Glutamatergic input–output properties of thalamic astrocytes

Astrocytes in the somatosensory ventrobasal (VB) thalamus of rats respond to glutamatergic synaptic input with metabotropic glutamate receptor (mGluR) mediated intracellular calcium ([Ca2+]i) elevations. Astrocytes in the VB thalamus also release the gliotransmitter (GT) glutamate in a Ca2+-dependent manner. The tripartite synapse hypothesis posits that astrocytic [Ca2+]i elevations resulting from synaptic input releases gliotransmitters that then feedback to modify the synapse. Understanding the dynamics of this process and the conditions under which it occurs are therefore important steps in elucidating the potential roles and impact of GT release in particular brain activities. In this study, we investigated the relationship between VB thalamus afferent synaptic input and astrocytic glutamate release by recording N-methyl-d-aspartate (NMDA) receptor-mediated slow inward currents (SICs) elicited in neighboring neurons. We found that Lemniscal or cortical afferent stimulation, which can elicit astrocytic [Ca2+]i elevations, do not typically result in the generation of SICs in thalamocortical (TC) neurons. Rather, we find that the spontaneous emergence of SICs is largely resistant to acute afferent input. The frequency of SICs, however, is correlated to long-lasting afferent activity. In contrast to short-term stimulus-evoked GT release effects reported in other brain areas, astrocytes in the VB thalamus do not express a straightforward input–output relationship for SIC generation but exhibit integrative characteristics.
Highlights ▶VB thalamus afferents were stimulated at a range of frequencies and durations to investigate the interaction of afferent input and astrocytic glutamate output. ▶Acute afferent activity does not result in the evoking of astrocyte glutamate-mediated slow inward currents. ▶Prolonged afferent activity, however, increases SIC frequency in a time-dependent manner. ▶VB thalamus astrocytes therefore exhibit integrative properties that modulate the rate of spontaneous glutamate release.