scholarly journals Refractoriness accounts for variable spike burst responses in somatosensory cortex

2017 ◽  
Author(s):  
Bartosz Teleńczuk ◽  
Richard Kempter ◽  
Gabriel Curio ◽  
Alain Destexhe
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Single Neuron ◽  
Primary Somatosensory Cortex ◽  
General Mechanism ◽  
Population Activity ◽  
Synaptic Inputs ◽  
Neuron Spike ◽  
Biophysical Mechanism ◽  
Spike Patterns

AbstractNeurons in the primary somatosensory cortex (S1) respond to peripheral stimulation with synchronised bursts of spikes, which lock to the macroscopic 600 Hz EEG waves. The mechanism of burst generation and synchronisation in S1 is not yet understood. Using models of single-neuron responses fitted to unit recordings from macaque monkeys, we show that these synchronised bursts are the consequence of correlated synaptic inputs combined with a refractory mechanism. In the presence of noise these models reproduce also the observed trial-to-trial response variability, where individual bursts represent one of many stereotypical temporal spike patterns. When additional slower and global excitability fluctuations are introduced the single-neuron spike patterns are correlated with the population activity, as demonstrated in experimental data. The underlying biophysical mechanism of S1 responses involves thalamic inputs arriving through depressing synapses to cortical neurons in a high-conductance state. Our findings show that a simple feedforward processing of peripheral inputs could give rise to neuronal responses with non-trivial temporal and population statistics. We conclude that neural systems could use refractoriness to encode variable cortical states into stereotypical short-term spike patterns amenable to processing at neuronal time scales (tens of milliseconds).Significance statementNeurons in the hand area of the primary somatosensory cortex respond to repeated presentation of the same stimulus with variable sequences of spikes, which can be grouped into distinct temporal spike patterns. In a simplified model, we show that such spike patterns are product of synaptic inputs and intrinsic neural properties. This model can reproduce both single-neuron and population responses only when a private variability in each neuron is combined with a multiplicative gain shared over whole population, which fluctuates over trials and might represent the dynamical state of the early stages of sensory processing. This phenomenon exemplifies a general mechanism of transforming the ensemble cortical states into precise temporal spike patterns at the level of single neurons.

Intrinsic discharge patterns and somatosensory inputs for neurons in raccoon primary somatosensory cortex

1994 ◽  
Vol 72 (6) ◽  
pp. 2827-2839 ◽  
Author(s):  
P. J. Istvan ◽  
P. Zarzecki
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Primary Somatosensory Cortex ◽  
Membrane Properties ◽  
Postsynaptic Potentials ◽  
Synaptic Inputs ◽  
Ionic Conductances ◽  
Discharge Patterns ◽  
Intrinsic Membrane Properties ◽  
Stimulation Of

1. Discharge patterns of neurons are regulated by synaptic inputs and by intrinsic membrane properties such as their complement of ionic conductances. Discharge patterns evoked by synaptic inputs are often used to identify the source and modality of sensory input. However, the interpretation of these discharge patterns may be complicated if different neurons respond to the same synaptic input with a variety of discharge patterns due to differences in intrinsic membrane properties. The purposes of this study were 1) to investigate intrinsic discharge patterns of neurons in primary somatosensory cortex of raccoon in vivo and 2) to use somatosensory postsynaptic potentials evoked by stimulation of forepaw digits to determine thalamocortical connectivity for the same neurons. 2. Conventional intracellular recordings with sharp electrodes were made from 121 neurons in the cortical representation of glabrous skin of digit four (d4). Intracellular injection of identical current pulses (100-120 ms in duration) elicited various patterns of discharge in different neurons. Neurons were classified on the basis of these intrinsic patterns of discharge, rates of spike adaptation, and characteristics of spike waveforms. Three main groups were identified: regular spiking (RS) neurons, intrinsic bursting (IB) neurons, and fast spiking (FS) neurons. Subclasses were identified for the RS and IB groups. 3. Neurons were tested for somatosensory inputs by stimulating electrically d3, d4, and d5. Excitatory postsynaptic potentials (EPSPs) were elicited in 100% of the neurons by electrical stimulation of d4, the "on-focus" digit. EPSPs were usually followed by inhibitory postsynaptic potentials (IPSPs). Many neurons (41%) responded with EPSP-IPSP sequences after stimulation of d3 or d5, the "off-focus" digits. 4. Latencies of somatosensory EPSPs and IPSPs were used to determine the synaptic order in the cortical circuitry of RS, IB, and FS neurons. EPSPs with monosynaptic thalamocortical latencies were recorded in RS, IB, and FS neurons. 5. We conclude that precise patterns of neural discharge in primary somatosensory cortex cannot be reliable estimates of sensory inputs reaching these neurons because patterns of discharge are so strongly influenced by intrinsic membrane properties. Ionic conductances governing patterns of neuronal discharge seem almost identical in intact cortex of raccoon, rat, and cat, and in slices of rodent cortex, because similar patterns of discharge are found. The consistency of patterns of discharge across species and types of preparation suggests that these intrinsic membrane properties are a general property of cerebral cortical neurons and should be considered when evaluation sensory coding by these neurons.

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.

Effects of 5-HT on thalamocortical synaptic transmission in the developing rat

1994 ◽  
Vol 72 (5) ◽  
pp. 2438-2450 ◽  
Author(s):  
R. W. Rhoades ◽  
C. A. Bennett-Clarke ◽  
M. Y. Shi ◽  
R. D. Mooney
Keyword(s):  
Synaptic Transmission ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Input Resistance ◽  
Inhibitory Effect ◽  
Primary Somatosensory Cortex ◽  
Excitatory Postsynaptic Potential ◽  
Dependent Manner ◽  
Cortical Cells ◽  
Thalamocortical Axons

1. Recent immunocytochemical and receptor binding data have demonstrated a transient somatotopic patterning of serotonin (5-HT)-immunoreactive fibers in the primary somatosensory cortex of developing rats and a transient expression of 5-HT1B receptors on thalamocortical axons from the ventral posteromedial thalamic nucleus (VPM). 2. These results suggest that 5-HT should strongly modulate thalamocortical synaptic transmission for a limited time during postnatal development. This hypothesis was tested in intracellular recording experiments carried out in thalamocortical slice preparations that included VPM, the thalamic radiations, and the primary somatosensory cortex. Effects of 5-HT and analogues were monitored on membrane potentials and input resistances of cortical neurons and on the amplitude of the synaptic potentials evoked in them by stimulation of VPM. 3. Results obtained from cortical neurons in slices taken from rats during the first 2 wk of life indicated that 5-HT strongly inhibited the VPM-evoked excitatory postsynaptic potential (EPSP) recorded from cortical neurons in a dose-dependent manner. In contrast, 5-HT had no significant effects on membrane potential, input resistance, or depolarizations induced by direct application of glutamic acid to cortical cells. 4. The effects of 5-HT were mimicked by the 5-HT1B receptor agonists 1-[3-(trifluoromethyl)phenyl]-piperazine (TFMPP) and 7-trifluoromethyl-4(4-methyl-1-piperazinyl)-pyrrolo[1,2-a]-quinoxaline maleate and antagonized by the 5-HT1B receptor antagonist (-)-pindolol. The 5-HT1A agonist [(+/-)8-hydroxydipropylaminotetralin HBr] (8-OH-DPAT) had less effect on the VPM-elicited EPSP, and the effects of 5-HT upon this response were generally not antagonized by either 1-(2-methoxyphenyl)-4-[4-(2- phthalimmido)butyl]piperazine HBr (a 5-HT1A antagonist) or ketanserine (a 5-HT2 antagonist) or spiperone (a 5-HT1A and 2 antagonist). 5. The ability of 5-HT to inhibit the VPM-evoked EPSP in cortical neurons was significantly reduced in slices from animals > 2 wk of age. The effectiveness of TFMPP in such animals was even more attenuated than that of 5-HT, and the effectiveness of 8-OH-DPAT was unchanged with age. These results are consistent with the disappearance of 5-HT1B receptors from thalamocortical axons after the second postnatal week and the maintenance of 5-HT1A receptors on some neurons. 6. All of the results obtained in this study are consistent with the conclusion that 5-HT has a profound, but developmentally transient, presynaptic inhibitory effect upon thalamocortical transmission in the rat's somatosensory cortex.

Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys

1987 ◽  
Vol 57 (6) ◽  
pp. 1-1 ◽  
Author(s):  
S. Warren ◽  
H. A. Hamalainen ◽  
E. P. Gardner
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Weighted Average ◽  
Direction Selectivity ◽  
Primary Somatosensory Cortex ◽  
Objective Classification

S. Warren, H. A. Hamalainen, and E. P. Gardner, “Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys.” It was incorrectly stated that Orban and co-workers(J. Neurophysiol. 45: 1059–1073, 1981) attributed direction selectivity to cortical neurons having a direction index (DI) ge 20. Orban et al. actually used a weighted average of DIs and defined cells with a mean DI (MDI) above 50 as direction selective. Their criterion for direction selectivity was stricter and not less stringent, as stated in the paper. This error does not alter any of the data or conclusions of Warren et al.

Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys

1987 ◽  
Vol 57 (1) ◽  
pp. 1-1
Author(s):  
S. Warren ◽  
H. A. Hamalainen ◽  
E. P. Gardner
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Weighted Average ◽  
Direction Selectivity ◽  
Primary Somatosensory Cortex ◽  
Objective Classification

S. Warren, H. A. Hamalainen, and E. P. Gardner, “Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys.” It was incorrectly stated that Orban and co-workers ( J. Neurophysiol. 45: 1059–1073, 1981) attributed direction selectivity to cortical neurons having a direction index (DI)≥20. Orban et al. actually used a weighted average of DIs and defined cells with a mean DI (MDI) above 50 as direction selective. Their criterion for direction selectivity was stricter and not less stringent, as stated in the paper. This error does not alter any of the data or conclusions of Warren et al.

scholarly journals Distinct patterns of activity in individual cortical neurons and local networks in primary somatosensory cortex of mice evoked by mechanical limb stimulation

2020 ◽  
Author(s):  
Mischa V. Bandet ◽  
Bin Dong ◽  
Ian R. Winship
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Optical Recording ◽  
Primary Somatosensory Cortex ◽  
Autofluorescence Imaging ◽  
Neuronal Activation ◽  
Local Networks ◽  
Two Photon ◽  
Evoked Activity ◽  
Sensory Evoked

AbstractTo distinguish between somatic stimuli, the primary somatosensory cortex should process dissimilar stimuli with distinct patterns of neuronal activation. Two-photon calcium imaging permits simultaneous optical recording of sensory evoked activity in hundreds of cortical neurons during varied sensory stimulation. Hence, it allows a visualization of patterns of activity in individual neurons and local cortical networks in response to distinct stimulation. Here, flavoprotein autofluorescence imaging was used to map the somatosensory cortex of anaesthetized C57BL/6 mice, and in vivo two-photon Ca2+ imaging was used to define patterns of neuronal activation during mechanical stimulation of the contralateral forelimb or hindlimb at various frequencies (3, 10, 100, 200, and 300 Hz). The data revealed that neurons within the limb associated somatosensory cortex exhibit stimulus-specific patterns of activity. Subsets of neurons were found to have sensory-evoked activity that is either primarily responsive to single stimulus frequencies or broadly responsive to multiple frequencies of limb movement. High frequency stimuli were shown to elicit more activation across the population, with a greater percentage of the population responding and greater percentage of cells with high amplitude responses. Stimulus-evoked cell-cell correlations within these neuronal networks varied as a function of frequency of stimulation, such that each stimulus elicited a distinct pattern that was more consistent across multiple trials of the same stimulus compared to trials at different frequencies of stimulation. The variation in cortical response to these artificial stimuli can thus be represented by the population pattern of supra-threshold Ca2+ transients, the magnitude and temporal properties of the evoked activity, and the structure of the stimulus-evoked correlation between responsive neurons.

Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys

1986 ◽  
Vol 56 (3) ◽  
pp. 598-622 ◽  
Author(s):  
S. Warren ◽  
H. A. Hamalainen ◽  
E. P. Gardner
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Statistical Tests ◽  
Direction Selectivity ◽  
Primary Somatosensory Cortex ◽  
Relative Distribution ◽  
Textured Surfaces ◽  
Simple Method ◽  
Firing Rates ◽  
Moving Stimuli

In order to classify movement-sensitive neurons in SI cortex, and to estimate their relative distribution, we have developed a new simple method for controlled motion of textured surfaces across the skin, as well as a set of objective criteria for determining direction selectivity. Moving stimuli were generated using 5 mm thick precision gear wheels, whose teeth formed a grafting. They were mounted on the shafts of low-torque potentiometers (to measure the speed and direction of movement) and rolled manually across the skin using the potentiometer shaft as an axle. As the grafting wheel was advanced, its ridges sequentially contacted a specific set of points on the skin, leaving gaps of defined spacing that were unstimulated. This stimulus was reproducible from trial to trial and produced little distention of the skin. Three objective criteria were used to categorize responses: the ratio of responses to motion in the most and least preferred directions [direction index (DI)], the difference between mean firing rates in the two directions divided by the average standard deviation [index of discriminability (delta'e)], and statistical tests. Neurons were classified as direction sensitive if DI greater than 35, delta's greater than or equal to 1.35 (equivalent to 75% correct discrimination by an unbiased observer), and firing rates in most- and least-preferred directions were significantly different (P less than 0.05). Good agreement was found between the three classification schemes. Recordings were made from 1,020 cortical neurons in the hand and forearm regions of primary somatosensory cortex (areas 3b, 1 and 2) of five macaque monkeys. Tangential motion across the skin was found to be an extremely effective stimulus for SI cortical neurons. Two hundred eighty six of 757 tactile neurons (38%) responded more vigorously to moving stimuli than to pressure or tapping the skin. One hundred twenty-one cells were tested with moving gratings and were classified according to their ability to differentiate movement in longitudinal and transverse directions. Responses to the moving gratings resembled those observed when stroking the skin with brushed, edges, or blunt probes. Three major types of firing patterns were found: motion sensitive, direction sensitive, and orientation sensitive. Motion-sensitive neurons (37%) responded to movement in both longitudinal and transverse directions with only slight difference in firing rates and interval distributions. Responses throughout the field were fairly uniform, and no clear point of maximum sensitivity was apparent. Direction-sensitive neurons (60%) displayed clear preferences for movement in one or more directions.4

scholarly journals Effects of spatiotemporal stimulus properties on spike timing correlations in owl monkey primary somatosensory cortex

2012 ◽  
Vol 108 (12) ◽  
pp. 3353-3369 ◽  
Author(s):  
Jamie L. Reed ◽  
Pierre Pouget ◽  
Hui-Xin Qi ◽  
Zhiyi Zhou ◽  
Melanie R. Bernard ◽  
...  
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Stimulus Onset ◽  
Spike Timing ◽  
Primary Somatosensory Cortex ◽  
Spatial Proximity ◽  
Electrode Arrays ◽  
Paired Stimuli ◽  
Tactile Stimuli ◽  
Source Of Information

The correlated discharges of cortical neurons in primary somatosensory cortex are a potential source of information about somatosensory stimuli. One aspect of neuronal correlations that has not been well studied is how the spatiotemporal properties of tactile stimuli affect the presence and magnitude of correlations. We presented single- and dual-point stimuli with varying spatiotemporal relationships to the hands of three anesthetized owl monkeys and recorded neuronal activity from 100-electrode arrays implanted in primary somatosensory cortex. Correlation magnitudes derived from joint peristimulus time histogram (JPSTH) analysis of single neuron pairs were used to determine the level of spike timing correlations under selected spatiotemporal stimulus conditions. Correlated activities between neuron pairs were commonly observed, and the proportions of correlated pairs tended to decrease with distance between the recorded neurons. Distance between stimulus sites also affected correlations. When stimuli were presented simultaneously at two sites, ∼37% of the recorded neuron pairs showed significant correlations when adjacent phalanges were stimulated, and ∼21% of the pairs were significantly correlated when nonadjacent digits were stimulated. Spatial proximity of paired stimuli also increased the average correlation magnitude. Stimulus onset asynchronies in the paired stimuli had small effects on the correlation magnitude. These results show that correlated discharges between neurons at the first level of cortical processing provide information about the relative locations of two stimuli on the hand.

Neuronal correlates of tactile speed in primary somatosensory cortex

2013 ◽  
Vol 110 (7) ◽  
pp. 1554-1566 ◽  
Author(s):  
Alexandra Dépeault ◽  
El-Mehdi Meftah ◽  
C. Elaine Chapman
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Primary Somatosensory Cortex ◽  
Spatial Period ◽  
Speed Scaling ◽  
Brain Extracts ◽  
Texture Sensitivity ◽  
Hand Region ◽  
The Brain ◽  
Area 3B

Moving stimuli activate all of the mechanoreceptive afferents involved in discriminative touch, but their signals covary with several parameters, including texture. Despite this, the brain extracts precise information about tactile speed, and humans can scale the tangential speed of moving surfaces as long as they have some surface texture. Speed estimates, however, vary with texture: lower estimates for rougher surfaces (increased spatial period, SP). We hypothesized that the discharge of cortical neurons playing a role in scaling tactile speed should covary with speed and SP in the same manner. Single-cell recordings ( n = 119) were made in the hand region of primary somatosensory cortex (S1) of awake monkeys while raised-dot surfaces (longitudinal SPs, 2–8 mm; periodic or nonperiodic) were displaced under their fingertips at speeds of 40–105 mm/s. Speed sensitivity was widely distributed (area 3b, 13/25; area 1, 32/51; area 2, 31/43) and almost invariably combined with texture sensitivity (82% of cells). A subset of cells (27/64 fully tested speed-sensitive cells) showed a graded increase in discharge with increasing speed for testing with both sets of surfaces (periodic, nonperiodic), consistent with a role in tactile speed scaling. These cells were almost entirely confined to caudal S1 (areas 1 and 2). None of the speed-sensitive cells, however, showed a pattern of decreased discharge with increased SP, as found for subjective speed estimates in humans. Thus further processing of tactile motion signals, presumably in higher-order areas, is required to explain human tactile speed scaling.

scholarly journals Convergence of Submodality-Specific Input Onto Neurons in Primary Somatosensory Cortex

2009 ◽  
Vol 102 (3) ◽  
pp. 1843-1853 ◽  
Author(s):  
Yu-Cheng Pei ◽  
Peter V. Denchev ◽  
Steven S. Hsiao ◽  
James C. Craig ◽  
Sliman J. Bensmaia
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Stimulus Onset ◽  
Sustained Response ◽  
Primary Somatosensory Cortex ◽  
Stimulus Interval ◽  
Specific Input ◽  
Afferent Fibers ◽  
Cortical Responses ◽  
Different Populations

At the somatosensory periphery, slowly adapting type 1 (SA1) and rapidly adapting (RA) afferents respond very differently to step indentations: SA1 afferents respond throughout the entire stimulus interval (sustained response), whereas RA afferents respond only at stimulus onset (on response) and offset (off response). We recorded the responses of cortical neurons to step indentations and found many neurons in areas 3b and 1 to exhibit properties that are intermediate between these two extremes: These neurons responded during the sustained portion of the stimulus and also at the offset of the stimulus. Several lines of evidence indicate that these neurons, which exist in large proportions even at these early stages of somatosensory cortical processing, receive input from both populations of afferents. First, we show that many cortical neurons have both a significant sustained response and a significant off response. Second, the strength of the off response is uncorrelated with that of the sustained response, which is to be expected if sustained and off responses stem from different populations of afferent fibers. Third, the bulk of the variance in cortical responses to step indentations can be accounted for using a linear combination of both SA1 and RA responses. Finally, we show that the off response in cortical neurons does not reflect rebound from inhibition. We conclude that the convergence of modality specific input onto individual neurons is common in primary somatosensory cortex and discuss how this conclusion might be reconciled with previous findings.

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