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Morphology, physiology and synaptic connectivity of local interneurons in the mouse somatosensory thalamus.

ABSTRACT: The thalamic reticular nucleus (TRN) neurons, projecting across the external medullary lamina, have long been considered to be the only significant source of inhibition of the somatosensory ventral posterior (VP) nuclei of the thalamus. Here we report for the first time effective local inhibition and disinhibition in the VP. Inhibitory interneurons were found in GAD67-GFP-expressing mice and studied using in vitro multiple patch clamp. Inhibitory interneurons have expansive bipolar or tripolar morphologies, reach across most of the VP nucleus and display low threshold bursting behaviour. They form triadic and non-triadic synaptic connections onto thalamocortical relay neurons and other interneurons, mediating feedforward inhibition and disinhibition. Synaptic inputs arrive before those expected from the TRN neurons, suggesting that local inhibition plays an early and significant role in the functioning of the somatosensory thalamus. KEY POINTS: The physiology and structure of local interneurons in the mouse somatosensory thalamus is described for the first time. Inhibitory interneurons have extensive dendritic arborization providing significant local dendro-dendritic inhibition in the somatosensory thalamus. Triadic and non-triadic synaptic connectivity onto thalamic relay neurons and other interneurons provides both local feedforward inhibition and disinhibition. Interneurons of the somatosensory thalamus provide inhibition before the thalamic reticular nucleus, suggesting they play an important role in sensory perception.

SUBMITTER: Simko J

PROVIDER: S-EPMC9298088 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Purpose: We aimed to resolve if there is a matched expression of neuropeptide receptor(s) and their ligand(s) between the sensory trunk of the trigeminal nerve (Pr5) and the ventrobasal hypothalamus on postnatal day 7 (P7) in mice. We hypothesized that a coincidence of neuropeptide expression and release from the ventrobasal thalamus and the cognate receptor(s) for the specific neuropeptide(s) in trigeminal neurons could allow for novel hypotheses be built on intercellular communication between peripheral axons and their postsynaptic targets in the thalamus. Thereby, this work can be informative of the developmental integration of the whisker pathway, one of the major sensory modalities in laboratory rodents. To this end, we used single-cell RNA-seq on cells dissociated from the ventrobasal thalamus and Pr5 on P7. Results: We tested this hypothesis by single-nucleus RNA-seq performed in parallel on the ventrobasal thalamus and Pr5 at P7. At this developmental stage, the ventrobasal thalamus contained two subtypes of Slc17a6+(glutamatergic) neurons, one subtype of Gad1/Gad2+ (GABA) neurons, astroglia, oligodendrocytes, and vascular components (n = 923 nuclei isolated from n = 3 pups of mixed sex). Slc17a6+ neurons, which we recognize as cortically projecting glutamate neurons, co-expressed molecular components underpinning barrel map formation (e.g., Grin1, Adcy1, Prkaca,99 Ache, Slc6a4) and a significant amount of the thalamocortical neuronal marker Cck, while other neuropeptides/hormones were absent or barely present (e.g., Npy, Sst). At the same time, we harvested n = 731 nuclei from the Pr5 by micro-excision at P7, of which ∼98% expressed Slc17a6, thus qualifying, in total or in part, as centrally-projecting sensory neurons. This neuronal cohort harbored axon guidance molecules, and neuropeptide receptors. Conclusions: We suggest that neuropeptides, particularly galanin, could participate in guidance decisions of Pr5 axons given the complementarity of ligand-receptor expression patterns, and that Galr1 expression could be a time locked feature for those neurons that actively undergo neuritogenesis at a given time.

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Morphology, physiology and synaptic connectivity of local interneurons in the mouse somatosensory thalamus.

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