Shared Dorsal Periaqueductal Gray Activation Patterns during Exposure to Innate and Conditioned Threats

Author(s)

Reis, Fernando M. C. V. ^[1] ; Liu, Jinhan ^[2] ; Schuette, Peter J. ^[1] ; Lee, Johannes Y. ^[2] ; Maesta-Pereira, Sandra ^[1] ; Chakerian, Meghmik ^[1] ; Wang, Weisheng ^[1] ; Canteras, Newton S. ^[3] ; Kao, Jonathan C. ^[2] ; Adhikari, Avishek ^[1]

Affiliation

^[1] Univ Calif Los Angeles, Dept Psychol, Los Angeles, CA 90095 - USA

^[2] Univ Calif Los Angeles, Dept Elect & Comp Engn, Los Angeles, CA 90095 - USA

^[3] Univ Sao Paulo, Inst Biomed Sci, Dept Anat, BR-05508000 Sao Paulo, SP - Brazil

• Document type: Journal article
• Source: JOURNAL OF NEUROSCIENCE; v. 41, n. 37, p. 5399-5420, SEP 15 2021.
• Web of Science Citations: 0

Abstract

The dorsal periaqueductal gray (dPAG) is critical to generate defensive behaviors during encounters with threats of multiple modalities. Here we use longitudinal calcium transient recordings of dPAG ensembles in freely moving mice to show that this region uses shared patterns of activity to represent distance to an innate threat (a live predator) and a conditioned threat (a shock grid). We also show that dPAG neural activity can predict diverse defensive behaviors. These data indicate the dPAG uses conserved population-level activity patterns to encode and coordinate defensive behaviors during exposure to both innate The brainstem dorsal periaqueductal gray (dPAG) has been widely recognized as being a vital node orchestrating the responses to innate threats. Intriguingly, recent evidence also shows that the dPAG mediates defensive responses to fear conditioned contexts. However, it is unknown whether the dPAG displays independent or shared patterns of activation during exposure to innate and conditioned threats. It is also unclear how dPAG ensembles encode and predict diverse defensive behaviors. To address this question, we used miniaturized microscopes to obtain recordings of the same dPAG ensembles during exposure to a live predator and a fear conditioned context in male mice. dPAG ensembles encoded not only distance to threat, but also relevant features, such as predator speed and angular offset between mouse and threat. Furthermore, dPAG cells accurately encoded numerous defensive behaviors, including freezing, stretch-attend postures, and escape. Encoding of behaviors and of distance to threat occurred independently in dPAG cells. dPAG cells also displayed a shared representation to encode these behaviors and distance to threat across innate and conditioned threats. Last, we also show that escape could be predicted by dPAG activity several seconds in advance. Thus, dPAG activity dynamically tracks key kinematic and behavioral variables during exposure to threats, and exhibits similar patterns of activation during defensive behaviors elicited by innate or conditioned threats. These data indicate that a common pathway may be recruited by the dPAG during exposure to a wide variety of threat modalities. (AU)

• FAPESP's process: 15/23092-3 - Signaling pathways involved in fear memory to predatory threats
• Grantee: Fernando Midea Cuccovia Vasconcelos Reis
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 14/05432-9 - Neural bases of fear and aggression
• Grantee: Newton Sabino Canteras
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 17/08668-1 - In vivo study of GABAergic and glutamatergic neuronal populations of the periaqueductal gray matter in response to different kinds of threat
• Grantee: Fernando Midea Cuccovia Vasconcelos Reis
• Support Opportunities: Scholarships abroad - Research Internship - Post-doctor