Sparse genetically defined neurons refine the canonical role of periaqueductal gray columnar organization
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During threat exposure, survival depends on defensive reactions. Prior works linked large glutamatergic populations in the midbrain periaqueductal gray (PAG) to defensive freezing and flight, and established that the overarching functional organization axis of the PAG is along anatomically-defined columns. Accordingly, broad activation of the dorsolateral column induces flight, while activation of the lateral or ventrolateral (l and vl) columns induces freezing. However, the PAG contains diverse cell types that vary in neurochemistry. How these cell types contribute to defense remains unknown, indicating that targeting sparse, genetically-defined populations may reveal how the PAG generates diverse behaviors. Though prior works showed that broad excitation of the lPAG or vlPAG causes freezing, we found in mice that activation of lateral and ventrolateral PAG (l/vlPAG) cholecystokinin-expressing (CCK) cells selectively caused flight to safer regions within an environment. Furthermore, inhibition of l/vlPAG-CCK cells reduced predator avoidance without altering other defensive behaviors like freezing. Lastly, l/vlPAG-CCK activity decreased when approaching threat and increased during movement to safer locations. These results suggest CCK cells drive threat avoidance states, which are epochs during which mice increase distance from threat and perform evasive escape. Conversely, l/vlPAG pan-neuronal activation promoted freezing, and these cells were activated near threat. Thus, CCK l/vlPAG cells have opposing function and neural activation motifs compared to the broader local ensemble defined solely by columnar boundaries. In addition to the anatomical columnar architecture of the PAG, the molecular identity of PAG cells may confer an additional axis of functional organization, revealing unexplored functional heterogeneity.
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Fernández‐Peña, C., Pace, R. L., Fernando, L. M., Sheppard, H., Pittman, B. G., & Schwarz, L. A. (2026) · Neuron · doi:10.1016/j.neuron.2026.06.012 · Cited by 1 · see citing works
Coizet, V., Tannir, R. A., Pautrat, A., & Overton, P. G. (2023) · Current Neuropharmacology · doi:10.2174/1570159x21666230818154903 · Cited by 2 · see citing works
Fundamentals of the septo-hippocampal system
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0009 · Cited by 1 · see citing works
Memory and the septo-hippocampal system
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0008 · Cited by 1 · see citing works
Adrenergic C1 neurons enhance anxiety via projections to PAGPreprint
Fernández‐Peña, C., Pace, R. L., Fernando, L. M., Pittman, B. G., & Schwarz, L. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.11.612440 · Cited by 1 · see citing works
Richards, B., Kilby, A. I., Cornish, J. L., Kim, J. H., Lawrence, A. J., & Perry, C. J. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.15.699820 · Cited by 1 · see citing works
Presynaptic temporal dynamics flexibly set input weights in the mouse escape circuitPreprint
Tan, Y. L., Thamilmaran, A., Zernicka-Glover, N. K., Campagner, D., & Branco, T. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.18.724906 · Cited by 1 · see citing works
What do hippocampal cell fields represent?
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0007
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0001
The neurology of anxiety—planning circuits
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0011
A theory of the septo-hippocampal system (SHS)
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0010
Symptoms and syndromes of anxiety
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0013
The neurology of anxiety—survival circuits
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0006
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0002
The treatment of anxiety and fear disorders
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0014
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0011
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0015
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0009
The anxiolytic drugs—our key tool
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0004
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0003
List of online appendices and reviews
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0010
A conceptual theory of the goal inhibition system
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0005
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0006
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0004
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0005
Richards, B. K., Kilby, A. I., Cornish, J. L., Kim, J. H., Lawrence, A. J., & Perry, C. J. (2026) · Brain Structure and Function · doi:10.1007/s00429-026-03146-0
Re-evaluation of the medial hypothalamic defence system through a cell-type lens
Hong, C. Y., & Kim, J. C. (2026) · Trends Open · doi:10.1016/j.treopn.2026.08.008
- Authors
- La-Vu, M. Q., Sethi, E., Maesta-Pereira, S., Schuette, P. J., Tobias, B. C., Reis, F. M., Wang, W., Torossian, A., Bishop, A., Leonard, S. J., Lin, L., Cahill, C. M., & Adhikari, A.
- Affiliations
- University of California, Los Angeles (US)
- Department of Psychology, University of California, Los Angeles
- Corresponding author
- Adhikari, Avishek
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2022-06-08
- Volume
- 11
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC9224993
- OpenAlex
- W4282921087
- Cited by
- 50
- References
- 74
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 28 · 2023: 6 · 2022: 2
- FWCI
- 5.54
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Institute of Mental Health (R00 MH106649, R01 MH119089, F31 MH121050-01A1)
- Achievement Rewards for College Scientists Foundation
- Brain and Behavior Research Foundation (22663, 27654, 27780)
- UCLA Health System (UCLA Affiliates fellowship)
- Hellman Foundation
- Fundação de Amparo à Pesquisa do Estado de São Paulo (2015/23092-3, 2017/08668-1)
- National Science Foundation (NSF-GRFP DGE-1650604)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- periaqueductal gray, defensive behavior, threat avoidance, flight behavior, freezing behavior, threat exposure, predator avoidance, glutamatergic neurons, neuronal heterogeneity
- MeSH terms
- Animals, Cholecystokinin, Fear, Neurons, Periaqueductal Gray, Mice
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