Abstract
The striatum participates in numerous important behaviors. Its principal projection neurons use GABA and peptides as neurotransmitters and interact extensively with interneurons, including cholinergic interneurons (ChIs) that are tonically active. Dissecting the interactions between projection neurons and ChIs is important for uncovering the role and mechanisms of the striatal microcircuits. Here, by combining several optogenetic tools with cell type-specific electrophysiological recordings, we uncovered direct electrical coupling between D1-type projection neurons and ChIs, in addition to the chemical transmission between these two major cell types. Optogenetic stimulation or inhibition led to bilateral current exchanges between D1 neurons and ChIs, which can be abolished by gap junction blockers. We further confirmed the presence of gap junctions through paired electrophysiological recordings and dye microinjections. Finally, we found that activating D1 neurons promotes basal activity of ChIs via gap junctions. Collectively, these results reveal the coexistence of the chemical synapse and gap junctions between D1 neurons and ChIs, which contributes to maintaining the tonically active firing patterns of ChIs.
Highlights
As the main input nucleus of the basal ganglia, the striatum participates in motor control and goal-directed behavior (Abudukeyoumu et al, 2019)
We injected retrograde transport-orientated adeno-associated virus (AAV) carrying recombinase flippase vector into the SNR and injected AAV virus carrying flippase-dependent vector fDIO-ChR2EYFP into the striatum to express ChR2 in D1 neurons projecting to the SNR (Figures 1A,B)
We examined the synaptic responses of cholinergic interneurons (ChIs) to the photostimulation of ChR2-expressing D1 neurons
Summary
As the main input nucleus of the basal ganglia, the striatum participates in motor control and goal-directed behavior (Abudukeyoumu et al, 2019). MSNs are typically classified into two subpopulations containing neurons expressing dopamine D1 receptor subtypes or dopamine D2 receptor subtypes, which project to the globus pallidus interna (GPi) and the substantia nigra pars reticularta (SNR) or the globus pallidus externa (GPe) (Gerfen, 1992; Lobo, 2009), respectively. Both types of projection neurons are GABAergic and inhibitory (Kreitzer, 2009). The remaining neurons consist of cholinergic interneurons (ChIs), and several different subtypes of GABAergic interneurons, such as NPY/SST/NOS interneurons, NPY-NGF (neurogliaform) interneurons, PV fast-spiking interneurons, TH interneurons, and CCK interneurons
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