The tectonigral pathway regulates appetitive locomotion in predatory hunting in mice

Abstract

Appetitive locomotion is essential for animals to approach rewards, such as food and prey. The neuronal circuitry controlling appetitive locomotion is unclear. In a goal-directed behavior—predatory hunting, we show an excitatory brain circuit from the superior colliculus (SC) to the substantia nigra pars compacta (SNc) to enhance appetitive locomotion in mice. This tectonigral pathway transmits locomotion-speed signals to dopamine neurons and triggers dopamine release in the dorsal striatum. Synaptic inactivation of this pathway impairs appetitive locomotion but not defensive locomotion. Conversely, activation of this pathway increases the speed and frequency of approach during predatory hunting, an effect that depends on the activities of SNc dopamine neurons. Together, these data reveal that the SC regulates locomotion-speed signals to SNc dopamine neurons to enhance appetitive locomotion in mice.

Functional Organisation of the Mouse Superior Colliculus

“…(Takatoh et al, 2021)). Retrograde tracing experiments also suggest that different targets of SC receive input from different SC neurons: LP-projectors are separate from PBGN-projectors (Shang et al, 2018) and SNc-projectors (Huang et al, 2021); ZI-projectors are separate from PAGprojectors, MLR-projectors (Shang et al, 2019), and SNc-projectors (Huang et al, 2021); SNcprojectors are separate from VTA-projectors (Huang et al, 2021). Functional evidence is however limited, and it remains possible that individual neurons are involved in multiple aspects of approach.…”

“…(behaviour) Unilateral manipulation of excitatory SC input to the VTA modifies orienting towards conspecifics (Prévost-Solié et al, 2019), and bilateral activation and inhibition of SC inputs to the SNc facilitate and impair hunting behaviour respectively (Huang et al, 2021). Inhibiting SC input to the SNc does not affect escape responses to visual threats, suggesting a specialised role.…”

“…Circuits in lateral motor-related SC appear more important in triggering pursuit behaviours. Inhibition of lateral motor-related SC neurons (subthalamus or SNc-projecting) (Shang et al, 2019;Huang et al, 2021), or neurons concentrated in lateral motor-related SC (PITX2+) (Masullo et al, 2019) impairs pursuit, that is movements towards prey (Shang et al, 2019;Huang et al, 2021;Xie et al, 2021), food or conspecifics (Huang et al, 2021). Inhibition of lateral SC also affects the direction (Vale, 2020) but not the speed of escape behaviour (Vale, 2020) (Shang et al, 2019;Huang et al, 2021).…”

“…Inhibition of lateral motor-related SC neurons (subthalamus or SNc-projecting) (Shang et al, 2019;Huang et al, 2021), or neurons concentrated in lateral motor-related SC (PITX2+) (Masullo et al, 2019) impairs pursuit, that is movements towards prey (Shang et al, 2019;Huang et al, 2021;Xie et al, 2021), food or conspecifics (Huang et al, 2021). Inhibition of lateral SC also affects the direction (Vale, 2020) but not the speed of escape behaviour (Vale, 2020) (Shang et al, 2019;Huang et al, 2021). Direct manipulations of motor-related SC, however, are yet to reveal the relative contribution of intermediate and deep parts of SC in triggering these behaviours.…”

The Dopaminergic Control of Movement-Evolutionary Considerations

“…Additionally, recent work in mice has shown that a direct projection from the SC to the SNc regulates locomotion-speed signals to dopamine neurons, and enhances appetitive locomotion [ 72 ]. Moreover, direct projections to the VTA have been related to wakefulness and innate defensive behaviors [ 73 , 74 ], indicating that the SC-SNc/VTA pathway plays several important roles.…”