Hearing loss differentially affects thalamic drive to two cortical interneuron subtypes

Journal of Neurophysiology

Volumn 110, Issue 4, 2013, Pages 999-1008

  Takesian, Anne E ^a   Kotak, Vibhakar C ^a   Sharma, Neeti ^a   Sanes, Dan H ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Auditory cortex; Development; Fast spiking interneuron; Low threshold spiking interneuron; Sensorineural hearing loss

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY CORTEX; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CELL TYPE; CONTROLLED STUDY; CORTICAL INHIBITORY INTERNEURON; DEPRESSION; EXCITATORY POSTSYNAPTIC POTENTIAL; HEARING IMPAIRMENT; INTERNEURON; MEDIAL GENICULATE BODY; NONHUMAN; PERCEPTION DEAFNESS; PREDICTION; PRIORITY JOURNAL; SPIKE; SYNAPSE; THALAMUS; WHOLE CELL;

EID: 84881648408     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00182.2013     Document Type: Article

References (93)

1. Adesnik H, Bruns W, Taniguchi H, Huang ZJ, Scanziani M. A neural circuit for spatial summation in visual cortex. Nature 490: 226-231, 2012.
2. Agmon A, Connors BW. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci 12: 319-329, 1992.
3. Ahuja TK, Wu SH. Developmental changes in physiological properties in the rat's dorsal nucleus of the lateral lemniscus. Hear Res 149: 33-45, 2000.
4. Bartley AF, Huang ZJ, Huber KM, Gibson JR. Differential activitydependent, homeostatic plasticity of two neocortical inhibitory circuits. J Neurophysiol 100: 1983-1994, 2008.
5. Beierlein M, Connors BW. Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. J Neurophysiol 88: 1924-1932, 2002.
6. Beierlein M, Gibson JR, Connors BW. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3: 904-910, 2000.
7. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003.
8. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667, 2009.
9. Chattopadyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang J. Experience and activity-dependent maturation of perisomatic GABAergic innvervation in primary visual cortex during a postnatal critical period. J Neurosci 24: 9598-9611, 2004.
10. Chittajallu R, Isaac JT. Emergence of cortical inhibition by coordinated sensory-driven plasticity at distinct synaptic loci. Nat Neurosci 13: 1240-1248, 2010.
11. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 365-366, 1990.
12. Cook RD, Hung TY, Miller RL, Smith DW, Tucci DL. Effects of conductive hearing loss on auditory nerve activity in gerbil. Hear Res 164: 127-137, 2002.
13. Cruikshank SJ, Lewis TJ, Connors BW. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10: 462-468, 2007.
14. Cruikshank SJ, Rose HJ, Metherate R. Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol 87: 361-384, 2002.
15. Cruikshank SJ, Urabe H, Nurmikko AV, Connors BW. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65: 230-245, 2010.
16. de la Rocha J, Marchetti C, Schiff M, Reyes A. Linking the response properties of cells in auditory cortex with network architecture: co-tuning vs. lateral inhibition. J Neurosci 28: 9151-9163, 2008.
17. Dorrn AL, Yuan K, Barker AJ, Schreiner CE, Froemke RC. Developmental sensory experience balances cortical excitation and inhibition. Nature 465: 932-936, 2010.
18. Francis HW, Manis PB. Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons. Hear Res 149: 91-105, 2000.
19. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48: 165-166, 2005.
20. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H. Relative abundance of subunit mRNAs determines gating and Ca2 permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15: 193-204, 1995.
21. Gentet LJ, Kremer Y, Taniguchi H, Huang ZJ, Staiger JF, Petersen CC. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci 15: 607-612, 2012.
22. Gentschev T, Sotelo C. Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultra-structural study. Brain Res 62: 37-60, 1973.
23. Gianfranceschi L, Siciliano R, Walls J, Morales B, Kirkwood A, Huang ZJ, Tonegawa S, Maffei L. Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc Natl Acad Sci USA 100: 12486-12491, 2003.
24. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79, 1999.
25. Goldberg EM, Clark BD, Zagha E, Nahmani M, Erisir A, Rudy B. K channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58: 387-400, 2008.
26. Gupta A, Wang Y, Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273-278, 2000.
27. Harrison RV, Negandhi J. Resting neural activity patterns in auditory brainstem and midbrain in conductive hearing loss. Acta Otolaryngol 132: 409-414, 2012.
28. Hayut I, Fanselow EE, Connors BW, Golomb D. LTS and FS inhibitory interneurons, short-term synaptic plasticity, and cortical circuit dynamics. PLoS Comput Biol 7: e1002248, 2011.
29. Hensch TK. Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6: 877-888, 2005.
30. Hull C, Isaacson JS, Scanziani M. Postsynaptic mechanisms govern the differential excitation of cortical neurons by thalamic inputs. J Neurosci 29: 9127-9136, 2009.
31. Itami C, Kimura F, Nakamura S. Brain-derived neurotrophic factor regulates the maturation of layer 4 fast-spiking cells after the second postnatal week in the barrel cortex. J Neurosci 27: 2241-2252, 2007.
32. Jiao Y, Zhang C, Yanagawa Y, Sun QQ. Major effects of sensory experience on the neocortical inhibitory circuits. J Neurosci 26: 8691-8701, 2006.
33. Kandler K, Friauf E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15: 6890-6904, 1995.
34. Katagiri H, Fagiolini M, Hensch TK. Optimization of somatic inhibition at critical period onset in mouse visual cortex. Neuron 53: 805-812, 2007.
35. Kotak VC, Fujisawa S, Lee FA, Karthikeyan O, Aoki C, Sanes DH. Hearing loss raises excitability in the auditory cortex. J Neurosci 25: 3908-3918, 2005.
36. Kotak VC, Takesian AE, Sanes DH. Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex. Cereb Cortex 18: 2098-2108, 2008.
37. Kral A, Sharma A. Developmental neuroplasticity after cochlear implantation. Trends Neurosci 35: 111-122, 2012.
38. Kral A, Tillein J, Heid S, Hartmann R, Klinke R. Postnatal cortical development in congenital auditory deprivation. Cereb Cortex 15: 552-562, 2005.
39. Kral A, Tillein J, Heid S, Klinke R, Hartmann R. Cochlear implants: cortical plasticity in congenital deprivation. Prog Brain Res 157: 283-313, 2006.
40. Lazarus MS, Huang ZJ. Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period of ocular dominance. J Neurophysiol 106: 775-787, 2011.
41. Le Magueresse C, Monyer H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 77: 388-405, 2013.
42. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, Herry C, Lüthi A. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480: 331-335, 2011.
43. Li YT, Ma WP, Li LY, Ibrahim LA, Wang SZ, Tao HW. Broadening of inhibitory tuning underlies contrast-dependent sharpening of orientation selectivity in mouse visual cortex. J Neurosci 32: 16466-16477, 2012.
44. Lippe WR. Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14: 1486-1495, 1994.
45. Long MA, Cruikshank SJ, Jutras MJ, Connors BW. Abrupt maturation of a spike-synchronizing mechanism in neocortex. J Neurosci 25: 7309-7316, 2005.
46. Lu Y, Monsivais P, Tempel BL, Rubel EW. Activity-dependent regulation of the potassium channel subunits Kv1.1 and Kv3.1. J Comp Neurol 470: 93-106, 2004.
47. Maffei A, Lambo ME, Turrigiano GG. Critical period for inhibitory plasticity in rodent binocular V1. J Neurosci 30: 3304-3309, 2010.
48. Maffei A, Nelson SB, Turrigiano GG. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7: 1353-1359, 2004.
49. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004.
50. Metherate R, Aramakis VB. Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. Brain Res Dev Brain Res 115: 131-144, 1999.
51. Morales B, Choi YK. Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 22: 8084-8090, 2002.
52. Oates PA, Kurtzberg D, Stapells DR. Effects of sensorineural hearing loss on cortical event-related potential and behavioral measures of speech-sound processing. Ear Hear 23: 399-415, 2002.
53. Ojima H, Murakami K. Intracellular characterization of suppressive responses in supragranular pyramidal neurons of cat primary auditory cortex in vivo. Cereb Cortex 12: 1079-1091, 2002.
54. Okaty BW, Miller MN, Sugino K, Hempel CM, Nelson SB. Transcriptional and electrophysiological maturation of neorcortical fast-spiking GABAergic interneurons. J Neurosci 29: 7040-7052, 2009.
55. Oswald AM, Reyes AD. Development of inhibitory timescales in auditory cortex. Cereb Cortex 21: 1351-1361, 2011.
56. Oswald AM, Reyes AD. Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. J Neurophysiol 99: 2998-3008, 2008.
57. Oswald AM, Schiff ML, Reyes AD. Synaptic mechanisms underlying auditory processing. Curr Opin Neurobiol 16: 371-376, 2006.
58. Razak KA, Fuzessery ZM. Development of inhibitory mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex. J Neurosci 27: 1769-1781, 2007.
59. Razak KA, Fuzessery ZM. Facilitatory mechanisms underlying selectivity for the direction and rate of frequency modulated sweeps in the auditory cortex. J Neurosci 28: 9806-9816, 2008.
60. Razak KA, Fuzessery ZM. Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat. J Neurophysiol 96: 1303-1319, 2006.
61. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285, 1998.
62. Rose HJ, Metherate R. Auditory thalamocortical transmission is reliable and temporally precise. J Neurophysiol 94: 2019-2030, 2005.
63. Sanes DH. The development of synaptic function and integration in the central auditory system. J Neurosci 94: 2019-2030, 1993.
64. Sanes DH, Woolley SM. A behavioral framework to guide research on central auditory development and plasticity. Neuron 72: 912-929, 2011.
65. Sharma A, Gilley PM, Dorman MF, Baldwin R. Deprivation-induced reorganization in children with cochlear implants. Int J Audiol 46: 494-499, 2007.
66. Sharma A, Martin K, Roland P, Bauer P, Sweeney MH, Gilley P, Dorman M. P1 latency as a biomarker for central auditory development in children with hearing impairment. J Am Acad Audiol 16: 564-573, 2005.
67. Sun HY, Dobrunz LE. Presynaptic kainate receptor activation is a novel mechanism for target cell-specific short-term facilitation at Schaffer collateral synapses. J Neurosci 26: 10796-10807, 2006.
68. Sun QQ. Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV. J Neurophysiol 102: 2955-2973, 2009.
69. Sun YJ, Wu GK, Liu B, Li P, Zhou M, Xiao Z, Tao HW, Zhang LI. Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature 465: 927-931, 2010.
70. Swadlow HA. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13: 25-32, 2003.
71. Swanson GT, Kamboj SK, Cull-Candy SG. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17: 58-69, 1997.
72. Takesian AE, Kotak VC, Sanes DH. Age-dependent effect of hearing loss on cortical inhibitory synapse function. J Neurophysiol 107: 937-947, 2012.
73. Takesian AE, Kotak VC, Sanes DH. Developmental hearing loss disrupts synaptic inhibition: implications for auditory processing. Future Neurol 4: 331-349, 2009.
74. Takesian AE, Kotak VC, Sanes DH. Presynaptic GABAB receptors regulate experience-dependent development of inhibitory short-term plasticity. J Neurosci 30: 2716-2727, 2010.
75. Tan AY, Atencio CA, Polley DB, Merzenich MM, Schreiner CE. Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons. Neuroscience 146: 449-462, 2007.
76. Tan Z, Hang Hu Huang J, Agmon A. Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc Natl Acad Sci USA 105: 2187-2192, 2008.
77. Thomson AM. Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J Physiol 502: 131-147, 1997.
78. Tierney TS, Russell FA, Moore DR. Susceptibility of developing cochlear nucleus neurons to deafferentation-induced death abruptly ends just before the onset of hearing. J Comp Neurol 378: 295-306, 1997.
79. Tritsch NX, Rodríguez-Contreras A, Crins TT, Wang HC, Borst JG, Bergles DE. Calcium action potentials in hair cells pattern auditory neuron activity before hearing onset. Nat Neurosci 13: 1050-1052, 2010.
80. Tucci DL, Cant NB, Durham D. Effects of conductive hearing loss on gerbil central auditory system activity in silence. Hear Res 155: 124-132, 2001.
81. Turrigiano G. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb Perspect Biol 4: a005736, 2012.
82. Vale C, Sanes DH. Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain. J Neurosci 20: 1912-1921, 2000.
83. Vale C, Sanes DH. The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus. Eur J Neurosci 16: 2394-2404, 2002.
84. Wang Y, Manis PB. Temporal coding by cochlear nucleus bushy cells in DBA/2J mice with early onset hearing loss. J Assoc Res Otolaryngol 7: 412-424, 2006.
85. Wenner P. Mechanisms of GABAergic homeostatic plasticity. Neural Plast 2011: 489470, 2011.
86. Wilent WB, Contreras D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8: 1364-1370, 2005.
87. Wilson NR, Runyan CA, Wang FL, Sur M. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488: 343-348, 2012.
88. Wu GK, Li P, Tao HW, Zhang LI. Nonmonotonic synaptic excitation and imbalanced inhibition underlying cortical intensity tuning. Neuron 52: 705-715, 2006.
89. Wu SH, Oertel D. Maturation of synapses and electrical properties of cells in the cochlear nuclei. J Neurosci 23: 4868-4877, 1987.
90. Xiang Z, Huguenard JR, Prince DA. Cholinergic switching within neocortical inhibitory networks. Science 281: 985-988, 1998.
91. Xu H, Jeong HY, Tremblay R, Rudy B. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77: 155-167, 2013.
92. Xu H, Kotak VC, Sanes DH. Conductive hearing loss disrupts synaptic and spike adaptation in developing auditory cortex. J Neurosci 27: 9417-9426, 2007.
93. Zhang LI, Tan AY, Schreiner CE, Merzenich MM. Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424: 201-205, 2003.