Arginine–vasopressin-expressing neurons in the murine suprachiasmatic nucleus exhibit a circadian rhythm in network coherence in vivo

Jan 19, 2023Proceedings of the National Academy of Sciences of the United States of America

Daily rhythm in coordinated activity of hormone-producing neurons in the mouse brain’s body clock

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Abstract

SCN AVP neurons show periodic, slow likely reflecting burst firing.

Substantial heterogeneity in function is observed among AVP neurons, with unstable rhythms and weak rhythmicity at the population level.
Approximately 33% of neuron pairs exhibit rhythmic at any given time.
Coherence among AVP neuronal pairs demonstrates a strong rhythm at the population level, peaking at specific circadian times.
The timing of maximal coherence corresponds with peak neuronal activity for the SCN.
Interactions between AVP neurons may play a more significant role in regulating circadian rhythms than individual neuron activity.

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The suprachiasmatic nucleus (SCN) is composed of functionally distinct subpopulations of GABAergic neurons which form a neural network responsible for synchronizing most physiological and behavioral circadian rhythms in mammals. To date, little is known regarding which aspects of SCN rhythmicity are generated by individual SCN neurons, and which aspects result from neuronal interaction within a network. Here, we utilize in vivo miniaturized microscopy to measure fluorescent GCaMP-reported calcium dynamics in arginine vasopressin (AVP)-expressing neurons in the intact SCN of awake, behaving mice. We report that SCN AVP neurons exhibit periodic, slow which we demonstrate, using in vivo electrical recordings, likely reflect burst firing. Further, we observe substantial heterogeneity of function in that AVP neurons exhibit unstable rhythms, and relatively weak rhythmicity at the population level. Network analysis reveals that correlated cellular behavior, or , among neuron pairs also exhibited stochastic rhythms with about 33% of pairs rhythmic at any time. Unlike single-cell variables, coherence exhibited a strong rhythm at the population level with time of maximal coherence among AVP neuronal pairs at CT/ZT 6 and 9, coinciding with the timing of maximal neuronal activity for the SCN as a whole. These results demonstrate robust circadian variation in the coordination between stochastically rhythmic neurons and that interactions between AVP neurons in the SCN may be more influential than single-cell activity in the regulation of circadian rhythms. Furthermore, they demonstrate that cells in this circuit, like those in many other circuits, exhibit profound heterogenicity of function over time and space.

Key numbers

33%

Rhythmic Neuron Pairs

Percentage of AVP neuron pairs exhibiting rhythmic in calcium dynamics.

20%

Calcium Wave Dynamics

Percentage of AVP neurons exhibiting rhythmicity in calcium wave frequency.

35 to 50%

Dynamic Rhythmicity

Range of AVP neurons exhibiting rhythmicity on individual 24-hour days.

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Arginine–vasopressin-expressing neurons in the murine suprachiasmatic nucleus exhibit a circadian rhythm in network coherence in vivo

Abstract

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