Light and dopamine impact two circadian neurons to promote morning wakefulness

Aug 14, 2024Current biology : CB

Light and dopamine influence two daily rhythm neurons to support waking up in the morning

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Abstract

Single-cell sequencing identified 17 Drosophila circadian neuron groups, including two that express the neuropeptide ion transport peptide (ITP) and are crucial for morning activity.

Inhibiting the two ITP-expressing lateral neurons significantly reduces morning activity in Drosophila.
These neurons express higher levels of the type 1-like dopamine receptor Dop1R1 compared to other lateral neurons.
Mutating Dop1R1 in the two ITP neurons leads to significantly decreased morning activity.
Dop1R1 activation in these neurons shows stronger responses to dopamine in the morning than at other times.
Morning levels of Dop1R1 mRNA are higher and are influenced by light exposure.

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In both mammals and flies, circadian brain neurons orchestrate physiological oscillations and behaviors like wake and sleep-these neurons can be subdivided by morphology and by gene expression patterns. Recent single-cell sequencing studies identified 17 Drosophila circadian neuron groups. One of these includes only two lateral neurons (LNs), which are marked by the expression of the neuropeptide ion transport peptide (ITP). Although these two ITPLNs have long been grouped with five other circadian evening activity cells, inhibiting the two neurons alone strongly reduces morning activity, indicating that they also have a prominent morning function. As dopamine signaling promotes activity in Drosophila, like in mammals, we considered that dopamine might influence this morning activity function. Moreover, the ITPLNs express higher mRNA levels than other LNs of the type 1-like dopamine receptor Dop1R1. Consistent with the importance of Dop1R1, cell-specific CRISPR-Cas9 mutagenesis of this receptor in the two ITPLNs renders flies significantly less active in the morning, and ex vivo live imaging shows Dop1R1-dependent cyclic AMP (cAMP) responses to dopamine in these two neurons. Notably, the response is more robust in the morning, reflecting higher morning Dop1R1 mRNA levels in the two neurons. As mRNA levels are not elevated in constant darkness, this suggests light-dependent upregulation of morning Dop1R1 transcript levels. Taken together with the enhanced morning cAMP response to dopamine, the data indicate how light and dopamine promote morning wakefulness in flies, mimicking the important effect of light on morning wakefulness in humans. + + +

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Light and dopamine impact two circadian neurons to promote morning wakefulness

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