Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice

Abstract

Sequential encoding of motor programs is essential for behavior generation. However, whether it is critical for instinctive behavior is still largely unknown. Mouse hunting behavior typically contains a sequential motor program, including the prey search, chase, attack, and consumption. Here, we reveal that the neuronal activity in the lateral periaqueductal gray (LPAG) follows a sequential pattern and is time-locked to different hunting actions. Optrode recordings and photoinhibition demonstrate that LPAGVgat neurons are required for the prey detection, chase and attack, while LPAGVglut2 neurons are selectively required for the attack. Ablation of inputs that could trigger hunting, including the central amygdala, the lateral hypothalamus, and the zona incerta, interrupts the activity sequence pattern and substantially impairs hunting actions. Therefore, our findings reveal that periaqueductal gray neuronal ensembles encode the sequential hunting motor program, which might provide a framework for decoding complex instinctive behaviors.

Proposing a neural framework for the evolution of elaborate courtship displays

“…Hunting in mice involves sequential activation of three discrete stereotyped behaviors – chase, attack, and eating. Here, the authors of this study show that each motor action is controlled by a distinct subpopulation within the dorsolateral PAG and that behavioral-specific neuronal clusters are activated in sequential order during the stereotyped hunting sequence ( Yu et al, 2021 ). In this way, neural ensembles within the PAG itself appear to link different discrete motor acts into a more complex behavioral trait.…”

“…A recent exciting study investigating the role of PAG in the stereotyped predatorial hunting sequence in mice suggests this is possible. Specifically, using a combination of electrophysiological and optogenetic approaches, Yu et al, 2021 show that distinct populations of neurons in the dorsolateral PAG are associated with each of the three actions in this behavior (chase, attack, and eating) and that these populations are sequentially activated during hunting ( Yu et al, 2021 ). Such studies would require behavioral standardization across labs, as well as closely related species, to assess how these seemingly ‘micro behaviors’ might be sequenced to form a more complex ritualized display.…”

“…It is divided into often functionally separate, but interconnected, columns that fan out from the most dorsal part of the PAG to its most ventral portion ( Silva and McNaughton, 2019 ). Dorsal regions of the PAG act as the common motor output node for many instinctive survival behaviors, while different regions (or columns) within the dorsal PAG appear to contain action-selective codes for each of these different behaviors ( Yu et al, 2021 ). For the remainder of the review, we will largely focus on the dorsal PAG.…”

“…As such, our ideas are largely grounded in indirect evidence that otherwise points to the PAG as a major brain region that potentially drives motor programs that make up complex courtship routines. Foremost among this evidence is the fact that, in most vertebrate systems studied to date, the PAG is described as the primary motor output node for the regulation of instinctive and relatively complex survival actions, including forms of attack and defensive behavior, hunting, parenting, mating, and vocalization ( Evans et al, 2018 ; Falkner et al, 2020 ; Subramanian et al, 2008 ; Tovote et al, 2016 ; Tschida et al, 2019 ; Wei et al, 2021 ; Yu et al, 2021 ). A distinctive property of the PAG is that it is subdivided into molecularly and anatomically conserved subdivisions, or columns, that are tightly associated with the production of these distinct types of behavior ( Bandler and Keay, 1996 ; Bandler and Shipley, 1994 ).…”

Functional Organisation of the Mouse Superior Colliculus

“…Activation of medial SC populations concentrated in (NTSR1+) ( Gale and Murphy, 2014 ), or including (CAMK2+) ( Wei et al, 2015 ), the optic layer activates CeA and induces arrest ( Sans-Dublanc et al, 2021 ), and manipulating CeA alters freezing responses to visual looming stimuli ( Zelikowsky et al, 2018 ). CeA may promote arrest or freezing via several potential pathways, perhaps even through its projection to periaqueductal grey (PAG) ( Tovote et al, 2015 ; Vaaga et al, 2020 ; Yu et al, 2021 ).…”