, has used this method in a number of hallmark studies that have added to our present knowledge, such as the link between selective electrical stimulation of semicircular canal nerves and the generation of directionally corresponding eye movements. His achievements paved the way for other major milestones including the differential recruitment order of vestibular fibers for cathodal and anodal currents, pronounced discharge adaptation of irregularly firing afferents, potential activation of hair cells, and fiber type-specific activation of central circuits. Previous disputes about the structural substrate for GVS are resolved by integrating knowledge of ion channel-related response dynamics of afferents, fiber type-specific innervation patterns, and central convergence and integration of semicircular canal and otolith signals. On the basis of solid knowledge of the methodology, specific waveforms of GVS are currently used in clinical diagnosis and patient treatment, such as vestibular implants and noisy galvanic stimulation.


2017 ◽  
Vol 118 (4) ◽  
pp. 2371-2377 ◽  
Author(s):  
Zoe M. Boundy-Singer ◽  
Hannes P. Saal ◽  
Sliman J. Bensmaia

The nervous system achieves stable perceptual representations of objects despite large variations in the activity patterns of sensory receptors. Here, we explore perceptual constancy in the sense of touch. Specifically, we investigate the invariance of tactile texture perception across changes in scanning speed. Texture signals in the nerve have been shown to be highly dependent on speed: temporal spiking patterns in nerve fibers that encode fine textural features contract or dilate systematically with increases or decreases in scanning speed, respectively, resulting in concomitant changes in response rate. Nevertheless, texture perception has been shown, albeit with restricted stimulus sets and limited perceptual assays, to be independent of scanning speed. Indeed, previous studies investigated the effect of scanning speed on perceived roughness, only one aspect of texture, often with impoverished stimuli, namely gratings and embossed dot patterns. To fill this gap, we probe the perceptual constancy of a wide range of textures using two different paradigms: one that probes texture perception along well-established sensory dimensions independently and one that probes texture perception as a whole. We find that texture perception is highly stable across scanning speeds, irrespective of the texture or the perceptual assay. Any speed-related effects are dwarfed by differences in percepts evoked by different textures. This remarkable speed invariance of texture perception stands in stark contrast to the strong dependence of the texture responses of nerve fibers on scanning speed. Our results imply neural mechanisms that compensate for scanning speed to achieve stable representations of surface texture. NEW & NOTEWORTHY Our brain forms stable representations of objects regardless of viewpoint, a phenomenon known as invariance that has been described in several sensory modalities. Here, we explore invariance in the sense of touch and show that the tactile perception of texture does not depend on scanning speed. This perceptual constancy implies neural mechanisms that extract information about texture from the response of nerve fibers such that the resulting neural representation is stable across speeds.


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