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

Artificial forms of mechanical limb stimulation are used within multiple fields of study to determine the level of cortical excitability and to map the trajectory of neuronal recovery from cortical damage or disease. Square-wave mechanical or electrical stimuli are often used in these studies, but a characterization of sensory-evoked response properties to square-waves with distinct fundamental frequencies but overlapping harmonics has not been performed. To distinguish between somatic stimuli, the primary somatosensory cortex must be able to represent distinct stimuli with unique patterns of activity, even if they have overlapping features. Thus, mechanical square-wave stimulation was used in conjunction with regional and cellular imaging to examine regional and cellular response properties evoked by different frequencies of stimulation. 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 square-wave 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 responding to various frequencies of square-wave stimuli 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 stimulation. High frequency stimuli were shown to elicit more population activity, 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 different square-wave 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 neurons.

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

10.1101/2020.07.14.202101 ◽

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.

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Spatio-Temporal Subthreshold Receptive Fields in the Vibrissa Representation of Rat Primary Somatosensory Cortex

Journal of Neurophysiology ◽

10.1152/jn.1998.80.6.2882 ◽

1998 ◽

Vol 80 (6) ◽

pp. 2882-2892 ◽

Cited By ~ 214

Author(s):

Christopher I. Moore ◽

Sacha B. Nelson

Keyword(s):

Receptive Field ◽

Somatosensory Cortex ◽

Rise Time ◽

Cortical Plasticity ◽

Temporal Dynamics ◽

Receptive Fields ◽

Excitatory Input ◽

Primary Somatosensory Cortex ◽

Spatio Temporal ◽

Sensory Evoked

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.

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Optogenetic Modulation of a Minor Fraction of Parvalbumin-Positive Interneurons Specifically Affects Spatiotemporal Dynamics of Spontaneous and Sensory-Evoked Activity in Mouse Somatosensory Cortex in Vivo

Cerebral Cortex ◽

10.1093/cercor/bhx261 ◽

2017 ◽

Vol 27 (12) ◽

pp. 5784-5803 ◽

Cited By ~ 9

Author(s):

Jenq-Wei Yang ◽

Pierre-Hugues Prouvot ◽

Vicente Reyes-Puerta ◽

Maik C Stüttgen ◽

Albrecht Stroh ◽

...

Keyword(s):

Somatosensory Cortex ◽

Spatiotemporal Dynamics ◽

Minor Fraction ◽

Evoked Activity ◽

Sensory Evoked ◽

A Minor

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

Journal of Neurophysiology ◽

10.1152/jn.1994.72.5.2438 ◽

1994 ◽

Vol 72 (5) ◽

pp. 2438-2450 ◽

Cited By ~ 85

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.

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

Journal of Neurophysiology ◽

10.1152/jn.1987.57.6.1-a ◽

1987 ◽

Vol 57 (6) ◽

pp. 1-1 ◽

Cited By ~ 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.

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Diverse roles for the posteromedial thalamus in sensory evoked cortical plasticity

Journal of Neurophysiology ◽

10.1152/jn.00291.2020 ◽

2020 ◽

Author(s):

Matthew James Buchan ◽

Gemma Gothard ◽

Alexander von Klemperer ◽

Joram J van Rheede

Keyword(s):

Somatosensory Cortex ◽

Cortical Plasticity ◽

Primary Somatosensory Cortex ◽

Somatosensory Processing ◽

Sensory Evoked

The posteromedial thalamus (POm) has extensive recurrent connectivity with the whisker-related primary somatosensory cortex (wS1) of rodents. However, its functional contribution to somatosensory processing in wS1 remains unclear. This article reviews several recent findings which begin to elucidate the role of POm in sensory evoked plasticity and discusses their implications for somatosensory processing.

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

Journal of Neurophysiology ◽

10.1152/jn.1987.57.1.1-a ◽

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.

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

Journal of Neurophysiology ◽

10.1152/jn.1994.72.6.2827 ◽

1994 ◽

Vol 72 (6) ◽

pp. 2827-2839 ◽

Cited By ~ 14

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.

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