Auditory cortex controls sound-driven innate defense behaviour through corticofugal projections to inferior colliculus

Nature Communications

Volumn 6, Issue , 2015, Pages

  Xiong, Xiaorui R ^a,b   Liang, Feixue ^a,c   Zingg, Brian ^a,b   Ji, Xu Ying ^a,c   Ibrahim, Leena A ^a,b   Tao, Huizhong W ^a   Zhang, Li I ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DEFENSE BEHAVIOR; INHIBITION; INNATE BEHAVIOR; NEUROLOGY; SENSORY SYSTEM;

ANIMAL CELL; ARTICLE; AUDITORY CORTEX; BEHAVIOR; DEFENSIVE BEHAVIOR; FEMALE; INFERIOR COLLICULUS; MALE; MOUSE; NERVE CELL; NERVE FIBER; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; SOUND; ANIMAL; ANIMAL BEHAVIOR; AUDITORY STIMULATION; C57BL MOUSE; PHYSIOLOGY;

ANIMALIA;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; BEHAVIOR, ANIMAL; FEMALE; INFERIOR COLLICULI; MALE; MICE; MICE, INBRED C57BL;

EID: 84931291653     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8224     Document Type: Article

References (51)

1. Motta, S. C. et al. Dissecting the brain's fear system reveals the hypothalamus is critical for responding in subordinate conspecific intruders. Proc. Natl Acad. Sci. U. S. A. 106, 4870-4875 (2009).
2. Pagani, J. H., Rosen, J. B. The medial hypothalamic defensive circuit and 2, 5-dihydro-2, 4, 5-trimethylthiazoline (TMT) induced fear: comparison of electrolytic and neurotoxic lesions. Brain Res. 1286, 133-146 (2009).
3. Blanchard, D. C., Blanchard, R. J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J. Comp. Physiol. Psychol. 81, 281-290 (1972).
4. Yilmaz, M., Meister, M. Rapid innate defensive responses of mice to looming visual stimuli. Curr. Biol. 23, 2011-2015 (2013).
5. Litvin, Y., Blanchard, D. C., Blanchard, R. J. Rat 22 kHz ultrasonic vocalizations as alarm cries. Behav. Brain Res. 182, 166-172 (2007).
6. Choi, J. S., Brown, T. H. Central amygdala lesions block ultrasonic vocalization and freezing as conditional but not unconditional responses. J. Neurosci. 23, 8713-8721 (2003).
7. Brandao, M. L., Anseloni, V. Z., Pandossio, J. E., De Araujo, J. E., Castilho, V. M. Neurochemical mechanisms of the defensive behavior in the dorsal midbrain. Neurosci. Biobehav. Rev. 23, 863-875 (1999).
8. Eilam, D. Die hard: a blend of freezing and fleeing as a dynamic defense-implications for the control of defensive behavior. Neurosci. Biobehav. Rev. 29, 1181-1191 (2005).
9. Bandler, R., Shipley, M. T. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci. 17, 379-389 (1994).
10. Letzkus, J. J. et al. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331-335 (2011).
11. LeDoux, J. E. Rethinking the emotional brain. Neuron 73, 653-676 (2012).
12. Johansen, J. P., Cain, C. K., Ostroff, L. E., LeDoux, J. E. Molecular mechanisms of fear learning and memory. Cell 147, 509-524 (2011).
13. LeDoux, J. E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184 (2000).
14. Maren, S. Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 24, 897-931 (2001).
15. Haubensak, W. et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468, 270-276 (2010).
16. Fanselow, M. S., Poulos, A. M. The neuroscience of mammalian associative learning. Annu. Rev. Psychol. 56, 207-234 (2005).
17. Olsen, S. R., Bortone, D. S., Adesnik, H., Scanziani, M. Gain control by layer six in cortical circuits of vision. Nature 483, 47-52 (2012).
18. Xiong, X. R. et al. Interaural level difference-dependent gain control and synaptic scaling underlying binaural computation. Neuron 79, 738-753 (2013).
19. Zhou, M. et al. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 17, 841-850 (2014).
20. Weiner, J. A., Schreiner, C. E. in The Inferior Colliculus. (eds Winer, J. A., Schreiner, C. E. ) 1-68 (Springer, 2005).
21. Li, L. Y., Li, Y. T., Zhou, M., Tao, H. W., Zhang, L. I. Intracortical multiplication of thalamocortical signals in mouse auditory cortex. Nat. Neurosci. 16, 1179-1181 (2013).
22. Li, Y. T., Ibrahim, L. A., Liu, B. H., Zhang, L. I., Tao, H. W. Linear transformation of thalamocortical input by intracortical excitation. Nat. Neurosci. 16, 1324-1330 (2013).
23. Fenno, L., Yizhar, O., Deisseroth, K. The development and application of optogenetics. Annu. Rev. Neurosci. 34, 389-412 (2011).
24. Petersen, C. C., Crochet, S. Synaptic computation and sensory processing in neocortical layer 2/3. Neuron 78, 28-48 (2013).
25. Znamenskiy, P., Zador, A. M. Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination. Nature 497, 482-485 (2013).
26. Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793-802 (2012).
27. Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51 (2000).
28. Sun, Y. J., Kim, Y. J., Ibrahim, L. A., Tao, H. W., Zhang, L. I. Synaptic mechanisms underlying functional dichotomy between intrinsic-bursting and regular-spiking neurons in auditory cortical layer 5. J, Neurosci. 33, 5326-5339 (2013).
29. Huffman, R. F., Henson, Jr. O. W. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain. Res. Brain Res. Rev. 15, 295-323 (1990).
30. Winer, J. A. Decoding the auditory corticofugal systems. Hear. Res. 212, 1-8 (2006).
31. Petreanu, L., Mao, T., Sternson, S. M., Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142-1145 (2009).
32. Chow, B. Y. et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98-102 (2010).
33. Gruters, K. G., Groh, J. M. Sounds and beyond: multisensory and other nonauditory signals in the inferior colliculus. Front. Neural Circuits 6, 96 (2012).
34. Schenberg, L. C. et al. Functional specializations within the tectum defense systems of the rat. Neurosci. Biobehav. Rev. 29, 1279-1298 (2005).
35. Vianna, D. M., Brandao, M. L. Anatomical connections of the periaqueductal gray: specific neural substrates for different kinds of fear. Braz. J Med. Biol. Res. 36, 557-566 (2003).
36. Winer, J. A. Decoding the auditory corticofugal systems. Hear. Res. 207, 1-9 (2005).
37. Koch, M. The neurobiology of startle. Prog. Neurobiol. 59, 107-128 (1999).
38. Koch, M., Schnitzler, H. U. The acoustic startle response in rats-circuits mediating evocation, inhibition and potentiation. Behav. Brain Res. 89, 35-49 (1997).
39. Oliver, D. L. in The Inferior Colliculus. (eds Winer, J. A., Schreiner, C. E. ) (Springer, 2005).
40. Stebbings, K. A., Lesicko, A. M., Llano, D. A. The auditory corticocollicular system: molecular and circuit-level considerations. Hear. Res. 314, 51-59 (2014).
41. Suga, N., Xiao, Z., Ma, X., Ji, W. Plasticity and corticofugal modulation for hearing in adult animals. Neuron 36, 9-18 (2002).
42. Yan, W., Suga, N. Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat. Neurosci. 1, 54-58 (1998).
43. Bajo, V. M., Nodal, F. R., Moore, D. R., King, A. J. The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nat. Neurosci. 13, 253-260 (2010).
44. Li, L. Y. et al. A feedforward inhibitory circuit mediates lateral refinement of sensory representation in upper layer 2/3 of mouse primary auditory cortex. J. Neurosci. 34, 13670-13683 (2014).
45. Li, L. Y. et al. Differential receptive field properties of parvalbumin and somatostatin inhibitory neurons in mouse auditory cortex. Cereb. Cortex. doi:10. 1093/cercor/bht417 (2014).
46. Sun, Y. J. et al. Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature 465, 927-931 (2010).
47. Wu, G. K., Arbuckle, R., Liu, B. H., Tao, H. W., Zhang, L. I. Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58, 132-143 (2008).
48. Zhou, M. et al. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 17, 841-850 (2014).
49. Zingg, B. et al. Neural networks of the mouse neocortex. Cell 156, 1096-1111 (2014).
50. Liu, B. H., Wu, G. K., Arbuckle, R., Tao, H. W., Zhang, L. I. Defining cortical frequency tuning with recurrent excitatory circuitry. Nat. Neurosci. 10, 1594-1600 (2007).
51. Allen, T. A. et al. Imaging the spread of reversible brain inactivations using fluorescent muscimol. J. Neurosci. Methods 171, 30-38 (2008).