Abstract
Animals promote their survival by avoiding rapidly approaching objects that indicate threats. In mice, looming-evoked defensive responses are triggered by the superior colliculus (SC) which receives direct retinal inputs. However, the specific neural circuits that begin in the retina and mediate this important behaviour remain unclear. Here we identify a subset of retinal ganglion cells (RGCs) that controls mouse looming-evoked defensive responses through axonal collaterals to the dorsal raphe nucleus (DRN) and SC. Looming signals transmitted by DRN-projecting RGCs activate DRN GABAergic neurons that in turn inhibit serotoninergic neurons. Moreover, activation of DRN serotoninergic neurons reduces looming-evoked defensive behaviours. Thus, a dedicated population of RGCs signals rapidly approaching visual threats and their input to the DRN controls a serotonergic self-gating mechanism that regulates innate defensive responses. Our study provides new insights into how the DRN and SC work in concert to extract and translate visual threats into defensive behavioural responses.
Highlights
Animals promote their survival by avoiding rapidly approaching objects that indicate threats
To deliver retrograde tracer into the dorsal raphe nucleus (DRN) while avoiding the retinorecipient superior colliculus (SC), an angled approach was used and the DRN was reached by passing the electrode through the inferior colliculus (Fig. 1a); each animal (n 1⁄4 8) received a single injection of 200 nl of cholera toxin B subunit (CTB) conjugated to Alexa Fluor 488 (CTB-488)
Injections centred in the DRN with no contamination of the SC (Fig. 1b and Supplementary Fig. 1a–e) labelled approximately 600 retinal ganglion cells (RGCs) uniformly distributed across the retina (573±21 RGCs per retina, n 1⁄4 16; Fig. 1c)
Summary
Animals promote their survival by avoiding rapidly approaching objects that indicate threats. We identify a subset of retinal ganglion cells (RGCs) that controls mouse looming-evoked defensive responses through axonal collaterals to the dorsal raphe nucleus (DRN) and SC. A dedicated population of RGCs signals rapidly approaching visual threats and their input to the DRN controls a serotonergic self-gating mechanism that regulates innate defensive responses. If the DRN received looming-related signals transmitted from RGCs with branching axons innervating the SC, it might be in a position to modulate looming-evoked behaviour via its extensive 5-HT projections. We report that DRN/SC-projecting RGCs are necessary for looming-induced defensive responses and that DRN 5-HT neuron activity regulates the circuits that control looming-evoked behaviour
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