Brainstem serotonin neurons selectively gate retinal information flow to thalamus

• Published in: Neuron (Cambridge, Mass.) Vol. 111; no. 5; pp. 711 - 726.e11
• Main Authors: Reggiani, Jasmine D.S., Jiang, Qiufen, Barbini, Melanie, Lutas, Andrew, Liang, Liang, Fernando, Jesseba, Deng, Fei, Wan, Jinxia, Li, Yulong, Chen, Chinfei, Andermann, Mark L.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.03.2023
• Subjects: 5-HT1B; Animals; Axons - physiology; Calcium; dLGN; dorsal raphe nucleus; Geniculate Bodies - physiology; glutamate release; htr1b; Mice; neuromodulation; Receptor, Serotonin, 5-HT1B - metabolism; retinal ganglion cell axons; Retinal Ganglion Cells - physiology; serotonin; Serotonin - metabolism; thalamus; Thalamus - physiology; two-photon calcium imaging; retinal ganglion cell axons; neuromodulation; dorsal raphe nucleus; dLGN; serotonin; htr1b; 5-HT1B; two-photon calcium imaging; glutamate release; thalamus
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2022.12.006

Retinal ganglion cell (RGC) types relay parallel streams of visual feature information. We hypothesized that neuromodulators might efficiently control which visual information streams reach the cortex by selectively gating transmission from specific RGC axons in the thalamus. Using fiber photometry recordings, we found that optogenetic stimulation of serotonergic axons in primary visual thalamus of awake mice suppressed ongoing and visually evoked calcium activity and glutamate release from RGC boutons. Two-photon calcium imaging revealed that serotonin axon stimulation suppressed RGC boutons that responded strongly to global changes in luminance more than those responding only to local visual stimuli, while the converse was true for suppression induced by increases in arousal. Converging evidence suggests that differential expression of the 5-HT1B receptor on RGC presynaptic terminals, but not differential density of nearby serotonin axons, may contribute to the selective serotonergic gating of specific visual information streams before they can activate thalamocortical neurons. [Display omitted] •Serotonin suppresses retinal axon spike-evoked presynaptic Ca2+ and glutamate release•Suppression was stronger in retinal axons driven by full-field luminance change•Serotonin and arousal suppress different subsets of retinal axons in thalamus•Serotonergic suppression may scale with 5-HT1B expression in retinal axonal boutons Reggiani et al. find that, in awake mouse primary thalamus, serotonin from brainstem inputs suppresses retinal axon bouton presynaptic calcium signals and glutamate release. Different retinal axon classes were more strongly suppressed by serotonin versus by pupil-linked arousal, indicating diverse gating of visual information streams before they activate thalamocortical neurons.