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

Escaping towards shelter is an adaptive behaviour offering protection against predation. In mice, this is preceded by a fast, memory-guided head rotation towards the shelter[1]. It is not known how the escape circuit incorporates spatial information to execute rapid and accurate flights to safety. Here we show that retrosplenial cortex (RSP) and superior colliculus (SC) form a monosynaptic circuit that continuously encodes shelter direction and is necessary for spatially-accurate escape.
Using Neuropixels probes, we found head-shelter angle cells (HSAC) in RSP and SC. Both multivariate tuning curve analysis and generalized linear models showed HSA to be a key predictor of their firing rate. HSACs tile angular space such that HSA can be decoded accurately at the population level. Rabies tracing and channelrhodopsin-assisted circuit mapping revealed that both excitatory and inhibitory SC neurons receive monosynaptic input from RSP. This synapse is critical for HSA encoding in SC and accurate escape: chemogenetic inactivation of SC-projecting RSP neurons disrupted single-cell and population encoding of HSA in SC and resulted in inaccurate orientation to shelter during escape. No impairment was observed in sensory-guided orientation nor navigation-to-reward tasks, suggesting that RSP input to SC selectively conveys shelter position, but is not necessary for SC-based motor control. Next, we probed HSA encoding and population dynamics in excitatory and inhibitory SC neurons in response to RSP input using dual-opsin RSP stimulation and optotagging in vivo. We found an activity pattern compatible with RSP input mapping HSA onto the SC network using a centre-surround inhibition mechanism, that was modelled using spiking-RNNs constrained by experimental data.
Combining molecular, computational and electrophysiological techniques, we identified a circuit-motif through which spatial memories are transmitted to a motor-control area to guide goal-directed behaviour. This cortical-subcortical interface may be a general blueprint for increasing the flexibility of instinctive behaviours.
[1]Vale et al.,2017,Current Biology