The Relay of High-Frequency Sensory Signals in the Whisker-to-Barreloid Pathway

Abstract

The present study investigated the operational features of whisker-evoked EPSPs in barreloid cells and the ability of the whisker-to-barreloid pathway to relay high rates of whisker deflection in lightly anesthetized rats. Results show that lemniscal EPSPs are single-fiber events with fast rise times (<500 microsec) that strongly depress at short inter-EPSP intervals. They occur at short latencies (3.84 +/- 0.96 msec) with little jitters (<300 microsec) after electrical stimulation of the whisker follicle. Waveform analysis indicates that one to three lemniscal axons converge on individual barreloid cells to produce EPSPs of similar rise times but different amplitudes. When challenged by high rates of whisker deflection, cells in the whisker-to-barreloid pathway demonstrate a remarkable frequency-following ability. Primary vibrissa afferents could follow in a phase-locked manner trains of sinusoidal deflections at up to 1 kHz. Although trigeminothalamic cells could still faithfully follow deflection rates of 200-300 Hz, the actual frequency-following ability of individual cells depends on the amplitude, velocity, and direction of displacements. The discharges of trigeminothalamic cells induce corresponding phase-locked EPSPs in barreloid cells, which trigger burst discharges at stimulus onset. During the following cycles of the stimulus train, few action potentials ensue because of the strong synaptic depression at lemniscal synapses. It is concluded that the whisker-to-barreloid pathway can relay vibratory inputs with a high degree of temporal precision, but that the relay of this information to the cerebral cortex requires the action of modulators, and possibly phase-locked discharges among an ensemble of relay cells.

Cortical control of adaptation and sensory relay mode in the thalamus

“…Behaviorally relevant inputs for mice and rats are sequences of whisker stimuli that occur when a mouse rhythmically moves its whiskers during exploration and when the whiskers are swept along objects with uneven surfaces (32). As in other sensory thalamo-cortical systems, VPM neurons exhibit characteristic rapid adaptation to sensory inputs (6,33,34). One cause of this adaptation is the strong depression of synapses between the brainstem and VPM, which results in a successive decrease in EPSP magnitude (6).…”

“…Response adaptation is a key feature of sensory systems (1, 2) including VPM (6,33,34) where adaptation prevents the relay of high-frequency tactile information. VPM inputs to the cortex (42) activate L6 during whisker stimulation (25,43), suggesting that tactile activity itself is important for L6-mediated gating of frequency cues.…”

A New Thalamic Pathway of Vibrissal Information Modulated by the Motor Cortex

“…They most likely convey information related to whisker motion (proprioception), texture and shape discrimination, and object location in the whisking space, or again different pathways may be operative in different behavioral contexts [e.g., the exploratory and object recognition modes discussed by Curtis and Kleinfeld (2006)]. Approximately 75% of the PrV cells have a receptive field dominated by a single vibrissa (Minnery and Simons, 2003), and their projections in the VPM show little convergence [on average, a VPM relay cell receives input from one to two PrV neurons (Castro-Alamancos, 2002;Deschênes et al, 2003)]. The prevailing view is that this fine-grained system serves texture and shape discrimination.…”

Synaptic Responses to Whisker Deflections in Rat Barrel Cortex as a Function of Cortical Layer and Stimulus Intensity

“…In the rodent barrel system, neurons are exquisitely sensitive to velocity (Gibson and Welker, 1983;Ito, 1985;Shoykhet et al, 2000;Deschenes et al, 2003;Temereanca and Simons, 2003;Lee and Simons, 2004) and acceleration (Temereanca and Simons, 2003) at which the corresponding principal whisker in the mystacial pad is deflected. As rodents explore, their whiskers repetitively move back and forth at 5-15 Hz (Welker et al, 1964;Carvell and Simons, 1995;Berg and Kleinfeld, 2003) contacting surfaces and objects, causing small angular deflections at the base of the whiskers.…”