Midbrain circuits for defensive behaviour

Nature

Volumn 534, Issue 7606, 2016, Pages 206-212

  Tovote, Philip ^a   Esposito, Maria Soledad ^a,b   Botta, Paolo ^a,e   Chaudun, Fabrice ^c   Fadok, Jonathan P ^a   Markovic, Milica ^a   Wolff, Steffen B E ^a,f   Ramakrishnan, Charu ^d   Fenno, Lief ^d   Deisseroth, Karl ^d   Herry, Cyril ^c   Arber, Silvia ^a,b   Lüthi, Andreas ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c INSTITUT FRANÇOIS MAGENDIE   (France)

^d STANFORD UNIVERSITY   (United States)

^e CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

^f HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 2; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID;

ANATOMY; BRAIN; DEFENSE BEHAVIOR; NERVOUS SYSTEM DISORDER; NEUROLOGY; PHYSIOLOGICAL RESPONSE; SURVIVAL;

AMYGDALA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; COPING BEHAVIOR; DEFENSIVE BEHAVIOR; ELECTROPHYSIOLOGY; FREEZING; IN VITRO STUDY; IN VIVO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; LATENT PERIOD; MAGNOCELLULAR NUCLEUS; MESENCEPHALON; MOUSE; NEUROANATOMY; NONHUMAN; OPTOGENETICS; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CATALEPSY; CYTOLOGY; ESCAPE BEHAVIOR; MALE; MEDULLA OBLONGATA; METABOLISM; NERVE CELL INHIBITION; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; PHYSIOLOGY;

PRIMATES; RODENTIA;

AMYGDALA; ANIMALS; ESCAPE REACTION; FREEZING REACTION, CATALEPTIC; GABAERGIC NEURONS; GLUTAMIC ACID; MALE; MEDULLA OBLONGATA; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; OPTOGENETICS; PERIAQUEDUCTAL GRAY;

EID: 84973595215     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature17996     Document Type: Article

References (51)

1. Anderson, D. J. & Adolphs, R. A framework for studying emotions across species. Cell 157, 187-200 (2014).
2. Blanchard, D. C. & Blanchard, R. J. in Handbook of Anxiety and Fear Vol. 17 (eds Blanchard, R. J., Blanchard, D. C., Griebel, G. & Nutt, D.) Ch. 2.4, 63-79 (Academic, 2008).
3. LeDoux, J. Rethinking the emotional brain. Neuron 73, 653-676 (2012).
4. Deisseroth, K. Circuit dynamics of adaptive and maladaptive behaviour. Nature 505, 309-317 (2014).
5. Tovote, P., Fadok, J. P. & Lüthi, A. Neuronal circuits for fear and anxiety. Nature Rev. Neurosci. 16, 317-331 (2015).
6. Rosen, J. B. & Schulkin, J. From normal fear to pathological anxiety. Psychol. Rev. 105, 325-350 (1998).
7. Perusini, J. N. & Fanselow, M. S. Neurobehavioral perspectives on the distinction between fear and anxiety. Learn. Mem. 22, 417-425 (2015).
8. Blanchard, D. C., Griebel, G., Pobbe, R. & Blanchard, R. J. Risk assessment as an evolved threat detection and analysis process. Neurosci. Biobehav. Rev. 35, 991-998 (2011).
9. Blanchard, R. J. & Blanchard, D. C. Crouching as an index of fear. J. Comp. Physiol. Psychol. 67, 370-375 (1969).
10. Fanselow, M. S. & Bolles, R. C. Naloxone and shock-elicited freezing in the rat. J. Comp. Physiol. Psychol. 93, 736-744 (1979).
11. Blanchard, D. C., Griebel, G. & Blanchard, R. J. Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic. Neurosci. Biobehav. Rev. 25, 205-218 (2001).
12. Gross, C. T. & Canteras, N. S. The many paths to fear. Nature Rev. Neurosci. 13, 651-658 (2012).
13. Carrive, P. The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav. Brain Res. 58, 27-47 (1993).
14. Leman, S., Dielenberg, R. A. & Carrive, P. Effect of dorsal periaqueductal gray lesion on cardiovascular and behavioural responses to contextual conditioned fear in rats. Behav. Brain Res. 143, 169-176 (2003).
15. Tomaz, C., Brandão, M., Bagri, A., Carrive, P. & Schmitt, P. Flight behavior induced by microinjection of GABA antagonists into periventricular structures in detelencephalated rats. Pharmacol. Biochem. Behav. 30, 337-342 (1988).
16. Walker, P. & Carrive, P. Role of ventrolateral periaqueductal gray neurons in the behavioral and cardiovascular responses to contextual conditioned fear and poststress recovery. Neuroscience 116, 897-912 (2003).
17. Zhang, S. P., Bandler, R. & Carrive, P. Flight and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial midbrain periaqueductal gray of the cat. Brain Res. 520, 73-82 (1990).
18. Morgan, M. M. & Clayton, C. C. Defensive behaviors evoked from the ventrolateral periaqueductal gray of the rat: comparison of opioid and GABA disinhibition. Behav. Brain Res. 164, 61-66 (2005).
19. Fanselow, M. S. in The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Immunohistochemical Organization (eds Depaulis, A. & Bandler, R.) 151-173 (Plenum, 1991).
20. Bandler, R., Depaulis, A. & Vergnes, M. Identification of midbrain neurones mediating defensive behaviour in the rat by microinjections of excitatory amino acids. Behav. Brain Res. 15, 107-119 (1985).
21. Bandler, R. & Carrive, P. Integrated defence reaction elicited by excitatory amino acid microinjection in the midbrain periaqueductal grey region of the unrestrained cat. Brain Res. 439, 95-106 (1988).
22. Tovote, P. et al. Activation of central CRF receptor 1 by cortagine results in enhanced passive coping with a naturalistic threat in mice. Psychoneuroendocrinology 35, 887-895 (2010).
23. Rizvi, T. A., Ennis, M., Behbehani, M. M. & Shipley, M. T. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J. Comp. Neurol. 303, 121-131 (1991).
24. Oka, T., Tsumori, T., Yokota, S. & Yasui, Y. Neuroanatomical and neurochemical organization of projections from the central amygdaloid nucleus to the nucleus retroambiguus via the periaqueductal gray in the rat. Neurosci. Res. 62, 286-298 (2008).
25. Canteras, N. S., Simerly, R. B. & Swanson, L. W. Projections of the ventral premammillary nucleus. J. Comp. Neurol. 324, 195-212 (1992).
26. Silva, B. A. et al. Independent hypothalamic circuits for social and predator fear. Nature Neurosci. 16, 1731-1733 (2013).
27. Wang, L., Chen, I. Z. & Lin, D. Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron 85, 1344-1358 (2015).
28. An, X., Bandler, R., Ongür, D. & Price, J. L. Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J. Comp. Neurol. 401, 455-479 (1998).
29. Choi, J. S. & Kim, J. J. Amygdala regulates risk of predation in rats foraging in a dynamic fear environment. Proc. Natl Acad. Sci. USA 107, 21773-21777 (2010).
30. Behbehani, M. M. Functional characteristics of the midbrain periaqueductal gray. Prog. Neurobiol. 46, 575-605 (1995).
31. Depaulis, A., Morgan, M. M. & Liebeskind, J. C. GABAergic modulation of the analgesic effects of morphine microinjected in the ventral periaqueductal gray matter of the rat. Brain Res. 436, 223-228 (1987).
32. Vaughan, C. W., Ingram, S. L., Connor, M. A. & Christie, M. J. How opioids inhibit GABA-mediated neurotransmission. Nature 390, 611-614 (1997).
33. Ciocchi, S. et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468, 277-282 (2010).
34. LeDoux, J. E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184 (2000).
35. Knobloch, H. S. et al. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73, 553-566 (2012).
36. Wall, N. R., Wickersham, I. R., Cetin, A., De La Parra, M. & Callaway, E. M. Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc. Natl Acad. Sci. USA 107, 21848-21853 (2010).
37. Fenno, L. E. et al. Targeting cells with single vectors using multiple-feature Boolean logic. Nature Methods 11, 763-772 (2014).
38. Herry, C. et al. Switching on and off fear by distinct neuronal circuits. Nature 454, 600-606 (2008).
39. Lima, S. Q., Hromádka, T., Znamenskiy, P. & Zador, A. M. PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PLoS ONE 4, e6099 (2009).
40. Esposito, M. S., Capelli, P. & Arber, S. Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature 508, 351-356 (2014).
41. Orlovsky, G. N., Deliagina, T. G. & Grillner, S. in Neuronal Control of Locomotion: From Mollusc to Man Ch. 10 and 12 (Oxford Univ. Press, 1999).
42. Stamatakis, A. M. et al. A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80, 1039-1053 (2013).
43. Halladay, L. R. & Blair, H. T. Distinct ensembles of medial prefrontal cortex neurons are activated by threatening stimuli that elicit excitation vs. inhibition of movement. J. Neurophysiol. 114, 793-807 (2015).
44. Keay, K. A. & Bandler, R. Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci. Biobehav. Rev. 25, 669-678 (2001).
45. Depaulis, A., Keay, K. A. & Bandler, R. Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp. Brain Res. 90, 307-318 (1992).
46. Vianna, D. M., Landeira-Fernandez, J. & Brandão, M. L. Dorsolateral and ventral regions of the periaqueductal gray matter are involved in distinct types of fear. Neurosci. Biobehav. Rev. 25, 711-719 (2001).
47. Letzkus, J. J. et al. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331-335 (2011).
48. Wolff, S. B. et al. Amygdala interneuron subtypes control fear learning through disinhibition. Nature 509, 453-458 (2014).
49. Hangya, B., Pi, H. J., Kvitsiani, D., Ranade, S. P. & Kepecs, A. From circuit motifs to computations: mapping the behavioral repertoire of cortical interneurons. Curr. Opin. Neurobiol. 26, 117-124 (2014).
50. Lüthi, A. & Lüscher, C. Pathological circuit function underlying addiction and anxiety disorders. Nature Neurosci. 17, 1635-1643 (2014).
51. Franklin, K. B. J. & Paxinos, G. Atlas of the Mouse Brain 4th edn (Academic, 2001).