Transformation of Adaptation and Gain Rescaling along the Whisker Sensory Pathway

Miguel Maravall,Rasmus S Petersen,Andrea Alenda,Michael R Bale,Samuel G Solomon

doi:10.1371/journal.pone.0082418

Miguel Maravall, Rasmus S Petersen + Show 3 more

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https://doi.org/10.1371/journal.pone.0082418

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Abstract

Neurons in all sensory systems have a remarkable ability to adapt their sensitivity to the statistical structure of the sensory signals to which they are tuned. In the barrel cortex, firing rate adapts to the variance of a whisker stimulus and neuronal sensitivity (gain) adjusts in inverse proportion to the stimulus standard deviation. To determine how adaptation might be transformed across the ascending lemniscal pathway, we measured the responses of single units in the first and last subcortical stages, the trigeminal ganglion (TRG) and ventral posterior medial thalamic nucleus (VPM), to controlled whisker stimulation in urethane-anesthetized rats. We probed adaptation using a filtered white noise stimulus that switched between low- and high-variance epochs. We found that the firing rate of both TRG and VPM neurons adapted to stimulus variance. By fitting the responses of each unit to a Linear-Nonlinear-Poisson model, we tested whether adaptation changed feature selectivity and/or sensitivity. We found that, whereas feature selectivity was unaffected by stimulus variance, units often exhibited a marked change in sensitivity. The extent of these sensitivity changes increased systematically along the pathway from TRG to barrel cortex. However, there was marked variability across units, especially in VPM. In sum, in the whisker system, the adaptation properties of subcortical neurons are surprisingly diverse. The significance of this diversity may be that it contributes to a rich population representation of whisker dynamics.

Highlights

Adaptation, the accommodation of neuronal responses to ongoing stimulation, occurs across species and sensory modalities [1]
The aim of the present study is to address this issue by analyzing how adaptation to stimulus statistics progresses along the whisker pathway, from the first stage of processing in the trigeminal ganglion (TRG) to the final subcortical relay stage, the ventral posterior medial nucleus of the thalamus (VPM)
To determine how adaptation modifies the encoding of whisker motion at different subcortical processing stages in the whisker sensory pathway, we recorded the responses of well-isolated single units from the TRG (n = 11) and ventral posterior medial thalamic nucleus (VPM) (n = 18) of urethaneanesthetized rats (n = 15) to simultaneous deflection of the whiskers with a noise stimulus

Summary

Introduction

Adaptation, the accommodation of neuronal responses to ongoing stimulation, occurs across species and sensory modalities [1]. In the primary somatosensory ‘‘barrel’’ cortex, neurons are tuned to fast temporal features of vibrissa (‘‘whisker’’) motion, such as instantaneous velocity [12,13,14,15,16,17,18,19] The gain of this stimulus-response relationship depends on the stimulus statistics of the current sensory environment, such that an increase in the variance of whisker motion causes a compensatory decrease in gain and vice versa [20,21]. It is not yet known whether these adaptive changes originate in the barrel cortex itself or in the ascending somatosensory pathway.

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