scholarly journals Emergence of an Invariant Representation of Texture in Primate Somatosensory Cortex

2019 ◽  
Vol 30 (5) ◽  
pp. 3228-3239 ◽  
Author(s):  
Justin D Lieber ◽  
Sliman J Bensmaia

Abstract A 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 (from Brodmann areas 3b, 1, and 2). 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.

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.


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.


2018 ◽  
Author(s):  
Justin D. Lieber ◽  
Sliman J. Bensmaia

SummaryIn the somatosensory nerves, the tactile perception of texture is driven by spatial and temporal patterns of activation distributed across three populations of afferents. These disparate streams of information must then be integrated centrally to achieve a unified percept of texture. To investigate the representation of texture in somatosensory cortex, we scanned a wide range of natural textures across the fingertips of Rhesus macaques and recorded the responses evoked in Brodmann’s areas 3b, 1, and 2. We found that texture identity is reliably encoded in the idiosyncratic responses of populations of cortical neurons, giving rise to a high-dimensional representation of texture. Cortical neurons fall along a continuum in their sensitivity to fine vs. coarse texture, and neurons at the extrema of this continuum seem to receive their major input from different afferent populations. Finally, we show that cortical responses can account for several aspects of texture perception in humans.


2019 ◽  
Vol 116 (8) ◽  
pp. 3268-3277 ◽  
Author(s):  
Justin D. Lieber ◽  
Sliman J. Bensmaia

In the somatosensory nerves, the tactile perception of texture is driven by spatial and temporal patterns of activation distributed across three populations of afferents. These disparate streams of information must then be integrated centrally to achieve a unified percept of texture. To investigate the representation of texture in somatosensory cortex, we scanned a wide range of natural textures across the fingertips of rhesus macaques and recorded the responses evoked in Brodmann’s areas 3b, 1, and 2. We found that texture identity is reliably encoded in the idiosyncratic responses of populations of cortical neurons, giving rise to a high-dimensional representation of texture. Cortical neurons fall along a continuum in their sensitivity to fine vs. coarse texture, and neurons at the extrema of this continuum seem to receive their major input from different afferent populations. Finally, we show that cortical responses can account for several aspects of texture perception in humans.


2021 ◽  
Vol 22 (13) ◽  
pp. 6845
Author(s):  
Rebecca L. Pratt

The buzz about hyaluronan (HA) is real. Whether found in face cream to increase water volume loss and viscoelasticity or injected into the knee to restore the properties of synovial fluid, the impact of HA can be recognized in many disciplines from dermatology to orthopedics. HA is the most abundant polysaccharide of the extracellular matrix of connective tissues. HA can impact cell behavior in specific ways by binding cellular HA receptors, which can influence signals that facilitate cell survival, proliferation, adhesion, as well as migration. Characteristics of HA, such as its abundance in a variety of tissues and its responsiveness to chemical, mechanical and hormonal modifications, has made HA an attractive molecule for a wide range of applications. Despite being discovered over 80 years ago, its properties within the world of fascia have only recently received attention. Our fascial system penetrates and envelopes all organs, muscles, bones and nerve fibers, providing the body with a functional structure and an environment that enables all bodily systems to operate in an integrated manner. Recognized interactions between cells and their HA-rich extracellular microenvironment support the importance of studying the relationship between HA and the body’s fascial system. From fasciacytes to chronic pain, this review aims to highlight the connections between HA and fascial health.


1995 ◽  
Vol 73 (5) ◽  
pp. 1876-1891 ◽  
Author(s):  
M. B. Calford ◽  
M. N. Semple

1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level-dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking-derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the "tuning" of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker.(ABSTRACT TRUNCATED AT 400 WORDS)


1991 ◽  
Vol 66 (4) ◽  
pp. 1156-1165 ◽  
Author(s):  
V. L. Smith-Swintosky ◽  
C. R. Plata-Salaman ◽  
T. R. Scott

1. Extracellular action potentials were recorded from 50 single neurons in the insular-opercular cortex of two alert cynomolgus monkeys during gustatory stimulation of the tongue and palate. 2. Sixteen stimuli, including salts, sugars, acids, alkaloids, monosodium glutamate, and aspartame, were chosen to represent a wide range of taste qualities. Concentrations were selected to elicit a moderate gustatory response, as determined by reference to previous electrophysiological data or to the human psychophysical literature. 3. The cortical region over which taste-evoked activity could be recorded included the frontal operculum and anterior insula, an area of approximately 75 mm3. Taste-responsive cells constituted 50 (2.7%) of the 1,863 neurons tested. Nongustatory cells responded to mouth movement (20.7%), somatosensory stimulation of the tongue (9.6%), stimulus approach or anticipation (1.7%), and tongue extension (0.6%). The sensitivities of 64.6% of these cortical neurons could not be identified by our stimulation techniques. 4. Taste cells had low spontaneous activity levels (3.7 +/- 3.0 spikes/s, mean +/- SD) and showed little inhibition. They were moderately broadly tuned, with a mean entropy coefficient of 0.76 +/- 0.17. Excitatory responses were typically not robust. 5. Hierarchical cluster analysis was used to determine whether neurons could be divided into discrete types, as defined by their response profiles to the entire stimulus array. There was an apparent division of response profiles into four general categories, with primary sensitivities to sodium (n = 18), glucose (n = 15), quinine (n = 12), and acid (n = 5). However, these categories were not statistically independent. Therefore the notion of functionally distinct neuron types was not supported by an analysis of the distribution of response profiles. It was the case, however, that neurons in the sodium category could be distinguished from other neurons by their relative specificity. 6. The similarity among the taste qualities represented by this stimulus array was assessed by calculating correlations between the activity profiles they elicited from these 50 neurons. The results generally confirmed expectations derived from human psychophysical studies. In a multidimensional representation of stimulus similarity, there were groups that contained acids, sodium salts, and chemicals that humans label bitter and sweet. 7. The small proportion of insular-opercular neurons that are taste sensitive and the low discharge rates that taste stimuli are able to evoke from them suggest a wider role for this cortical area than just gustatory coding.(ABSTRACT TRUNCATED AT 400 WORDS)


2003 ◽  
Vol 89 (6) ◽  
pp. 3070-3082 ◽  
Author(s):  
Jason S. Rothman ◽  
Paul B. Manis

In the ventral cochlear nucleus (VCN), neurons transform information from auditory nerve fibers into a set of parallel ascending pathways, each emphasizing different aspects of the acoustic environment. Previous studies have shown that VCN neurons differ in their intrinsic electrical properties, including the K+ currents they express. In this study, we examine these K+ currents in more detail using whole cell voltage-clamp techniques on isolated VCN cells from adult guinea pigs at 22°C. Our results show a differential expression of three distinct K+ currents. Whereas some VCN cells express only a high-threshold delayed-rectifier-like current ( IHT), others express IHT in combination with a fast inactivating current ( IA) and/or a slow-inactivating low-threshold current ( ILT). IHT, ILT, and IA, were partially blocked by 1 mM 4-aminopyridine. In contrast, only ILT was blocked by 10–100 nM dendrotoxin-I. A surprising finding was the wide range of levels of ILT, suggesting ILT is expressed as a continuum across cell types rather than modally in a particular cell type. IA, on the other hand, appears to be expressed only in cells that show little or no ILT, the Type I cells. Boltzmann analysis shows IHT activates with 164 ± 12 (SE) nS peak conductance, -14.3 ± 0.7 mV half-activation, and 7.0 ± 0.5 mV slope factor. Similar analysis shows ILT activates with 171 ± 22 nS peak conductance, -47.4 ± 1.0 mV half-activation, and 5.8 ± 0.3 mV slope factor.


2004 ◽  
Vol 92 (2) ◽  
pp. 959-976 ◽  
Author(s):  
Renaud Jolivet ◽  
Timothy J. Lewis ◽  
Wulfram Gerstner

We demonstrate that single-variable integrate-and-fire models can quantitatively capture the dynamics of a physiologically detailed model for fast-spiking cortical neurons. Through a systematic set of approximations, we reduce the conductance-based model to 2 variants of integrate-and-fire models. In the first variant (nonlinear integrate-and-fire model), parameters depend on the instantaneous membrane potential, whereas in the second variant, they depend on the time elapsed since the last spike [Spike Response Model (SRM)]. The direct reduction links features of the simple models to biophysical features of the full conductance-based model. To quantitatively test the predictive power of the SRM and of the nonlinear integrate-and-fire model, we compare spike trains in the simple models to those in the full conductance-based model when the models are subjected to identical randomly fluctuating input. For random current input, the simple models reproduce 70–80 percent of the spikes in the full model (with temporal precision of ±2 ms) over a wide range of firing frequencies. For random conductance injection, up to 73 percent of spikes are coincident. We also present a technique for numerically optimizing parameters in the SRM and the nonlinear integrate-and-fire model based on spike trains in the full conductance-based model. This technique can be used to tune simple models to reproduce spike trains of real neurons.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jennifer Resnik ◽  
Daniel B Polley

Cortical neurons remap their receptive fields and rescale sensitivity to spared peripheral inputs following sensory nerve damage. To address how these plasticity processes are coordinated over the course of functional recovery, we tracked receptive field reorganization, spontaneous activity, and response gain from individual principal neurons in the adult mouse auditory cortex over a 50-day period surrounding either moderate or massive auditory nerve damage. We related the day-by-day recovery of sound processing to dynamic changes in the strength of intracortical inhibition from parvalbumin-expressing (PV) inhibitory neurons. Whereas the status of brainstem-evoked potentials did not predict the recovery of sensory responses to surviving nerve fibers, homeostatic adjustments in PV-mediated inhibition during the first days following injury could predict the eventual recovery of cortical sound processing weeks later. These findings underscore the potential importance of self-regulated inhibitory dynamics for the restoration of sensory processing in excitatory neurons following peripheral nerve injuries.


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