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.

Synaptic mechanisms of cortical representational plasticity: somatosensory and corticocortical EPSPs in reorganized raccoon SI cortex

1993 ◽  
Vol 69 (5) ◽  
pp. 1422-1432 ◽  
Author(s):  
P. Zarzecki ◽  
S. Witte ◽  
E. Smits ◽  
D. C. Gordon ◽  
P. Kirchberger ◽  
...  
Keyword(s):  
Somatosensory Cortex ◽  
Intracellular Recording ◽  
Cortical Neurons ◽  
Primary Somatosensory Cortex ◽  
Cortical Representation ◽  
Synaptic Connections ◽  
Excitatory Postsynaptic Potentials ◽  
Postsynaptic Potentials ◽  
Cerebral Neocortex ◽  
Synaptic Mechanisms

1. Reorganizations of representational maps have been described for a variety of sensory and motor regions of cerebral neocortex in several species. The purpose of this study was to investigate synaptic mechanisms of the reorganizations of primary somatosensory cortex that follow removal of a digit or the joining of two digits into a syndactyly. We examined neurons in the cortical representation of digit 4 (d4). Intracellular recording was used to compare somatosensory and corticocortical excitatory postsynaptic potentials (EPSPs) in normal raccoons, with EPSPs recorded in two experimental groups of animals surviving for a mean of 22 wk after removal of d4, or union of d4 with digit 3 (d3). 2. In normal animals with d4 intact, EPSPs were evoked from this on-focus digit in 100% of cortical neurons. EPSPs were evoked from d3 and digit 5 (off-focus digits) in only a minority of neurons in normal raccoons. The incidence of somatosensory EPSPs from off-focus digits increased dramatically after removal of d4 or its union with d3. Latencies of EPSPs evoked from off-focus digits decreased after d4 removal, so that they were as short as latencies from d4 in normal animals. In contrast, for the group of animals with d3-d4 syndactyly, latencies of EPSPs from off-focus digits were not shorter than responses from these digits in normal animals. 3. Corticocortical EPSPs were no more common in animals with d4 removed than in intact animals. Furthermore, corticocortical EPSPs after d4 removal did not differ in their latencies, amplitudes, half-widths, or integrated amplitudes. The only detected change was that corticocortical EPSPs had faster rising phases after removal of d4. In contrast, after d3-d4 syndactyly, corticocortical EPSPs were more common than in normal animals. 4. Digit removal and digital syndactyly had distinctive effects on somatosensory and corticocortical EPSPs. These results do not identify unique synaptic mechanisms for cortical representational plasticity, nor do they specify the involved CNS site(s). Several synaptic mechanisms consistent with the results are considered in the DISCUSSION, including synaptic proliferation to form new synaptic connections and enhanced effectiveness of existing corticocortical synapses.

scholarly journals Responses of neurons in the primary somatosensory cortex to itch- and pain-producing stimuli in rats

2020 ◽  
Vol 123 (5) ◽  
pp. 1944-1954 ◽  
Author(s):  
Sergey G. Khasabov ◽  
Hai Truong ◽  
Victoria M. Rogness ◽  
Kevin D. Alloway ◽  
Donald A. Simone ◽  
...  
Keyword(s):  
Cerebral Cortex ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Small Area ◽  
Single Unit ◽  
Electrophysiological Study ◽  
Primary Somatosensory Cortex ◽  
Itch Sensation ◽  
The Face ◽  
Stimulation Of

Processing of information related to itch sensation at the level of cerebral cortex is not well understood. In this first single-unit electrophysiological study of pruriceptive cortical neurons, we show that neurons responsive to noxious and pruritic stimulation of the cheek of the face are concentrated in a small area of the dysgranular cortex, indicating that these neurons encode information related to itch and pain.

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.

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.

Membrane Properties and Monosynaptic Retinal Excitation of Neurons in the Turtle Accessory Optic System

1997 ◽  
Vol 78 (2) ◽  
pp. 614-627 ◽  
Author(s):  
Naoki Kogo ◽  
Michael Ariel
Keyword(s):  
Receptive Field ◽  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Membrane Properties ◽  
Retinal Ganglion ◽  
Optic System ◽  
Accessory Optic System ◽  
Postsynaptic Potentials ◽  
Synaptic Inputs ◽  
Bon Cells

Kogo, Naoki and Michael Ariel. Membrane properties and monosynaptic retinal excitation of neurons in the turtle accessory optic system. J. Neurophysiol. 78: 614–627, 1997. Using an eye-attached isolated brain stem preparation of a turtle, Pseudemys scripta elegans, in conjunction with whole cell patch techniques, we recorded intracellular activity of accessory optic system neurons in the basal optic nucleus (BON). This technique offered long-lasting stable recordings of individual synaptic events. In the reduced preparation (most of the dorsal structures were removed), large spontaneous excitatory synaptic inputs [excitatory postsynaptic potentials (EPSPs)] were frequently recorded. Spontaneous inhibitory postsynaptic potentials were rarely observed except in few cases. Most EPSPs disappeared after injection of lidocaine into the retina. A few EPSPs of small size remained, suggesting that these EPSPs either were from intracranial sources or may have been miniature spontaneous synaptic potentials from retinal ganglion cell axon terminals. Population EPSPs were synchronously evoked by electrical stimulation of the contralateral optic nerve. Their constant onset latency and their ability to follow short-interval paired stimulation indicated that much of the population EPSP's response was monosynaptic. Visually evoked BON spikes and EPSP inputs to BON showed direction sensitivity when a moving pattern was projected onto the entire contralateral retina. With the use of smaller moving patterns, the receptive field of an individual BON cell was identified. A small spot of light, projected within the receptive field, guided the placement of a bipolar stimulation electrode to activate retinal ganglion cells that provided input to that BON cell. EPSPs evoked by this retinal microstimulation showed features of unitary EPSPs. Those EPSPs had distinct low current thresholds. Recruitment of other inputs was only evident when the stimulation level was increased substantially above threshold. The average size of evoked unitary EPSPs was 7.8 mV, confirming the large size of synaptic inputs of this system relative to nonsynaptic noise. EPSP shape was plotted (rise time vs. amplitude), with the use of either evoked unitary EPSPs or spontaneous EPSPs. Unlike samples of spontaneous EPSPs, data from many unitary EPSPs formed distinct clusters in these scatterplots, indicating that these EPSPs had a unique shape among the whole population of EPSPs. In most BON cells studied, hyperpolarization-activated channels caused a slow depolarization sag that reached a plateau within 0.5–1 s. This property suggests that BON cells may be more complicated than a simple site for convergence of direction-sensitive retinal ganglion cells to form a central retinal slip signal for control of oculomotor reflexes.

scholarly journals Cutaneous stimulation of the digits and lips evokes responses with different adaptation patterns in primary somatosensory cortex

NeuroImage ◽  
2010 ◽  
Vol 52 (4) ◽  
pp. 1477-1486 ◽  
Author(s):  
Mihai Popescu ◽  
Steven Barlow ◽  
Elena-Anda Popescu ◽  
Meredith E. Estep ◽  
Lalit Venkatesan ◽  
...  
Keyword(s):  
Somatosensory Cortex ◽  
Primary Somatosensory Cortex ◽  
Cutaneous Stimulation ◽  
Stimulation Of

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.

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