Asymmetric vasopressin signaling spatially organizes the master circadian clock

Jun 23, 2018The Journal of comparative neurology

Uneven vasopressin signals help organize the brain’s main clock for daily rhythms

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Abstract

Arginine vasopressin (AVP) signaling organizes the suprachiasmatic nucleus (SCN) into distinct anteroposterior domains.

Spatial mapping of gene expression revealed anterior and posterior domains for AVP signaling components within the SCN.
Distinct expression patterns of V1a and V1b AVP receptors suggest they have different roles in regulating SCN function.
Inhibiting V1A and V1B signaling altered SCN period and phase in a spatially specific manner.
V1 antagonism resulted in the longest period change in the anterior SCN and the largest phase change in the posterior SCN.
Separate antagonism of V1A and V1B signaling affected SCN function according to their anteroposterior expression patterns.
AVP signaling also influenced SCN period and phase along the dorsoventral axis, indicating broader effects on SCN organization.

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The suprachiasmatic nucleus (SCN) is the neural network that drives daily rhythms in behavior and physiology. The SCN encodes environmental changes through the phasing of cellular rhythms across its anteroposterior axis, but it remains unknown what signaling mechanisms regulate clock function along this axis. Here we demonstrate that arginine vasopressin (AVP) signaling organizes the SCN into distinct anteroposterior domains. Spatial mapping of SCN gene expression using in situ hybridization delineated anterior and posterior domains for AVP signaling components, including complementary patterns of V1a and V1b expression that suggest different roles for these two AVP receptors. Similarly, anteroposterior patterning of transcripts involved in Vasoactive Intestinal Polypeptide- and Prokineticin2 signaling was evident across the SCN. Using bioluminescence imaging, we then revealed that inhibiting V1A and V1B signaling alters period and phase differentially along the anteroposterior SCN. V1 antagonism lengthened period the most in the anterior SCN, whereas changes in phase were largest in the posterior SCN. Further, separately antagonizing V1A and V1B signaling modulated SCN function in a manner that mapped onto anteroposterior expression patterns. Lastly, V1 antagonism influenced SCN period and phase along the dorsoventral axis, complementing effects on the anteroposterior axis. Together, these results indicate that AVP signaling modulates SCN period and phase in a spatially specific manner, which is expected to influence how the master clock interacts with downstream tissues and responds to environmental changes. More generally, we reveal anteroposterior asymmetry in neuropeptide signaling as a recurrent organizational motif that likely influences neural computations in the SCN clock network.

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Asymmetric vasopressin signaling spatially organizes the master circadian clock

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