scholarly journals Rapid geometric feature signaling in the spiking activity of a complete population of tactile nerve fibers

2018 ◽  
Author(s):  
Benoit P. Delhaye ◽  
Xinyue Xia ◽  
Sliman J. Bensmaia
Keyword(s):  
Cortical Neurons ◽  
Time Course ◽  
Alternative Hypothesis ◽  
Nerve Fibers ◽  
Spatial Code ◽  
Geometric Feature ◽  
Dexterous Manipulation ◽  
Edge Orientation ◽  
Biomimetic Approach ◽  
Stimulus Features

AbstractTactile feature extraction is essential to guide the dexterous manipulation of objects. The longstanding theory is that geometric features at each location of contact between hand and object are extracted from the spatial layout of the response of populations of tactile nerve fibers. However, recent evidence suggests that some features (edge orientation, e.g.) are extracted very rapidly (<200ms), casting doubt that this information relies on a spatial code, which ostensibly requires integrating responses over time. An alternative hypothesis is that orientation is conveyed in precise temporal spiking patterns. Here, we simulate, using a recently developed and validated model, the responses of tactile fibers from the entire human fingertip (∼800 afferents) to edges indented into the skin. We show that edge orientation can be quickly (<50 ms) and accurately (<3°) decoded from the spatial pattern of activation across the afferent population, starting with the very first spike. Next, we implement a biomimetic decoder of edge orientation, consisting of a bank of oriented Gabor filters, designed to mimic the documented responses of cortical neurons. We find that the biomimetic approach leads to orientation decoding performance that approaches the limit set by optimal decoders and is actually more robust to changes in other stimulus features. Finally, we show that orientation signals, measured from single units in non-human primate cortex (2 macaque monkeys, 1 female), follow a time course consistent with that of their counterparts in the nerve. We conclude that a spatial code is fast and accurate enough to support object manipulation.

scholarly journals Rapid geometric feature signaling in the simulated spiking activity of a complete population of tactile nerve fibers

2019 ◽  
Vol 121 (6) ◽  
pp. 2071-2082 ◽  
Author(s):  
Benoit P. Delhaye ◽  
Xinyue Xia ◽  
Sliman J. Bensmaia
Keyword(s):  
Feature Extraction ◽  
Spatial Pattern ◽  
Time Course ◽  
Object Manipulation ◽  
Nerve Fibers ◽  
Spatial Code ◽  
Neural Population ◽  
Geometric Features ◽  
Dexterous Manipulation ◽  
Edge Orientation

Tactile feature extraction is essential to guide the dexterous manipulation of objects. The longstanding theory is that geometric features at each location of contact between hand and object are extracted from the spatial layout of the response of populations of tactile nerve fibers. However, recent evidence suggests that some features (e.g., edge orientation) are extracted very rapidly (<200 ms), casting doubt that this information relies on a spatial code, which ostensibly requires integrating responses over time. An alternative hypothesis is that orientation is conveyed in precise temporal spiking patterns. Here we simulate, using a recently developed and validated model, the responses of the two relevant subpopulations of tactile fibers from the entire human fingertip (~800 afferents) to edges indented into the skin. We show that edge orientation can be quickly (<50 ms) and accurately (<3°) decoded from the spatial pattern of activation across the afferent population, starting with the very first spike. Next, we implement a biomimetic decoder of edge orientation, consisting of a bank of oriented Gabor filters, designed to mimic the documented responses of cortical neurons. We find that the biomimetic approach leads to orientation decoding performance that approaches the limit set by optimal decoders and is actually more robust to changes in other stimulus features. Finally, we show that orientation signals, measured from single units in the somatosensory cortex of nonhuman primates (2 macaque monkeys, 1 female), follow a time course consistent with that of their counterparts in the nerve. We conclude that a spatial code is fast and accurate enough to support object manipulation. NEW & NOTEWORTHY The dexterous manipulation of objects relies on the rapid and accurate extraction of the objects’ geometric features by the sense of touch. Here we simulate the responses of all the nerve fibers that innervate the fingertip when an edge is indented into the skin and characterize the time course over which signals about its orientation evolve in this neural population. We show that orientation can be rapidly and accurately decoded from the spatial pattern of afferent activation using spatial filters that mimic the response properties of neurons in cortical somatosensory neurons along a time course consistent with that observed in cortex. We conclude that the classical model of tactile feature extraction is rapid and accurate enough to support object manipulation.

scholarly journals Changing the responses of cortical neurons from sub- to suprathreshold using single spikes in vivo

eLife ◽  
2013 ◽  
Vol 2 ◽  
Author(s):  
Verena Pawlak ◽  
David S Greenberg ◽  
Henning Sprekeler ◽  
Wulfram Gerstner ◽  
Jason ND Kerr
Keyword(s):  
Cortical Neurons ◽  
Time Course ◽  
Visual Stimulation ◽  
Spike Timing ◽  
Sensory Cortex ◽  
Sensory Coding ◽  
Computational Simulations ◽  
Subthreshold Voltage ◽  
Stimulus Features

Action Potential (APs) patterns of sensory cortex neurons encode a variety of stimulus features, but how can a neuron change the feature to which it responds? Here, we show that in vivo a spike-timing-dependent plasticity (STDP) protocol—consisting of pairing a postsynaptic AP with visually driven presynaptic inputs—modifies a neurons' AP-response in a bidirectional way that depends on the relative AP-timing during pairing. Whereas postsynaptic APs repeatedly following presynaptic activation can convert subthreshold into suprathreshold responses, APs repeatedly preceding presynaptic activation reduce AP responses to visual stimulation. These changes were paralleled by restructuring of the neurons response to surround stimulus locations and membrane-potential time-course. Computational simulations could reproduce the observed subthreshold voltage changes only when presynaptic temporal jitter was included. Together this shows that STDP rules can modify output patterns of sensory neurons and the timing of single-APs plays a crucial role in sensory coding and plasticity.

scholarly journals Information diversity in individual auditory cortical neurons is associated with functionally distinct coordinated neuronal ensembles

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jermyn Z. See ◽  
Natsumi Y. Homma ◽  
Craig A. Atencio ◽  
Vikaas S. Sohal ◽  
Christoph E. Schreiner
Keyword(s):  
Cortical Neurons ◽  
Single Neuron ◽  
Receptive Fields ◽  
Acoustic Feature ◽  
Neuronal Ensembles ◽  
Neuron Spike ◽  
Information Diversity ◽  
Feature Selectivity ◽  
Stimulus Features ◽  
Time Specific

AbstractNeuronal activity in auditory cortex is often highly synchronous between neighboring neurons. Such coordinated activity is thought to be crucial for information processing. We determined the functional properties of coordinated neuronal ensembles (cNEs) within primary auditory cortical (AI) columns relative to the contributing neurons. Nearly half of AI cNEs showed robust spectro-temporal receptive fields whereas the remaining cNEs showed little or no acoustic feature selectivity. cNEs can therefore capture either specific, time-locked information of spectro-temporal stimulus features or reflect stimulus-unspecific, less-time specific processing aspects. By contrast, we show that individual neurons can represent both of those aspects through membership in multiple cNEs with either high or absent feature selectivity. These associations produce functionally heterogeneous spikes identifiable by instantaneous association with different cNEs. This demonstrates that single neuron spike trains can sequentially convey multiple aspects that contribute to cortical processing, including stimulus-specific and unspecific information.

Dynamic coupling among neocortical neurons during evoked and spontaneous spike-wave seizure activity

1994 ◽  
Vol 72 (5) ◽  
pp. 2051-2069 ◽  
Author(s):  
M. Steriade ◽  
F. Amzica
Keyword(s):  
Cortical Neurons ◽  
Time Course ◽  
Early Stage ◽  
Field Potential ◽  
Time Lags ◽  
Temporal Relations ◽  
Intracellular Recordings ◽  
Field Potentials ◽  
Thalamic Nuclei ◽  
Spike Wave

1. We investigated the development from patterns of electroencephalogram (EEG) synchronization to paroxysms consisting of spike-wave (SW) complexes at 2–4 Hz or to seizures at higher frequencies (7–15 Hz). We used multisite, simultaneous EEG, extracellular, and intracellular recordings from various neocortical areas and thalamic nuclei of anesthetized cats. 2. The seizures were observed in 25% of experimental animals, all maintained under ketamine and xylazine anesthesia, and were either induced by thalamocortical volleys and photic stimulation or occurred spontaneously. Out of unit and field potential recordings within 370 cortical and 65 thalamic sites, paroxysmal events occurred in 70 cortical and 8 thalamic sites (approximately 18% and 12%, respectively), within which a total of 181 neurons (143 extracellular and 38 intracellular) were simultaneously recorded in various combinations of cell groups. 3. Stimulus-elicited and spontaneous SW seizures at 2–4 Hz lasted for 15–35 s and consisted of barrages of action potentials related to the spiky depth-negative (surface-positive) field potentials, followed by neuronal silence during the depth-positive wave component of SW complexes. The duration of inhibitory periods progressively increased during the seizure, at the expense of the phasic excitatory phases. 4. Intracellular recordings showed that, during such paroxysms, cortical neurons displayed a tonic depolarization (approximately 10–20 mV), sculptured by rhythmic hyperpolarizations. 5. In all cases, measures of synchrony demonstrated time lags between discharges of simultaneously recorded cortical neurons, from as short as 3–10 ms up to 50 ms or even longer intervals. Synchrony was assessed by cross-correlograms, by a method termed first-spike-analysis designed to detect dynamic temporal relations between neurons and relying on the detection of the first action potential in a spike train, and by a method termed sequential-field-correlation that analyzed the time course of field potentials simultaneously recorded from different cortical areas. 6. The degree of synchrony progressively increased from preseizure sleep patterns to the early stage of the SW seizure and, further, to its late stage. In some cases the time relation between neurons during the early stages of seizures was inversed during late stages. 7. These data show that, although the common definition of SW seizures, regarded as suddenly generalized and bilaterally synchronous activities, may be valid at the macroscopic EEG level, cortical neurons display time lags between their rhythmic spike trains, progressively increased synchrony, and changes in the temporal relations between their discharges during the paroxysms.(ABSTRACT TRUNCATED AT 400 WORDS)

Temporal Dynamics of Shape Analysis in Macaque Visual Area V2

2004 ◽  
Vol 92 (5) ◽  
pp. 3030-3042 ◽  
Author(s):  
Jay Hegdé ◽  
David C. Van Essen
Keyword(s):  
Cortical Neurons ◽  
Time Course ◽  
Temporal Dynamics ◽  
Visual Stimulation ◽  
Signal To Noise Ratio ◽  
Stimulus Onset ◽  
Visual Area ◽  
Response Modulation ◽  
Population Response ◽  
Area V2

The firing rate of visual cortical neurons typically changes substantially during a sustained visual stimulus. To assess whether, and to what extent, the information about shape conveyed by neurons in visual area V2 changes over the course of the response, we recorded the responses of V2 neurons in awake, fixating monkeys while presenting a diverse set of static shape stimuli within the classical receptive field. We analyzed the time course of various measures of responsiveness and stimulus-related response modulation at the level of individual cells and of the population. For a majority of V2 cells, the response modulation was maximal during the initial transient response (40–80 ms after stimulus onset). During the same period, the population response was relatively correlated, in that V2 cells tended to respond similarly to specific subsets of stimuli. Over the ensuing 80–100 ms, the signal-to-noise ratio of individual cells generally declined, but to a lesser degree than the evoked-response rate during the corresponding time bins, and the response profiles became decorrelated for many individual cells. Concomitantly, the population response became substantially decorrelated. Our results indicate that the information about stimulus shape evolves dynamically and relatively rapidly in V2 during static visual stimulation in ways that may contribute to form discrimination.

Synaptic Interactions Between Thalamic and Cortical Inputs Onto Cortical Neurons In Vivo

2004 ◽  
Vol 91 (5) ◽  
pp. 1990-1998 ◽  
Author(s):  
Pablo Fuentealba ◽  
Sylvain Crochet ◽  
Igor Timofeev ◽  
Mircea Steriade
Keyword(s):  
Cortical Neurons ◽  
Time Course ◽  
Input Resistance ◽  
Maximal Effect ◽  
Time Intervals ◽  
Neocortical Neurons ◽  
Synaptic Interactions ◽  
Cortical Responses ◽  
Cortical Inputs

To study the interactions between thalamic and cortical inputs onto neocortical neurons, we used paired-pulse stimulation (PPS) of thalamic and cortical inputs as well as PPS of two cortical or two thalamic inputs that converged, at different time intervals, onto intracellularly recorded cortical and thalamocortical neurons in anesthetized cats. PPS of homosynaptic cortico-cortical pathways produced facilitation, depression, or no significant effects in cortical pathways, whereas cortical responses to thalamocortical inputs were mostly facilitated at both short and long intervals. By contrast, heterosynaptic interactions between either cortical and thalamic, or thalamic and cortical, inputs generally produced decreases in the peak amplitudes and depolarization area of evoked excitatory postsynaptic potentials (EPSPs), with maximal effect at ∼10 ms and lasting from 60 to 100 ms. All neurons tested with thalamic followed by cortical stimuli showed a decrease in the apparent input resistance ( Rin), the time course of which paralleled that of decreased responses, suggesting that shunting is the factor accounting for EPSP's decrease. Only half of neurons tested with cortical followed by thalamic stimuli displayed changes in Rin. Spike shunting in the thalamus may account for those cases in which decreased synaptic responsiveness of cortical neurons was not associated with decreased Rin because thalamocortical neurons showed decreased firing probability during cortical stimulation. These results suggest a short-lasting but strong shunting between thalamocortical and cortical inputs onto cortical neurons.

scholarly journals Fast-spiking GABA circuit dynamics in the auditory cortex predict recovery of sensory processing following peripheral nerve damage

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jennifer Resnik ◽  
Daniel B Polley
Keyword(s):  
Peripheral Nerve ◽  
Auditory Cortex ◽  
Sensory Processing ◽  
Cortical Neurons ◽  
Sensory Nerve ◽  
Intracortical Inhibition ◽  
Nerve Fibers ◽  
Nerve Damage ◽  
Inhibitory Neurons ◽  
Sound Processing

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.

scholarly journals Sensory computations in the cuneate nucleus of macaques

2021 ◽  
Vol 118 (49) ◽  
pp. e2115772118
Author(s):  
Aneesha K. Suresh ◽  
Charles M. Greenspon ◽  
Qinpu He ◽  
Joshua M. Rosenow ◽  
Lee E. Miller ◽  
...  
Keyword(s):  
Cortical Neurons ◽  
Receptive Fields ◽  
Nerve Fibers ◽  
Cuneate Nucleus ◽  
Local Skin ◽  
Response Properties ◽  
Conventional View ◽  
Random Dot Patterns ◽  
Object Features ◽  
Spatiotemporal Response

Tactile nerve fibers fall into a few classes that can be readily distinguished based on their spatiotemporal response properties. Because nerve fibers reflect local skin deformations, they individually carry ambiguous signals about object features. In contrast, cortical neurons exhibit heterogeneous response properties that reflect computations applied to convergent input from multiple classes of afferents, which confer to them a selectivity for behaviorally relevant features of objects. The conventional view is that these complex response properties arise within the cortex itself, implying that sensory signals are not processed to any significant extent in the two intervening structures—the cuneate nucleus (CN) and the thalamus. To test this hypothesis, we recorded the responses evoked in the CN to a battery of stimuli that have been extensively used to characterize tactile coding in both the periphery and cortex, including skin indentations, vibrations, random dot patterns, and scanned edges. We found that CN responses are more similar to their cortical counterparts than they are to their inputs: CN neurons receive input from multiple classes of nerve fibers, they have spatially complex receptive fields, and they exhibit selectivity for object features. Contrary to consensus, then, the CN plays a key role in processing tactile information.

scholarly journals Emergence of an invariant representation of texture in primate somatosensory cortex

2019 ◽  
Author(s):  
Justin D. Lieber ◽  
Sliman J. Bensmaia
Keyword(s):  
Cortical Neurons ◽  
Rhesus Macaques ◽  
Scanning Speed ◽  
Nerve Fibers ◽  
Invariant Representation ◽  
Major Function ◽  
Neural Representations ◽  
Wide Range ◽  
Sensory Modalities ◽  
Exploratory Movements

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.

scholarly journals Left-Hemispheric Asymmetry for Object-Based Attention: an ERP Study

2019 ◽  
Vol 9 (11) ◽  
pp. 315 ◽  
Author(s):  
Andrea Orlandi ◽  
Alice Mado Proverbio
Keyword(s):  
Visual Attention ◽  
Hemispheric Asymmetry ◽  
Time Course ◽  
Electrophysiological Study ◽  
Target Selection ◽  
Neural Correlates ◽  
Specific Stimulus ◽  
Object Categories ◽  
Object Based ◽  
Stimulus Features

It has been shown that selective attention enhances the activity in visual regions associated with stimulus processing. The left hemisphere seems to have a prominent role when non-spatial attention is directed towards specific stimulus features (e.g., color, spatial frequency). The present electrophysiological study investigated the time course and neural correlates of object-based attention, under the assumption of left-hemispheric asymmetry. Twenty-nine right-handed participants were presented with 3D graphic images representing the shapes of different object categories (wooden dummies, chairs, structures of cubes) which lacked detail. They were instructed to press a button in response to a target stimulus indicated at the beginning of each run. The perception of non-target stimuli elicited a larger anterior N2 component, which was likely associated with motor inhibition. Conversely, target selection resulted in an enhanced selection negativity (SN) response lateralized over the left occipito-temporal regions, followed by a larger centro-parietal P300 response. These potentials were interpreted as indexing attentional selection and categorization processes, respectively. The standardized weighted low-resolution electromagnetic tomography (swLORETA) source reconstruction showed the engagement of a fronto-temporo-limbic network underlying object-based visual attention. Overall, the SN scalp distribution and relative neural generators hinted at a left-hemispheric advantage for non-spatial object-based visual attention.

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