Adaptation in Thalamic Barreloid and Cortical Barrel Neurons to Periodic Whisker Deflections Varying in Frequency and Velocity

Abstract

. Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. J Neurophysiol 92: 3244 -3254, 2004. First published August 11, 2004 doi:10.1152/jn.00257.2004. Layer IV circuitry in the rodent whisker-to-barrel pathway transforms the thalamic input signal spatially and temporally. Excitatory and inhibitory barrel neurons display response properties that differ from each other and from their common thalamic inputs. Here we further examine thalamocortical response transformations by characterizing the responses of individual thalamic barreloid neurons and presumed excitatory and inhibitory cortical barrel neurons to periodic whisker deflections varying in frequency from 1 to 40 Hz. Both pulsatile and sinusoidal periodic stimulation of fixed deflection amplitude were used to assess stimulus-evoked adaptation of thalamocortical units (TCUs), fast-spike barrel units (FSUs: presumed inhibitory neurons), and regular-spike barrel units (RSUs: presumed excitatory neurons). Monotonic, frequency-dependent reductions in firing were observed in thalamic and cortical neurons to the second and subsequent stimuli in trains of high (pulsatile)-and low (sinusoidal)-velocity deflections. RSUs and FSUs adapted substantially more than their thalamic input neurons, and at all frequencies, FSUs fired at higher rates than the other two cell types. For example at 40 Hz, response magnitudes of TCUs decreased by 34%, FSUs by 72%, and RSUs by 78%. Across frequencies, RSUs and FSUs displayed more cycle-by-cycle entrainment and phase-locked responses for (high velocity) pulsatile than (lower velocity) sinusoidal deflections; for TCUs, phase-locking was equivalent for both stimuli, but entrainment was higher for sinusoidal deflections. Strong feed-forward inhibition, in conjunction with synaptic depression, renders the firing of barrel neurons sparse but temporally faithful to the occurrence of repetitive whisker deflections, especially when they are of high velocity.

Integration of Vibrotactile Signals for Whisker-Related Perception in Rats Is Governed by Short Time Constants: Comparison of Neurometric and Psychometric Detection Performance

“…Both maximum spike probabilities and spike counts progressively adapted, with the major amount of attenuation being achieved with the second pulse already. These results are in both qualitative and quantitative agreement with a previous report using suprathreshold stimuli in anesthetized rats (Khatri et al, 2004).…”

“…The plots reveal that, for both 10 and 20 Hz, responses to subsequent pulses were reduced. We quantified the amount of reduction using the adaptation index (AI) used in the study by Khatri et al (2004). AI was computed in two ways: first, as the maximum spike probability within each 25 ms interval following pulse onset normalized to the maximum spike probability for the first pulse; second, as the integral of the spike probability (i.e., total spike count) in the same period, normalized in an analogous way.…”

“…In contrast to this expectation, neurons along the whisker-related tactile pathway show strong firing rate adaptation with repetitive deflections at frequencies higher than 10 Hz, indicating highly sublinear temporal integration (Fanselow and Nicolelis, 1999;Chung et al, 2002;Arabzadeh et al, 2003;Garabedian et al, 2003;Khatri and Simons, 2004;SanchezJimenez et al, 2009). Adaptation is strongest in primary somatosensory cortex and seems to be at least partly based on the action of intracortical inhibitory networks Schwarz, 2003, 2006;Webber and Stanley, 2004).…”

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

“…In a previous study using different frequencies of whisker stimulation for 1 minute, local field potentials and astrocyte somata calcium responses peaked at 5 Hz and decreased at 10 Hz, which they attributed to neuronal adaptation (Wang et al 2006). While we chose to use higher frequencies of stimulation that mimic "stick-slip" events from whisking on textured surfaces, we also limited stimulation to much shorter epochs (1 or 8 s) that reliably produce field potential spikes and calcium transients within neurons (Khatri et al 2004;Musall et al 2014;Mayrhofer et al 2015). During this type of pulsatile whisker stimulation neuronal adaptation occurs within the first few pulses and the number of spikes per pulse decreases, particularly at higher frequencies (Khatri et al 2004;Fraser et al 2006;Musall et al 2014).…”

“…While we chose to use higher frequencies of stimulation that mimic "stick-slip" events from whisking on textured surfaces, we also limited stimulation to much shorter epochs (1 or 8 s) that reliably produce field potential spikes and calcium transients within neurons (Khatri et al 2004;Musall et al 2014;Mayrhofer et al 2015). During this type of pulsatile whisker stimulation neuronal adaptation occurs within the first few pulses and the number of spikes per pulse decreases, particularly at higher frequencies (Khatri et al 2004;Fraser et al 2006;Musall et al 2014). However, neuronal responses remain locked to the pulsatile stimulus (Ewert et al 2008) and are reproducible across many trials (Mayrhofer et al 2015).…”