Astrocytes and oligodendrocytes in the thalamus jointly maintain synaptic activity by supplying metabolites

Thalamic astrocytes and oligodendrocytes are coupled via gap junctions and form panglial networks. Here, we show that these networks have a key role in energy supply of neurons. Filling an astrocyte or an oligodendrocyte in acute slices with glucose or lactate is sufficient to rescue the decline of stimulation-induced field post-synaptic potential (fPSP) amplitudes during extracellular glucose deprivation (EGD). In mice lacking oligodendroglial coupling, loading an astrocyte with glucose does not rescue the EGD-mediated loss of fPSPs. Monocarboxylate and glucose transporters are required for rescuing synaptic activity during EGD. In mice deficient in astrocyte coupling, filling of an oligodendrocyte with glucose does not rescue fPSPs during EGD. Our results demonstrate that, in the thalamus, astrocytes and oligodendrocytes are jointly engaged in delivering energy substrates for sustaining neuronal activity and suggest that oligodendrocytes exert their effect mainly by assisting astrocytes in metabolite transfer to the postsynapse.

Automated summary

Thalamic astrocytes and oligodendrocytes form panglial networks via gap junctions, playing key roles in providing energy substrates for sustaining neuronal activity. Loading astrocytes or oligodendrocytes with glucose or lactate can rescue the decline of stimulation-induced field post-synaptic potential amplitudes during extracellular glucose deprivation, with monocarboxylate and glucose transporters being required for this activity. Oligodendrocytes mainly assist astrocytes in metabolite transfer to the postsynapse, as demonstrated in mice deficient in astrocyte or oligodendroglial coupling.