Abstract

Stimulus specific adaptation has been studied extensively in different modalities. High specificity implies that deviant stimulus induces a stronger response compared to a common stimulus. The thalamus gates sensory information to the cortex, therefore, the specificity of adaptation in the thalamus must have a great impact on cortical processing of sensory inputs. We studied the specificity of adaptation to whisker identity in the ventral posteromedial nucleus of the thalamus (VPM) in rats using extracellular and intracellular recordings. We found that subsequent to repetitive stimulation that induced strong adaptation, the response to stimulation of the same, or any other responsive whisker was equally adapted, indicating that thalamic adaptation is non-specific. In contrast, adaptation of single units in the upstream brainstem principal trigeminal nucleus (PrV) was significantly more specific. Depolarization of intracellularly recorded VPM cells demonstrated that adaptation is not due to buildup of inhibition. In addition, adaptation increased the probability of observing complete synaptic failures to tactile stimulation. In accordance with short-term synaptic depression models, the evoked synaptic potentials in response to whisker stimulation, subsequent to a response failure, were facilitated. In summary, we show that local short-term synaptic plasticity is involved in the transformation of adaptation in the trigemino-thalamic synapse and that the low specificity of adaptation in the VPM emerges locally rather than cascades from earlier stages. Taken together we suggest that during sustained stimulation, local thalamic mechanisms equally suppress inputs arriving from different whiskers before being gated to the cortex.

Highlights

  • Adaptation in primary sensory cortical areas is usually stimulus specific (Marlin et al, 1991; Ulanovsky et al, 2003; Katz et al, 2006), i.e., rare or deviant stimuli induce stronger responses compared to common stimuli

  • Our results argue that the specificity of adaptation to whisker identity in the thalamus is not inherited from earlier stages and that synaptic depression contributes to thalamic adaptation

  • We analyzed the effect of whisker identity; an equal reduction in CW response compared to the test response of the same whisker would indicate that adaptation is not specific

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Summary

Introduction

Adaptation in primary sensory cortical areas is usually stimulus specific (Marlin et al, 1991; Ulanovsky et al, 2003; Katz et al, 2006), i.e., rare or deviant stimuli induce stronger responses compared to common stimuli. It was proposed that the main role of the thalamus is to gate or modulate ascending information to the cortex VPM neurons are mainly driven by direct glutamatergic monosynaptic inputs from homologous ‘‘barrelette’’ cells located in the PrV (Magnusson et al, 1987; Castro-Alamancos, 2002a). Thalamic multi-whisker RFs could be directly inherited from PrV multiwhisker cells via trigemino-thalamic fibers. They could result from the convergence of single-whisker PrV axons on VPM cells. The innervation pattern of VPM cells by PrV inputs could play an important role in determining the specificity of adaptation in the VPM to whisker identity

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