Wideband phase locking to modulated whisker vibration point to a temporal code for texture in the rat's barrel cortex.

Rats probe objects with their whiskers and make decisions about sizes, shapes, textures and distances within a few tens of milliseconds. This perceptual analysis requires the processing of tactile high-frequency object components reflecting surface roughness. We have shown that neurons in the barrel cortex of rats encode high-frequency sinusoidal vibrations of whiskers for sustained periods when presented with constant amplitudes and frequencies. In a natural situation, however, stimulus parameters change rapidly when whiskers are brushing across objects. In this study, we therefore analysed cortical responses to vibratory movements of single whiskers with rapidly changing amplitudes and frequencies. The results show that different neural codes are employed for a processing of stimulus parameters. The frequency of whisker vibration is encoded by the temporal pattern of spike discharges, i.e., the phase-locked responses of barrel cortex neurons. In addition, oscillatory gamma band activity was induced during high-frequency stimulation. The pivotal descriptor of the amplitude of whisker displacement, the velocity, is reflected in the rate of spike discharges. While phase-locked discharges occurred over the entire range of frequencies tested (10-600 Hz), the discharge rate increased with stimulus velocity only up to about 60 µm/ms, saturating at a mean rate of ~117 spikes/s. In addition, the results show that whisker movements of more than 500 Hz bandwidth may be encoded by phase-locked responses of small groups of cortical neurons. Thus, even single whiskers may transmit information about wide ranges of textural components owing to their set of different types of hair follicle mechanoreceptors.

High-frequency whisker vibration is encoded by phase-locked responses of neurons in the rat's barrel cortex.

Rats perform texture discrimination during tactile exploration with their whiskers with high spatial and temporal precision. Although the peripheral mechanoreceptors provide tactile information with exquisite temporal resolution, physiological studies have suggested that this information might be lost at the cortical level. To address this discrepancy, multiunit and single-unit recordings were performed in the barrel cortex of isoflurane-anesthetized rats using continuous sinusoidal vibration of single whiskers at 15-700 Hz. In multiunit recordings, sustained phase-locked responses occurred up to vibration frequencies of 700 Hz, and 1:1 stimulus locking was observed up to 320 Hz. Wide-band responses of multiunits showed frequency encoding between 20 and 320 Hz. The discharge rates were not different for stimuli in the low- and high-frequency ranges, but they were significantly lower for non-phase-locked responses to high-frequency vibration. Response adaptation was present in only 25% of the cases, whereas in the majority of cases, entrainment to the vibratory frequency remained constant or even increased with stimulus duration. Increased entrainment to high-frequency stimulation was accompanied by the emergence of induced activity in the gamma-band range. Analysis of single-unit activity revealed that phase locking to vibratory stimuli was more precise than that observed for the multiunit responses. The results show that whisker vibrations at frequencies above 100 Hz are faithfully encoded by sustained phase-locked responses of cortical neurons under isoflurane anesthesia. It is conceivable that the awake animal makes use of the tactile signals at even much higher frequencies, which can be provided by the peripheral mechanoreceptors during texture discrimination.

Contributions of GABAergic and glutamatergic mechanisms to isoflurane-induced suppression of thalamic somatosensory information transfer.

Indications for a pivotal role of the thalamocortical network in producing the state of anesthesia have come from in vivo animal studies as well as imaging studies in humans. We studied possible synaptic mechanisms of anesthesia-induced suppression of touch perception in the rat's thalamus. Thalamocortical relay neurons (TCNs) receive ascending and descending glutamatergic excitatory inputs via NMDA and non-NMDA receptors (AMPAR) and are subjected to GABA(A)ergic inhibitory input which shapes the sensory information conveyed to the cortex. The involvement of these synaptic receptors in the suppressive effects of the prototypic volatile anesthetic isoflurane was assessed by local iontophoretic administration of receptor agonists/antagonists during extracellular recordings of TCNs of the ventral posteromedial nucleus responding to whisker vibration in rats anesthetized with isoflurane concentrations of approximately 0.9 vol.% (baseline) and approximately 1.9 vol.% (ISO high). ISO high induced a profound suppression of response activity reflected by a conversion of the sustained vibratory responses to ON responses. Administration of NMDA, AMPA, or GABA(A)R antagonists caused a reversal to sustained responses in 88, 94 and 88% of the neurons, respectively, with a recovery to baseline levels of response activity. The data show that the block of thalamocortical transfer of tactile information under ISO high may result from an enhancement of GABA(A)ergic inhibition and/or a reduction of glutamatergic excitation. Furthermore, they show that the ascending vibratory signals still reach the thalamic neurons under the high isoflurane concentration, indicating that this input is resistant to isoflurane while the attenuation of excitation may be brought about at the corticothalamic glutamatergic facilitatory input.

Temporal shaping of phasic neuronal responses by GABA- and non-GABA-mediated mechanisms in the somatosensory thalamus of the rat.

Trapezoidal mechanical movement of whiskers was used to study the responses of 44 single thalamic ventral posteromedial (VPM) neurons to dynamic and static stimulus components in urethane-anesthetized rats. The effects of local administration of the GABAA receptor antagonist, bicuculline, and the GABAB receptor antagonist, 2-hydroxysaclofen, were tested to determine whether and to what extent the responses altered when GABA-mediated inhibitory synaptic transmission was blocked. Two classes of phasically responding neurons were identified, ON/OFF and movement-sensitive types. Bicuculline enhanced the magnitudes of the responses from both types by 2.5-fold and ON/OFF responses were converted to movement-sensitive ones in 17 (43%) of the 40 ON/OFF neurons. 2-hydroxysaclofen either had no effect or appeared to act like a GABA agonist. In 21 (48%) neurons, a significantly reduced responsiveness was observed during a 100-ms period following the ON and OFF responses. This discharge suppression was especially prominent during the plateau phase of the stimulus, and in some cases extended for several 100 ms following its onset. This suppression was overcome neither by the GABA receptor antagonists, nor by ejection of AMPA or glutamate at currents that otherwise produced vigorous excitation. These results suggest that one functional role for GABAA-receptor-mediated synaptic inhibition in the somatosensory thalamus is the intramodal regulation of the form of expression of phasically responding neurons. Other thalamic inhibitory processes not mediated by GABAA or GABAB receptors that help to shape the expression of the responses of certain phasic neurons to maintained stimulation may exist. Overall, these mechanisms appear to mediate the precision of timing of thalamic neuronal firing in response to the rat's tactile environment.

Increased responsiveness of cortical neurons in contrast to thalamic neurons during isoflurane-induced EEG bursts in rats.

The neuronal mechanisms underlying the electroencephalographic (EEG) burst-suppression pattern are not yet understood, however, they are generally attributed to interactions within thalamocortical networks. In contrast, we report that the sensory cortex and the thalamus are disconnected, with thalamic sensory processing being unaffected by cortical EEG bursts. We studied the activity of single neurons of the somatosensory thalamocortical system in rats during burst-suppression EEG induced by the volatile anesthetic, isoflurane. In neurons of the thalamic ventrobasal complex, the discharge rate in response to tactile stimulation of their receptive fields did not differ significantly during EEG bursts and isoelectric periods. In contrast, in neurons of the primary somatosensory cortex, the response magnitude was significantly greater during EEG bursts as compared with isoelectric periods (mean increase to 293%). The results suggest that the profound suppression of cortical sensory information processing by isoflurane is suspended during EEG burst-induced elevated cortical excitation.