GABA A-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Pérez González, David ^a   Hernández, Olga ^a,b   Covey, Ellen ^a,c   Malmierca, Manuel S ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; TUNGSTEN; 4 AMINOBUTYRIC ACID; PYRIDAZINE DERIVATIVE;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRODE; INFERIOR COLLICULUS; LATENT PERIOD; MESENCEPHALON; MICROIONTOPHORESIS; NERVE STIMULATION; NONHUMAN; PIPETTE; PROBABILITY; RAT; RECEPTOR BLOCKING; SINGLE UNIT ACTIVITY; SPIKE WAVE; STIMULUS SPECIFIC ADAPTATION; SYNAPTIC INHIBITION; ACOUSTICS; ANIMAL; AUDITORY STIMULATION; BIOLOGICAL MODEL; DRUG EFFECT; ELECTROPHYSIOLOGY; METABOLISM; METHODOLOGY; NERVE CELL; PHYSIOLOGY; TIME;

ACOUSTIC STIMULATION; ACOUSTICS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ELECTROPHYSIOLOGY; GAMMA-AMINOBUTYRIC ACID; INFERIOR COLLICULI; MESENCEPHALON; MODELS, NEUROLOGICAL; NEURONS; PROBABILITY; PYRIDAZINES; RATS; RECEPTORS, GABA-A; TIME FACTORS;

EID: 84859063285     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034297     Document Type: Article

References (80)

1. Best AR, Wilson DA, (2004) Coordinate synaptic mechanisms contributing to olfactory cortical adaptation. J Neurosci 24: 652-660.
2. Carandini M, (2000) Visual cortex: Fatigue and adaptation. Curr Biol 10: R605-607.
3. Chung S, Li X, Nelson SB, (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34: 437-446.
4. Kohn A, (2007) Visual adaptation: physiology, mechanisms, and functional benefits. J Neurophysiol 97: 3155-3164.
5. Antunes FM, Nelken I, Covey E, Malmierca MS, (2010) Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS One 5: e14071.
6. Malmierca MS, Cristaudo S, Pérez-González D, Covey E, (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29: 5483-5493.
7. Pérez-González D, Malmierca MS, Covey E, (2005) Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22: 2879-2885.
8. Ulanovsky N, Las L, Nelken I, (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6: 391-398.
9. Yu XJ, Xu XX, He S, He J, (2009) Change detection by thalamic reticular neurons. Nat Neurosci 12: 1165-1170.
10. Nelken I, Ulanovsky N, (2007) Mismatch Negativity and Stimulus-Specific Adaptation in Animal Models. Journal of Psychophysiology 21: 214-223.
11. Jääskeläinen IP, Ahveninen J, Belliveau JW, Raij T, Sams M, (2007) Short-term plasticity in auditory cognition. Trends Neurosci 30: 653-661.
12. Reches A, Gutfreund Y, (2008) Stimulus-specific adaptations in the gaze control system of the barn owl. J Neurosci 28: 1523-1533.
13. Winkler I, Denham SL, Nelken I, (2009) Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cogn Sci 13: 532-540.
14. Fritz JB, Elhilali M, David SV, Shamma SA, (2007) Auditory attention-focusing the searchlight on sound. Curr Opin Neurobiol 17: 437-455.
15. Escera C, Alho K, Winkler I, Näätänen R, (1998) Neural mechanisms of involuntary attention to acoustic novelty and change. J Cogn Neurosci 10: 590-604.
16. Jääskeläinen IP, Ahveninen J, Bonmassar G, Dale AM, Ilmoniemi RJ, et al. (2004) Human posterior auditory cortex gates novel sounds to consciousness. Proc Natl Acad Sci U S A 101: 6809-6814.
17. Slabu L, Escera C, Grimm S, Costa-Faidella J, (2010) Early change detection in humans as revealed by auditory brainstem and middle-latency evoked potentials. Eur J Neurosci 32: 859-865.
18. Grimm S, Escera C, Slabu L, Costa-Faidella J, (2011) Electrophysiological evidence for the hierarchical organization of auditory change detection in the human brain. Psychophysiology 48: 377-384.
19. Anderson LA, Christianson GB, Linden JF, (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29: 7359-7363.
20. Zhao L, Liu Y, Shen L, Feng L, Hong B, (2011) Stimulus-specific adaptation and its dynamics in the inferior colliculus of rat. Neuroscience 181: 163-174.
21. Nelken I, (2004) Processing of complex stimuli and natural scenes in the auditory cortex. Curr Opin Neurobiol 14: 474-480.
22. Szymanski FD, Garcia-Lazaro JA, Schnupp JW, (2009) Current source density profiles of stimulus-specific adaptation in rat auditory cortex. J Neurophysiol 102: 1483-1490.
23. Oliver DL, Shneiderman A, (1991) The anatomy of the inferior colliculus. A cellular basis for integration of monaural and binaural information. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffmann DW, editors. Neurobiology of hearing New York Raven Press pp. 195-222.
24. Palombi PS, Caspary DM, (1996) GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons. J Neurophysiol 75: 2211-2219.
25. Ingham NJ, McAlpine D, (2005) GABAergic inhibition controls neural gain in inferior colliculus neurons sensitive to interaural time differences. J Neurosci 25: 6187-6198.
26. Koch U, Grothe B, (1998) GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol 80: 71-82.
27. LeBeau FE, Rees A, Malmierca MS, (1996) Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. J Neurophysiol 75: 902-919.
28. LeBeau FE, Malmierca MS, Rees A, (2001) Iontophoresis in vivo demonstrates a key role for GABAA and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21: 7303-7312.
29. Sivaramakrishnan S, Sterbing-D'Angelo SJ, Filipovic B, D'Angelo WR, Oliver DL, et al. (2004) GABA(A) synapses shape neuronal responses to sound intensity in the inferior colliculus. J Neurosci 24: 5031-5043.
30. Wu SH, Ma CL, Kelly JB, (2004) Contribution of AMPA, NMDA, and GABA(A) receptors to temporal pattern of postsynaptic responses in the inferior colliculus of the rat. J Neurosci 24: 4625-4634.
31. Casseday JH, Ehrlich D, Covey E, (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264: 847-850.
32. Casseday JH, Ehrlich D, Covey E, (2000) Neural measurement of sound duration: control by excitatory-inhibitory interactions in the inferior colliculus. J Neurophysiol 84: 1475-1487.
33. Covey E, Kauer JA, Casseday JH, (1996) Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J Neurosci 16: 3009-3018.
34. Kuwada S, Batra R, Yin TC, Oliver DL, Haberly LB, et al. (1997) Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci 17: 7565-7581.
35. Kelly JB, Caspary DM, (2005) Pharmacology of the inferior colliculus. In: A. WJ, Schreiner CE, editors. The inferior colliculus New York Springer.
36. Yang L, Pollak GD, Resler C, (1992) GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol 68: 1760-1774.
37. Caspary DM, Palombi PS, Hughes LF, (2002) GABAergic inputs shape responses to amplitude modulated stimuli in the inferior colliculus. Hear Res 168: 163-173.
38. Pollak GD, Burger RM, Park TJ, Klug A, Bauer EE, (2002) Roles of inhibition for transforming binaural properties in the brainstem auditory system. Hear Res 168: 60-78.
39. Rose D, Blakemore C, (1974) Effects of bicuculline on functions of inhibition in visual cortex. Nature 249: 375-377.
40. Isaacson JS, Scanziani M, (2011) How inhibition shapes cortical activity. Neuron 72: 231-243.
41. Katzner S, Busse L, Carandini M, (2011) GABAA inhibition controls response gain in visual cortex. J Neurosci 31: 5931-5941.
42. Yin S, Chen Z, Yu D, Feng Y, Wang J, (2008) Local inhibition shapes duration tuning in the inferior colliculus of guinea pigs. Hearing Research 237: 32-48.
43. Fuzessery ZM, Wenstrup JJ, Hall JC, Leroy S, (2003) Inhibition has little effect on response latencies in the inferior colliculus. J Assoc Res Otolaryngol 4: 60-73.
44. Hernández O, Espinosa N, Pérez-González D, Malmierca MS, (2005) The inferior colliculus of the rat: A quantitative analysis of monaural frequency response areas. Neuroscience 132: 203-217.
45. Candy JM, Boakes RJ, Key BJ, Worton E, (1974) Correlation of the release of amines and antagonists with their effects. Neuropharmacology 13: 423-430.
46. Malmierca MS, Blackstad TW, Osen KK, Karagulle T, Molowny RL, (1993) The central nucleus of the inferior colliculus in rat: a Golgi and computer reconstruction study of neuronal and laminar structure. J Comp Neurol 333: 1-27.
47. Malmierca MS, Seip KL, Osen KK, (1995) Morphological classification and identification of neurons in the inferior colliculus: a multivariate analysis. Anat Embryol (Berl) 191: 343-350.
48. Malmierca MS, Blackstad TW, Osen KK, (2011) Computer-assisted 3-D reconstructions of Golgi-impregnated neurons in the cortical regions of the inferior colliculus of rat. Hear Res 274: 13-26.
49. Malmierca MS, (2003) The structure and physiology of the rat auditory system: an overview. Int Rev Neurobiol 56: 147-211.
50. Malmierca MS, Hackett A, (2010) Structural organization of the ascending auditory pathway. In: Rees A, Palmer A, editors. The Auditory Brain Oxford Oxford University Press.
51. Hernández O, Rees A, Malmierca MS, (2006) A GABAergic component in the commissure of the inferior colliculus in rat. Neuroreport 17: 1611-1614.
52. Merchán M, Aguilar LA, Lopez-Poveda EA, Malmierca MS, (2005) The inferior colliculus of the rat: quantitative immunocytochemical study of GABA and glycine. Neuroscience 136: 907-925.
53. Reetz G, Ehret G, (1999) Inputs from three brainstem sources to identified neurons of the mouse inferior colliculus slice. Brain Res 816: 527-543.
54. Sun H, Wu SH, (2009) The physiological role of pre- and postsynaptic GABA(B) receptors in membrane excitability and synaptic transmission of neurons in the rat's dorsal cortex of the inferior colliculus. Neuroscience 160: 198-211.
55. Binns KE, Salt TE, (1997) Different roles for GABAA and GABAB receptors in visual processing in the rat superior colliculus. J Physiol 504 (Pt 3): 629-639.
56. Binns KE, Salt TE, (1995) Excitatory amino acid receptors modulate habituation of the response to visual stimulation in the cat superior colliculus. Vis Neurosci 12: 563-571.
57. Abbott LF, Varela JA, Sen K, Nelson SB, (1997) Synaptic depression and cortical gain control. Science 275: 220-224.
58. Tsodyks MV, Markram H, (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94: 719-723.
59. Wehr M, Zador AM, (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47: 437-445.
60. Zhang LI, Tan AY, Schreiner CE, Merzenich MM, (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424: 201-205.
61. Wehr M, Zador AM, (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442-446.
62. Eytan D, Brenner N, Marom S, (2003) Selective adaptation in networks of cortical neurons. J Neurosci 23: 9349-9356.
63. Mill R, Coath M, Wennekers T, Denham SL, (2011) Abstract stimulus-specific adaptation models. Neural Comput 23: 435-476.
64. Garagnani M, Pulvermuller F, (2011) From sounds to words: a neurocomputational model of adaptation, inhibition and memory processes in auditory change detection. Neuroimage 54: 170-181.
65. Hara K, Harris RA, (2002) The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg 94: 313-318.
66. Malmierca MS, Hernández O, Falconi A, Lopez-Poveda EA, Merchán M, et al. (2003) The commissure of the inferior colliculus shapes frequency response areas in rat: an in vivo study using reversible blockade with microinjection of kynurenic acid. Exp Brain Res 153: 522-529.
67. Malmierca MS, Saint Marie RL, Merchán MA, Oliver DL, (2005) Laminar inputs from dorsal cochlear nucleus and ventral cochlear nucleus to the central nucleus of the inferior colliculus: two patterns of convergence. Neuroscience 136: 883-894.
68. Malmierca MS, Hernández O, Rees A, (2005) Intercollicular commissural projections modulate neuronal responses in the inferior colliculus. Eur J Neurosci 21: 2701-2710.
69. Malmierca MS, Izquierdo MA, Cristaudo S, Hernández O, Pérez-González D, et al. (2008) A discontinuous tonotopic organization in the inferior colliculus of the rat. J Neurosci 28: 4767-4776.
70. Pérez-González D, Malmierca MS, Moore JM, Hernández O, Covey E, (2006) Duration selective neurons in the inferior colliculus of the rat: topographic distribution and relation of duration sensitivity to other response properties. J Neurophysiol 95: 823-836.
71. Merrill EG, Ainsworth A, (1972) Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng 10: 662-672.
72. Faure PA, Fremouw T, Casseday JH, Covey E, (2003) Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J Neurosci 23: 3052-3065.
73. Kurt S, Crook JM, Ohl FW, Scheich H, Schulze H, (2006) Differential effects of iontophoretic in vivo application of the GABAA-antagonists bicuculline and gabazine in sensory cortex. Hear Res 212: 224-235.
74. Razak KA, Fuzessery ZM, (2009) GABA shapes selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex. J Neurophysiol 102: 1366-1378.
75. Rees A, (1990) A closed field sound system for auditory neurophysiology. J Physiol Lond 430: 6.
76. Rees A, Sarbaz A, Malmierca MS, LeBeau FE, (1997) Regularity of firing of neurons in the inferior colliculus. J Neurophysiol 77: 2945-2965.
77. Näätänen R, (1992) Attention and brain function Hillsdale, NJ Erlbaum.
78. Ulanovsky N, Las L, Farkas D, Nelken I, (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24: 10440-10453.
79. Malmierca MS, Rees A, LeBeau FE, Bjaalie JG, (1995) Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357: 124-144.
80. Loftus WC, Malmierca MS, Bishop DC, Oliver DL, (2008) The cytoarchitecture of the inferior colliculus revisited: a common organization of the lateral cortex in rat and cat. Neuroscience 154: 196-205.