Adult plasticity in the subcortical auditory pathway of the maternal mouse

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Miranda, Jason A ^a,b   Shepard, Kathryn N ^a,b   McClintock, Shannon K ^a   Liu, Robert C ^a,b,c  

^a EMORY UNIVERSITY   (United States)

^b Georgia State University   (United States)

^c Center for Translational Social Neuroscience   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN;

ACOUSTIC NERVE FIBER; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY SYSTEM; AUDITORY THRESHOLD; BASAL GANGLION; BRAIN STEM; CALIBRATION; COCHLEAR NERVE; ELECTRODE; FEMALE; LATENT PERIOD; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PERSONAL EXPERIENCE; PREGNANCY; ANIMAL; AUDITORY NERVOUS SYSTEM; HEARING; PHYSIOLOGY; VOCALIZATION;

ANIMALS; AUDITORY PATHWAYS; AUDITORY PERCEPTION; BRAIN STEM; FEMALE; MICE; NEURONAL PLASTICITY; PREGNANCY; VOCALIZATION, ANIMAL;

EID: 84903761844     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101630     Document Type: Article

References (92)

1. de Boer J, Thornton ARD (2008) Neural correlates of perceptual learning in the auditory brainstem: Efferent activity predicts and reflects improvement at a speech-in-noise discrimination task. J Neurosci 28: 4929-4937.
2. Song JH, Skoe E, Wong PC, Kraus N (2008) Plasticity in the adult human auditory brainstem following short-term linguistic training. J Cogn Neurosci 20: 1892-1902.
3. Strait DL, Kraus N, Skoe E, Ashley R (2009) Musical experience and neural efficiency: effects of training on subcortical processing of vocal expressions of emotion. Eur J Neurosci 29: 661-668.
4. Krishnan A, Gandour JT, Bidelman GM (2010) The effects of tone language experience on pitch processing in the brainstem. J Neurolinguistics 23: 81-95.
5. Krishnan A, Gandour JT, Smalt CJ, Bidelman GM (2010) Language-dependent pitch encoding advantage in the brainstem is not limited to acceleration rates that occur in natural speech. Brain Lang 114: 193-198.
6. Tzounopoulos T, Kraus N (2009) Learning to encode timing: mechanisms of plasticity in the auditory brainstem. Neuron 62: 463-469.
7. Wu SH, Ma CL, Sivaramakrishnan S, Oliver DL (2002) Synaptic modification in neurons of the central nucleus of the inferior colliculus. Hear Res 168: 43-54. (Pubitemid 34756869)
8. King AJ, Dahmen JC, Keating P, Leach ND, Nodal FR, et al. (2011) Neural circuits underlying adaptation and learning in the perception of auditory space. Neurosci Biobehav Rev 35: 2129-2139.
9. Liu X, Yan Y, Wang Y, Yan J (2010) Corticofugal modulation of initial neural processing of sound information from the ipsilateral ear in the mouse. PloS one 5: e14038.
10. Luo F, Wang Q, Kashani A, Yan J (2008) Corticofugal modulation of initial sound processing in the brain. J Neurosci 28: 11615-11621.
11. Suga N (2012) Tuning shifts of the auditory system by corticocortical and corticofugal projections and conditioning. Neurosci Biobehav Rev 36: 969-988.
12. Sanes DH, Constantine-Paton M (1985) The development of stimulus following in the cochlear nerve and inferior colliculus of the mouse. Brain Res 354: 255- 267.
13. Sanes DH, Constantine-Paton M (1985) The sharpening of frequency tuning curves requires patterned activity during development in the mouse, Mus musculus. J Neurosci 5: 1152-1166. (Pubitemid 15098425)
14. Yu X, Sanes DH, Aristizabal O, Wadghiri YZ, Turnbull DH (2007) Large-scale reorganization of the tonotopic map in mouse auditory midbrain revealed by MRI. Proc Natl Acad Sci U S A 104: 12193-12198. (Pubitemid 47185652)
15. Ehret G (2005) Infant rodent ultrasounds - A gate to the understanding of sound communication. Behav Genet 35: 19-29.
16. Liu RC, Miller KD, Merzenich MM, Schreiner CE (2003) Acoustic variability and distinguishability among mouse ultrasound vocalizations. J Acoust Soc of Am 114: 3412-3422. (Pubitemid 37553651)
17. Haack B, Markl H, Ehret G (1983) Sound communication between parents and offspring. In: J. F Willott, editor editors. The auditory psychobiology of the mouse. Charles C Thomas Pub Ltd 57-97.
18. Ehret G, Koch M, Haack B, Markl H (1987) Sex and parental experience determine the onset of an instinctive behavior in mice. Naturwissenschaften 74: 47-47.
19. Galindo-Leon EE, Lin FG, Liu RC (2009) Inhibitory plasticity in a lateral band improves cortical detection of natural vocalizations. Neuron 62: 705-716.
20. Liu RC, Linden JF, Schreiner CE (2006) Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. Eur J of Neurosci 23: 3087-3097. (Pubitemid 43882889)
21. Liu RC, Schreiner CE (2007) Auditory cortical detection and discrimination correlates with communicative significance. PloS Biol 5: 1426-1439. (Pubitemid 47105337)
22. Cohen L, Rothschild G, Mizrahi A (2011) Multisensory integration of natural odors and sounds in the auditory cortex. Neuron 72: 357-369.
23. Rothschild G, Cohen L, Mizrahi A, Nelken I (2013) Elevated correlations in neuronal ensembles of mouse auditory cortex following parturition. J Neurosci 33: 12851-12861.
24. Al-Mana D, Ceranic B, Djahanbakhch O, Luxon LM (2008) Hormones and the auditory system: a review of physiology and pathophysiology. Neuroscience 153: 881-900.
25. Miranda JA, Liu RC (2009) Dissecting natural sensory plasticity: hormones and experience in a maternal context. Hear Res 252: 21-28.
26. Ehret G, Koch M (1989) Ultrasound-induced parental behavior in house mice is controlled by female sex hormones and parental experience. Ethology 80: 81-93.
27. Ehret G, Schmid C (2009) Reproductive cycle-dependent plasticity of perception of acoustic meaning in mice. Physiol Behav 96: 428-433.
28. Caruso S, Maiolino L, Agnello C, Garozzo A, Di Mari L, et al. (2003) Effects of patch or gel estrogen therapies on auditory brainstem response in surgically postmenopausal women: a prospective, randomized study. Fertil and Steril 79: 556-561. (Pubitemid 36293451)
29. Charitidi K, Canlon B (2010) Estrogen receptors in the central auditory system of male and female mice. Neuroscience 165: 923-933.
30. Coleman JR, Campbell D, Cooper WA, Welsh MG, Moyer J (1994) Auditory brainstem responses after ovarectomy and estrogen replacement in rat. Hear Res 80: 209-215. (Pubitemid 24360023)
31. Hultcrantz M, Simonoska R, Stenberg AE (2006) Estrogen and hearing: a summary of recent investigations. Acta Otolaryngol 126: 10-14. (Pubitemid 41781820)
32. Maney DL, Cho E, Goode CT (2006) Estrogen-dependent selectivity of genomic responses to birdsong. Eur J of Neurosci 23: 1523-1529.
33. Remage-Healey L, Coleman MJ, Oyama RK, Schlinger BA (2010) Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proc Natl Acad Sci U S A 107: 3852-3857.
34. Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305: 404-407. (Pubitemid 38938158)
35. Tremere LA, Jeong JK, Pinaud R (2009) Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 29: 5949-5963.
36. Tremere LA, Pinaud R (2011) Brain-generated estradiol drives long-term optimization of auditory coding to enhance the discrimination of communication signals. J Neurosci 31: 3271-3289.
37. Yovanof S, Feng AS (1983) Effects of estradiol on auditory evoked responses from the frog's auditory midbrain. Neurosci Lett 36: 291-297. (Pubitemid 13089824)
38. Barkley MS, Geschwind II, Bradford GE (1979) Gestational pattern of estradiol, testosterone and progesterone secretion in selected strains of mice. Biol Reprod 20: 733-738. (Pubitemid 9184941)
39. McCormack JT, Greenwald GS (1974) Progesterone and oestradiol-17beta concentrations in peripheral plasma during pregnancy in mouse. J Endocrinol 62: 101-107.
40. Zheng QY, Johnson KR, Erway LC (1999) Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses. Hear Res 130: 94-107. (Pubitemid 29172586)
41. Willott JF (2006) Measurement of the auditory brainstem response (ABR) to study auditory sensitivity in mice. Curr Protoc Neurosci Chapter 8: Unit8 21B.
42. Zhou XM, Jen PHS, Seburn KL, Frankel WN, Zheng QY (2006) Auditory brainstem responses in 10 inbred strains of mice. Brain Res 1091: 16-26. (Pubitemid 43993889)
43. Radziwon KE, June KM, Stolzberg DJ, Xu-Friedman MA, Salvi RJ, et al. (2009) Behaviorally measured audiograms and gap detection thresholds in CBA/CaJ mice. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195: 961-969.
44. Parham K, Xiao-Ming S, Kim DO (2001) Noninvasive assesment of auditory function in mice: Auditory brainstem response and distortion product otoacoustic emissions. In: J. F Willott, editor editors. Handbook of mouse auditory research: from behavior to molecular biology. Boca Raton, Florida: CRC Press LLC. 37-58.
45. McGinley MJ, Liberman MC, Bal R, Oertel D (2012) Generating synchrony from the asynchronous: compensation for cochlear traveling wave delays by the dendrites of individual brainstem neurons. J Neurosci 32: 9301-9311.
46. Pauli-Magnus D, Hoch G, Strenzke N, Anderson S, Jentsch TJ, et al. (2007) Detection and differentiation of sensorineural hearing loss in mice using auditory steady-state responses and transient auditory brainstem responses. Neuroscience 149: 673-684. (Pubitemid 47633030)
47. Henry KR (1979) Auditory brainstem volume-conducted responses: origins in the laboratory mouse. J Am Aud Soc 4: 173-178.
48. Jerger J, Hall J (1980) Effects of Age and Sex on Auditory Brainstem Response. Arch Otolaryngol 106: 387-391. (Pubitemid 10071618)
49. Ehret G, Buckenmaier J (1994) Estrogen-Receptor Occurrence in the Female Mouse-Brain - Effects of Maternal Experience, Ovariectomy, Estrogen and Anosmia. J Physiol Paris 88: 315-329.
50. Numan M (2006) Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behav Cogn Neurosci Rev 5: 163-190.
51. Rosenblatt JS, Mayer AD, Giordano AL (1988) Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 13: 29-46.
52. Dubuc PU (1985) Effects of estrogen on food intake, body weight, and temperature of male and female obese mice. Proc Soc Exp Biol Med 180: 468-473.
53. Wade GN, Gray JM (1979) Gonadal effects on food intake and adiposity: a metabolic hypothesis. Physiol Behav 22: 583-593. (Pubitemid 9169176)
54. Fritz JB, Elhilali M, David SV, Shamma SA (2007) Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in Al? Hear Res 229: 186-203. (Pubitemid 46924825)
55. Galbraith GC, Olfman DM, Huffman TM (2003) Selective attention affects human brain stem frequency-following response. Neuroreport 14: 735-738. (Pubitemid 36570932)
56. Hernández-Peón R, Scherrer H, Jouvet M (1956) Modification of Electric Activity in Cochlear Nucleus during "Attention" in Unanesthetized Cats. Science 123: 331-332.
57. Hoormann J, Falkenstein M, Hohnsbein J (2004) Effects of spatial attention on the brain stem frequency-following potential. Neuroreport 15: 1539-1542. (Pubitemid 38971167)
58. Maison S, Micheyl C, Collet L (2001) Influence of focused auditory attention on cochlear activity in humans. Psychophysiology 38: 35-40. (Pubitemid 32154943)
59. Brozoski TJ, Bauer CA, Caspary DM (2002) Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J Neurosci 22: 2383-2390. (Pubitemid 35386537)
60. Kaltenbach JA, Zhang J, Afman CE (2000) Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure. Hear Res 147: 282-292. (Pubitemid 30658073)
61. Wang H, Brozoski TJ, Caspary DM (2011) Inhibitory neurotransmission in animal models of tinnitus: Maladaptive plasticity. Hear Res 279: 111-117.
62. Zhang JS, Kaltenbach JA (1998) Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound. Neurosci Lett 250: 197-200. (Pubitemid 28355811)
63. Wang H, Brozoski TJ, Turner JG, Ling L, Parrish JL, et al. (2009) Plasticity at glycinergic synapses in dorsal cochlear nucleus of rats with behavioral evidence of tinnitus. Neuroscience 164: 747-759.
64. Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27: 676-682. (Pubitemid 39335838)
65. Levine RA (1999) Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. Am J Otolaryngol 20: 351-362.
66. Jewett DL (1970) Volume-conducted potentials in response to auditory stimuli as detected by averaging in the cat. Electroencephalogr Clin Neurophysiol 28: 609-618.
67. Caruso S, Cianci A, Grasso D, Agnello C, Galvani F, et al. (2000) Auditory brainstem response in postmenopausal women treated with hormone replacement therapy: A pilot study. Menopause 7: 178-183. (Pubitemid 30249899)
68. Khaliq F, Tandon OP, Goel N (2003) Auditory evoked responses in postmenopausal women on hormone replacement therapy. Indian J Physiol Pharmacol 47: 393-399. (Pubitemid 37151177)
69. Hunter KP, Willott JF (1987) Aging and the auditory brainstem response in mice with severe or minimal presbycusis. Hear Res 30: 207-218. (Pubitemid 18013420)
70. Guimaraes P, Frisina ST, Mapes F, Tadros SF, Frisina DR, et al. (2006) Progestin negatively affects hearing in aged women. Proc Natl Acad Sci U S A 103: 14246-14249. (Pubitemid 44453011)
71. Koenig H, Schumacher M, Ferzaz B, Thi A, Ressouches A, et al. (1995) Progesterone synthesis and myelin formation by Schwann cells. Science 268: 1500-1503.
72. Zhou R, Abbas PJ, Assouline JG (1995) Electrically evoked auditory brainstem response in peripherally myelin-deficient mice. Hear Res 88: 98-106.
73. Gregg C, Shikar V, Larsen P, Mak G, Chojnacki A, et al. (2007) White matter plasticity and enhanced remyelination in the maternal CNS. J Neurosci 27: 1812-1823.
74. Ehret G, Riecke S (2002) Mice and humans perceive multiharmonic communication sounds in the same way. Proc Natl Acad Sci U S A 99: 479-482. (Pubitemid 34060386)
75. Scattoni ML, Gandhy SU, Ricceri L, Crawley JN (2008) Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PloS One 3: e3067.
76. Allen PD, Ison JR (2010) Sensitivity of the mouse to changes in azimuthal sound location: angular separation, spectral composition, and sound level. Behav Neurosci 124: 265-277.
77. Frisina RD (2001) Subcortical neural coding mechanisms for auditory temporal processing. Hear Res 158: 1-27.
78. Oertel D (1999) The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61: 497-519.
79. Ehret G (1992) Categorical perception of mouse-pup ultrasounds in the temporal domain. Anim Behav 43: 409-416.
80. Ehret G, Haack B (1982) Ultrasound recognition in house mice: Key-Stimulus configuration and recognition mechanism J Comp Physiol 148: 245-251.
81. Geissler DB, Ehret G (2002) Time-critical integration of formants for perception of communication calls in mice. Proc Natl Acad Sci U S A 99: 9021-9025. (Pubitemid 34693676)
82. Keuroghlian AS, Knudsen EI (2007) Adaptive auditory plasticity in developing and adult animals. Prog Neurobiol 82: 109-121. (Pubitemid 46829606)
83. Shepard KN, Liu RC (2011) Experience restores innate female preference for male ultrasonic vocalizations. Genes Brain Behav 10: 28-34.
84. Ji WQ, Suga N (2007) Serotonergic modulation of plasticity of the auditory cortex elicited by fear conditioning. J Neurosci 27: 4910-4918.
85. Miasnikov AA, Chen JC, Weinberger NM (2008) Specific auditory memory induced by nucleus basalis stimulation depends on intrinsic acetylcholine. Neurobiol Learn Mem 90: 443-454.
86. Mehta MR, Quirk MC, Wilson MA (2000) Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25: 707-715.
87. Yan J, Ehret G (2002) Corticofugal modulation of midbrain sound processing in the house mouse. Eur J Neurosci 16: 119-128. (Pubitemid 35463602)
88. Yan J, Ehret G (2001) Corticofugal reorganization of the midbrain tonotopic map in mice. Neuroreport 12: 3313-3316. (Pubitemid 33010663)
89. Suga N, Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4: 783-794. (Pubitemid 37314401)
90. Newman JD (2007) Neural circuits underlying crying and cry responding in mammals. Behav Brain Res 182: 155-165.
91. Swain JE, Tasgin E, Mayes LC, Feldman R, Constable RT, et al. (2008) Maternal brain response to own baby-cry is affected by cesarean section delivery. J Child Psychol and Psychiatry 49: 1042-1052.
92. Banerjee SB, Liu RC (2013) Storing maternal memories: hypothesizing an interaction of experience and estrogen on sensory cortical plasticity to learn infant cues. Front Neuroendocrinol 34: 300-314.