Abstract

The rodent ventrobasal (VB) thalamus receives sensory inputs from the whiskers and projects to the cortex, from which it receives reciprocal excitatory afferents. Much is known about the properties and functional roles of these glutamatergic inputs to thalamocortical neurons in the VB, but no data are available on how these afferents can affect thalamic glial cells. In this study, we used combined electrophysiological recordings and intracellular calcium ([Ca2+]i) imaging to investigate glial cell responses to synaptic afferent stimulation. VB thalamus glial cells can be divided into two groups based on their [Ca2+]i and electrophysiological responses to sensory and corticothalamic stimulation. One group consists of astrocytes, which stain positively for S100B and preferentially load with SR101, have linear current–voltage relations and low input resistance, show no voltage-dependent [Ca2+]i responses, but express mGluR5-dependent [Ca2+]i transients following stimulation of the sensory and/or corticothalamic excitatory afferent pathways. Cells of the other glial group, by contrast, stain positively for NG2, and are characterized by high input resistance, the presence of voltage-dependent [Ca2+]i elevations and voltage-gated inward currents. There were no synaptically induced [Ca2+]i elevations in these cells under control conditions. These results show that thalamic glial cell responses to synaptic input exhibit different properties to those of thalamocortical neurons. As VB astrocytes can respond to synaptic stimulation and signal to neighbouring neurons, this glial cell organization may have functional implications for the processing of somatosensory information and modulation of behavioural state-dependent thalamocortical network activities.

Highlights

  • Thalamocortical (TC) neurons of the ventrobasal (VB) thalamus receive excitatory somatosensory inputs, notably in the rat from the vibrissae, and project to layer IV of the somatosensory cortex

  • Our findings show that both astrocytes and NG2+ glial cells respond to stimulation of the sensory and CT afferents with different receptors and output characteristics

  • In slices loaded with Fluo-4AM, synaptic stimulation of either the sensory or the CT afferents elicited relatively fast and brief [intracellular calcium (Ca2+]i) transients that are characteristic of neuronal synaptic responses, as well as slower, longer-lasting [Ca2+]i elevations that are characteristically observed in the smaller-diameter astroglia cells (Fig. 1A), as previously reported (Parri et al, 2001)

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Summary

Introduction

Thalamocortical (TC) neurons of the ventrobasal (VB) thalamus receive excitatory somatosensory inputs, notably in the rat from the vibrissae, and project to layer IV of the somatosensory cortex. Layer VI pyramidal neurons in the somatosensory cortex project back to the VB TC neurons, so completing the thalamocortical loop. Both the sensory and corticothalamic (CT) inputs to the VB are glutamatergic, the synaptic structures, postsynaptic receptor complement and functional properties of the two afferents differ. In common with other thalamic nuclei (Turner & Salt, 1998), increasing CT stimulus intensity results in graded postsynaptic responses in TC neurons, consistent with multiple afferent recruitment, whereas an allor-none response is recorded following stimulation of the lemniscal sensory input (Miyata & Imoto, 2006), which is taken as evidence of innervation by a single sensory afferent.

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