A subcortical excitatory circuit for sensory-triggered predatory hunting in mice

Abstract

Predatory hunting plays a fundamental role in animal survival. Little is known about the neural circuits that convert sensory cues into neural signals to drive this behavior. Here we identified an excitatory subcortical neural circuit from the superior colliculus to the zona incerta that triggers predatory hunting. The superior colliculus neurons that form this pathway integrate motion-related visual and vibrissal somatosensory cues of prey. During hunting, these neurons send out neural signals that are temporally correlated with predatory attacks, but not with feeding after prey capture. Synaptic inactivation of this pathway selectively blocks hunting for prey without impairing other sensory-triggered behaviors. These data reveal a subcortical neural circuit that is specifically engaged in translating sensory cues into neural signals to provoke predatory hunting.

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Fig. 1: Activation of the SC–S pathway provokes predatory hunting.
Fig. 2: The SC–S pathway is selectively required for predatory hunting.
Fig. 3: Characterization of subthalamus-projecting SC neurons.
Fig. 4: Single-unit recording from antidromically identified subthalamus-projecting SC neurons.
Fig. 5: Subthalamus-projecting SC neurons specifically encode predatory attack.
Fig. 6: GABA+ ZI neurons are the postsynaptic target of the SC–S pathway to mediate sensory-triggered predatory hunting.

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

Code availability

The MATLAB code for data analyses is available from the corresponding author upon request.

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Acknowledgements

The authors thank T. Südhof, K. Deisseroth, L. Luo, M. Luo and M. He for providing the plasmids and mouse lines. They also thank members of the Neuroscience Pioneer Club for valuable discussions. This work was supported by the National Natural Science Foundation of China (31671095, 31422026, 81471311, 31771150 and 91632301) and Startup Funding at NIBS. All data are archived at the NIBS.

Author information

P.C. conceived the study. C.S. performed the injections and fiber implantations. C.S., A.L. Z.X. and Y.L. performed the behavioral tests. C.S., Z.X. and A.L. performed the fiber photometry recording. C.S. Z.X., M.H. and A.L. conducted the histological analyses. C.S. and Z.C. performed slice physiology. W.S. and Y.W. provided the reagents. D.L., C.S., A.L., Z.C. and P.C. analyzed the data. P.C. wrote the manuscript.

Correspondence to Peng Cao.

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Competing interests

The authors declare no competing interests.

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Journal peer review information: Nature Neuroscience thanks Jennifer Hoy, Daesoo Kim, and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Figures 1–25 and Supplementary Tables 1–5.

Reporting Summary

Supplementary Video 1

Prey–predator distance measurement during predatory hunting. This movie shows the video taken by the overhead camera. The distance between prey (a cockroach) and predator (an example WT mouse) is continuously measured and shown with a green line between the centroids of the prey and predator. The time course of prey–predator distance (PPD) is plotted in real time during predatory hunting.

Supplementary Video 2

Predatory jaw attacks during predatory hunting. This movie shows the videos taken by the two horizontal cameras. The jaw attacks of the example WT mouse are marked with yellow vertical lines during its predatory hunting. Although the mouse also uses its paws to attack the cockroach, the frequency of paw attack is much lower than that of jaw attack.

Supplementary Video 3

Optogenetic activation of SC–S pathway promotes predatory hunting. By comparing the performance of the same mouse in laser-off phase (00:01–00:36) and in laser-on phase (00:39–01:10), this movie shows that optogenetic activation of SC–S pathway increases the efficiency of predatory hunting.

Supplementary Video 4

Activation of SC–S pathway provoked hunting without inducing food consumption. This movie shows that photostimulation of SC–S pathway specifically provoked hunting behavior without inducing food consumption when food pellet and prey were simultaneously present in the arena.

Supplementary Video 5

Activation of SC–S pathway provoked hunting without inducing social aggression. This movie shows that photostimulation of SC–S pathway specifically provoked hunting behavior without inducing attacks to social target when conspecifics and prey were simultaneously present in the arena.

Supplementary Video 6

In the absence of prey, activation of SC–S pathway induced hunting-related behavioral actions. This movie shows that, in an arena with corn-cob bedding but without prey, photostimulation of SC–S pathway induced hunting-related behavioral actions. This movie was captured with a high-speed camera (160 frames/s).

Supplementary Video 7

Effects of inactivation of SC–S pathway on predatory hunting. By comparing the performance of mice without (Ctrl mouse) or with (TeNT mouse) synaptic inactivation of SC–S pathway, this movie shows that inactivation of SC–S pathway impairs predatory hunting.

Supplementary Video 8

Effects of inactivation of SC–S pathway on visually triggered defensive behavior. By comparing the performance of mice without (Ctrl mouse) or with (TeNT mouse) synaptic inactivation of SC–S pathway, this movie shows that inactivation of SC–S pathway does not alter visually triggered defensive behavior.

Supplementary Video 9

Mouse strongly prefers to chase and attack a moving cockroach rather than a stationary one. In this movie, two cockroaches were simultaneously introduced to the mouse in the arena. One cockroach freely moved, the other was stationary in paralysis. The mouse readily chased and attacked the moving cockroach and ignored the stationary cockroach.

Supplementary Video 10

GCaMP signals of SC–S pathway in parallel with predatory hunting. This movie shows predatory hunting of an example mouse displayed in parallel with the trace of GCaMP signal and the time course of jaw attacks. It can be observed that the peaks of GCaMP signal is temporally matched with the jaw attacks of the mouse.

Supplementary Video 11

GCaMP signals of SC–S pathway during investigation of a textured object. This movie shows the trace of GCaMP signal in parallel with the investigation of a textured object (wood cube). It can be observed that the peaks of GCaMP signal is temporally matched with the vibrissal touch to the object.

Supplementary Video 12

S-projecting SC neurons are activated when the mouse attacks the prey. In this movie, GCaMP signal of an S-projecting SC neuron is displayed in parallel with jaw attacks during predatory hunting for a restrained prey. Note that S-projecting SC neurons are activated when the mouse attacks the prey.

Supplementary Video 13

MLR-projecting SC neurons are activated when the mouse starts to approach the prey. In this movie, GCaMP signal of MLR-projecting SC neurons is displayed in parallel with jaw attacks during predatory hunting for a restrained prey. Note that MLR-projecting SC neurons are activated when the mouse starts to approach the prey.

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