Auditory cortex is required for fear potentiation of gap detection

Journal of Neuroscience

Volumn 34, Issue 46, 2014, Pages 15437-15445

  Weible, Aldis P ^a   Liu, Christine ^a   Niell, Cristopher M ^a   Wehr, Michael ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Auditory cortex; Fear conditioning; Gap detection; Optogenetics

Indexed keywords

ATROPINE; DEXAMETHASONE; KETOPROFEN;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY RESPONSE; AUDITORY STIMULATION; AVERSION THERAPY; BEHAVIORAL SCIENCE; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; FEAR-POTENTIATED STARTLE TEST; FEMALE; FREEZING TOLERANCE; GAP DETECTION; HISTOLOGY; MALE; MOUSE; NONHUMAN; OPTOGENETICS; WHITE NOISE; ACTION POTENTIAL; ANIMAL; CONDITIONED REFLEX; FEAR; HEARING; NERVE CELL; NERVE CELL INHIBITION; PHYSIOLOGY; TIME; TRANSGENIC MOUSE;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; CONDITIONING, CLASSICAL; FEAR; FEMALE; MALE; MICE; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; OPTOGENETICS; TIME FACTORS;

EID: 84909983270     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3408-14.2014     Document Type: Article

References (53)

1. Armony JL, Servan-Schreiber D, Romanski LM, Cohen JD, LeDoux JE (1997) Stimulus generalization of fear responses: effects of auditory cortex lesions in a computational model and in rats. Cereb Cortex 7:157–165. CrossRef Medline
2. Bakin JS, Weinberger NM (1990) Classical conditioning induces CSspecific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res 536:271–286. CrossRef Medline
3. Bang SJ, Allen TA, Jones LK, Boguszewski P, Brown TH (2008) Asymmetrical stimulus generalization following differential fear conditioning. Neurobiol Learn Mem 90:200–216. CrossRef Medline
4. Bieszczad KM, Miasnikov AA, Weinberger NM (2013) Remodeling sensory cortical maps implants specific behavioral memory. Neuroscience 246: 40–51. CrossRef Medline
5. Boatman JA, Kim JJ (2006) A thalamo-cortico-amygdala pathway mediates audi-tory fear conditioning in the intact brain. Eur J Neurosci 24:894–900. CrossRef Medline
6. Brugge JF, Merzenich MM (1973) Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J Neurophysiol 36:1138–1158. Medline
7. Campeau S, Davis M (1995) Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15:2312–2327. Medline
8. Eggermont JJ (1999) Neural correlates of gap detection in three auditory cortical fields in the Cat. J Neurophysiol 81:2570–2581. Medline
9. Engineer CT, Perez CA, Chen YH, Carraway RS, Reed AC, Shetake JA, Jakkamsetti V, Chang KQ, Kilgard MP (2008) Cortical activity patterns predict speech discrimination ability. Nat Neurosci 11:603–608. CrossRef Medline
10. Fitzgibbons PJ, Gordon-Salant S (1996) Auditory temporal processing in elderly listeners. J Am Acad Audiol 7:183–189. Medline
11. Froemke RC, Merzenich MM, Schreiner CE (2007) A synaptic memory trace for cortical receptive field plasticity. Nature 450:425–429. CrossRef Medline
12. Glasberg BR, Moore BC, Bacon SP (1987) Gap detection and masking in hearing-impaired and normal-hearing subjects. J Acoust Soc Am 81: 1546–1556. CrossRef Medline
13. Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Dynamics of retrieval strategies for remote memories. Cell 147:678–689. CrossRef Medline
14. Han X, Chow BY, Zhou H, Klapoetke NC, Chuong A, Rajimehr R, Yang A, Baratta MV, Winkle J, Desimone R, Boyden ES (2011) A high-light sensitivity optical neural silencer: development and application to optogenetic control of nonhuman primate cortex. Front Syst Neurosci 5:18. CrossRef Medline
15. Ison JR, Pinckney LA (1983) Reflex inhibition in humans: sensitivity to brief silent periods in white noise. Percept Psychophys 34:84–88. CrossRef Medline
16. Ison JR, O’Connor K, Bowen GP, Bocirnea A (1991) Temporal resolution of gaps in noise by the rat is lost with functional decortication. Behav Neurosci 105:33–40. CrossRef Medline
17. Issa JB, Haeffele BD, Agarwal A, Bergles DE, Young ED, Yu DT (2014) Multiscale optical CA2+ imaging of tonal organization in mouse auditory cortex. Neuron 83:944–959. CrossRef Medline
18. Ji W, Suga N, Gao E (2005) Effects of agonists and antagonists of NMDA and ACh receptors on plasticity of bat auditory system elicited by fear conditioning. J Neurophysiol 94:1199–1211. CrossRef Medline
19. Kholodar-Smith DB, Allen TA, Brown TH (2008) Fear conditioning to discontinuous auditory cues requires perirhinal cortical function. Behav Neurosci 122:1178–1185. CrossRef Medline
20. Kudoh M, Nakayama Y, Hishida R, Shibuki K (2006) Requirement of the auditory association cortex for discrimination of vowel-like sounds in rats. Neuroreport 17:1761–1766. CrossRef Medline
21. Laxmi TR, Stork O, Pape HC (2003) Generalisation of conditioned fear and its behavioural expression in mice. Behav Brain Res 145:89–98. CrossRef Medline
22. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23: 155–184. CrossRef Medline
23. LeDoux JE, Sakaguchi A, Reis DJ (1984) Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. J Neurosci 4:683–698. Medline
24. LeDoux JE, Iwata J, Pearl D, Reis DJ (1986a) Disruption of auditory but not visual learning by destruction of intrinsic neurons in the rat medial geniculate body. Brain Res 371:395–399. CrossRef Medline
25. LeDoux JE, Sakaguchi A, Iwata J, Reis DJ (1986b) Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli. Neuroscience 17:615–627. CrossRef Medline
26. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, Herry C, Lüthi A (2011) A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480:331–335. CrossRef Medline
27. Li N, Ping J, Wu R, Wang C, Wu X, Li L (2008) Auditory fear conditioning modulates prepulse inhibition in socially reared rats and isolation-reared rats. Behav Neurosci 122:107–118. CrossRef Medline
28. Lindquist DH, Brown TH (2004) Temporal encoding in fear conditioning revealed through associative reflex facilitation. Behav Neurosci 118:395–402. CrossRef Medline
29. Lisker L, Abramson AS (1964) A cross-language study of voicing in initial stops: acoustical measurements. Word 20:384–422.
30. McLin DE III, Miasnikov AA, Weinberger NM (2002) Induction of behavioral associative memory by stimulation of the nucleus basalis. Proc Natl Acad Sci U S A 99:4002–4007. CrossRef Medline
31. Mechawar N, Cozzari C, Descarries L (2000) Cholinergic innervation in adult rat cerebral cortex: a quantitative immunocytochemical description. J Comp Neurol 428:305–318. CrossRef Medline
32. Moore AK, Wehr M (2013) Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J Neurosci 33: 13713–13723. CrossRef Medline
33. Ohl FW, Wetzel W, Wagner T, Rech A, Scheich H (1999) Bilateral ablation of auditory cortex in Mongolian gerbil affects discrimination of frequencymodulated tones but not of pure tones. LearnMem6:347–362. CrossRef Medline
34. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
35. Phillips DP, Hall SE, Boehnke SE (2002) Central auditory onset responses, and temporal asymmetries in auditory perception. Hear Res 167:192–205. CrossRef Medline
36. Plomp R (1964) The rate of decay of auditory sensation. J Acoust Soc Am 36:277–282. CrossRef
37. Poremba A, Gabriel M (1997) Medial geniculate lesions block amygdalar and cingulothalamic learning-related neuronal activity. J Neurosci 17: 8645–8655. Medline
38. Poremba A, Jones D, Gonzalez-Lima F (1998) Classical conditioning modifies cytochrome oxidase activity in the auditory system. Eur J Neurosci 10:3035–3043. CrossRef Medline
39. Romanski LM, LeDoux JE (1992) Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J Neurosci 12:4501–4509. Medline
40. Scheich H, Brechmann A, Brosch M, Budinger E, Ohl FW, Selezneva E, Stark H, Tischmeyer W, Wetzel W (2011) Behavioral semantics of learning and crossmodal processing in auditory cortex: the semantic processor concept. Hear Res 271:3–15. CrossRef Medline
41. Schneider BA, Pichora-Fuller MK, Kowalchuk D, Lamb M (1994) Gap detection and the precedence effect in young and old adults. J Acoust Soc Am 95:980–991. CrossRef Medline
42. Suga N, Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4:783–794. CrossRef Medline
43. Swerdlow NR, Geyer MA, Braff DL (2001) Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl) 156:194–215. CrossRef Medline
44. Tallal P, Stark RE, Mellits ED (1985) Identification of language-impaired children on the basis of rapid perception and production skills. Brain Lang 25:314–322. CrossRef Medline
45. Threlkeld SW, Penley SC, Rosen GD, Fitch RH (2008) Detection of silent gaps in white noise following cortical deactivation in rats. Neuroreport 19:893–898. CrossRef Medline
46. Walton JP, Frisina RD, Ison JR, O’Neill WE (1997) Neural correlates of behavioral gap detection in the inferior colliculus of the young CBA mouse. J Comp Physiol A 181:161–176. CrossRef Medline
47. Walton JP, Barsz K, Wilson WW (2008) Sensorineural hearing loss and neural correlates of temporal acuity in the inferior colliculus of the C57BL/6 mouse. J Assoc Res Otolaryngol 9:90–101. CrossRef Medline
48. Weible AP, Rowland DC, Monaghan CK, Wolfgang NT, Kentros CG (2012) Neural correlates of long-term object memory in the mouse anterior cingulate cortex. J Neurosci 32:5598–5608. CrossRef Medline
49. Weible AP, Moore AK, Liu C, DeBlander L, Wu H, Kentros C, Wehr M (2014) Perceptual gap detection is mediated by gap termination responses in auditory cortex. Curr Biol 24:1447–1455. CrossRef Medline
50. Weinberger NM (2004) Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5:279–290. CrossRef Medline
51. Weinberger NM (2007) Auditory associativememoryandrepresentational plasticity in the primary auditory cortex. Hear Res 229:54–68. CrossRef Medline
52. Zhang J, Laiwalla F, Kim JA, Urabe H, Van Wagenen R, Song YK, Connors BW, Zhang F, Deisseroth K, Nurmikko AV (2009) Integrated device for optical stimulation and spatiotemporal electrical recording of neural activity in lightsensitized brain tissue. J Neural Eng 6:055007. CrossRef Medline
53. Zou D, Wu X, Li L (2005) Fear conditioning facilitates rats gap detection measured by prepulse inhibition of the startle reflex. J Acoustical Society of America 117.