A cortico-collicular circuit for accurate orientation to shelter during escape

Abstract

When faced with predatorial threats, escaping towards shelter is an adaptive action that offers long-term protection against the attacker. From crustaceans to mammals, animals rely on knowledge of safe locations in the environment to rapidly execute shelter-directed escape actions1–3. While previous work has identified neural mechanisms of instinctive escape4–9, it is not known how the escape circuit incorporates spatial information to execute rapid and accurate flights to safety. Here we show that mouse retrosplenial cortex (RSP) and superior colliculus (SC) form a monosynaptic circuit that continuously encodes the shelter direction. Inactivation of SC-projecting RSP neurons decreases SC shelter-direction tuning while preserving SC motor function. Moreover, specific inactivation of RSP input onto SC neurons disrupts orientation and subsequent escapes to shelter, but not orientation accuracy to a sensory cue. We conclude that the RSC-SC circuit supports an egocentric representation of shelter direction and is necessary for optimal shelter-directed escapes. This cortical-subcortical interface may be a general blueprint for increasing the sophistication and flexibility of instinctive behaviours.

The retrosplenial cortex combines internal and external cues to encode head velocity during navigation

“…In addition, a gold pin was inserted inside a craniotomy rostral to the Bregma, secured to the skull, and attached to the ground wire. Neuropixels implants were additionally secured inside a custom-built 3D printed enclosure (43).…”

“…Open-field experiments. Open-field recordings were performed on an elevated 92-cm diameter circular arena located inside a 140 x 140 x 160 cm sound-proof enclosure (43). A surrounding hectagonal black wall (45 cm high from the arena surface) was placed at approximately 10-cm distance from its circumference.…”

“…To reconcile these data, we identified cortical AHV cells during navigation and, for the first time, determined their response properties to isolated and conjunctive sensory stimuli. We focused on AHV cells in the RSP since it is a cortical region forming part of the head direction network, encodes spatial and movement-related information (28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41)(42)(43), and is critically involved in spatial orientation and self motion-guided navigation (44)(45)(46)(47)(48)(49)(50).…”

Unraveling circuits of visual perception and cognition through the superior colliculus

“…In addition, stress accelerates looming-evoked escape in mice, and the locus coeruleus mediates the effect of stress via a projection from tyrosine-hydroxylase-positive neurons to the intermediate layer of the SC (Li et al, 2018). Finally, the projection of layer 5 neurons in the mouse retrosplenial cortex to the SC appears to encode the direction of shelter, as its inactivation disrupts sound-induced and shelter-directed escape behavior (Vale et al, 2020). Even in humans, the SC-pulvinar-amygdala pathway is activated when exposed to threat (Koller et al, 2019).…”

Construction of a hippocampal cognitive map depends upon spatial context

“…One possibility is the different circuits that underlie the initiation of locomotion and the initiation of goal-directed forelimb movements. The initiation of a navigational trajectory involves an orienting response and triggering of locomotion initiated in a circuit thought to include (at least) superior colliculus and mesencephalic locomotor areas [85][86][87] . As might be expected a priori from mutually exclusive actions, skilled forelimb movements are thought to be initiated via distinct cortical and subcortical areas including the premotor and primary motor cortical regions and reticular nuclei 69,70,88,89 .…”