Transient expression of the neuropeptide galanin modulates peripheral‑to‑central connectivity in the somatosensory thalamus during whisker development in mice

Zsofia Hevesi, Joanne Bakker, Evgenii O. Tretiakov, Csaba Adori, Anika Raabgrund, Swapnali S. Barde, Martino Caramia, Thomas Krausgruber, Sabrina Ladstätter, Christoph Bock, Tomas Hökfelt () and Tibor Harkany ()
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Zsofia Hevesi: Medical University of Vienna
Joanne Bakker: Karolinska Institutet
Evgenii O. Tretiakov: Medical University of Vienna
Csaba Adori: Karolinska Institutet
Anika Raabgrund: Medical University of Vienna
Swapnali S. Barde: Karolinska Institutet
Martino Caramia: Karolinska Institutet
Thomas Krausgruber: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Sabrina Ladstätter: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Christoph Bock: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Tomas Hökfelt: Karolinska Institutet
Tibor Harkany: Medical University of Vienna

Nature Communications, 2024, vol. 15, issue 1, 1-11

Abstract: Abstract The significance of transient neuropeptide expression during postnatal brain development is unknown. Here, we show that galanin expression in the ventrobasal thalamus of infant mice coincides with whisker map development and modulates subcortical circuit wiring. Time-resolved neuroanatomy and single-nucleus RNA-seq identified complementary galanin (Gal) and galanin receptor 1 (Galr1) expression in the ventrobasal thalamus and the principal sensory nucleus of the trigeminal nerve (Pr5), respectively. Somatodendritic galanin release from the ventrobasal thalamus was time-locked to the first postnatal week, when Gal1R+ Pr5 afferents form glutamatergic (Slc17a6+) synapses for the topographical whisker map to emerge. RNAi-mediated silencing of galanin expression disrupted glutamatergic synaptogenesis, which manifested as impaired whisker-dependent exploratory behaviors in infant mice, with behavioral abnormalities enduring into adulthood. Pharmacological probing of receptor selectivity in vivo corroborated that target recognition and synaptogenesis in the thalamus, at least in part, are reliant on agonist-induced Gal1R activation in inbound excitatory axons. Overall, we suggest a neuropeptide-dependent developmental mechanism to contribute to the topographical specification of a fundamental sensory neurocircuit in mice.

Date: 2024
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DOI: 10.1038/s41467-024-47054-5

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