GABAergic inhibition controls neural gain in inferior colliculus neurons sensitive to interaural time differences

Journal of Neuroscience

Volumn 25, Issue 26, 2005, Pages 6187-6198

  Ingham, Neil J ^a,b   McAlpine, David ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b PHYSIOLOGICAL LABORATORY   (United Kingdom)

Author keywords

GABAergic; Gain control; Inferior colliculus; Inhibition; Interaural time differences; Iontophoresis

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; ATROPINE; BICUCULLINE; HYPNORM;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; CONTROLLED STUDY; EVOKED RESPONSE; GUINEA PIG; INFERIOR COLLICULUS; INTERAURAL TIME DISCRIMINATION; IONTOPHORESIS; MEASUREMENT; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SIGNAL DETECTION; SOUND DETECTION;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PERCEPTION; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; INFERIOR COLLICULUS; NEURONS; TIME PERCEPTION;

EID: 21544467271     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0146-05.2005     Document Type: Article

References (51)

1. Adams JC (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183:519-538.
2. Adams JC (1980) Crossed and descending projections to the inferior colliculus. Neurosci Lett 19:1-5.
3. Adams JC, Mugnaini E (1984) Dorsal nucleus of the lateral lemniscus: a nucleus of GABAergic projection neurons. Brain Res Bull 13:585-590.
4. Aitkin LM, Anderson DJ, Brugge JF (1970) Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. J Neurophysiol 33:421-440.
5. Andersen RA, Roth GL, Aitkin LM, Merzenich MM (1980) The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat. J Comp Neurol 194:649-662.
6. Beyerl BD (1978) Afferent projections to the central nucleus of the inferior colliculus in the rat. Brain Res 145:209-223.
7. A receptors. J Physiol (Lond) 497:753-759.
8. Brugge JF, Anderson DJ, Aitkin LM (1970) Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. J Neurophysiol 33:441-458.
9. Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197:705-722.
10. Burger RM, Pollak GD (1998) Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus. J Neurophysiol 80:1686-1701.
11. Burger RM, Pollak GD (2001) Reversible inactivation of the dorsal nucleus of the lateral lemniscus reveals its role in the processing of multiple sound sources in the inferior colliculus of bats. J Neurosci 21:4830-4843.
12. Caspary DM, Milbrandt JC, Helfert RH (1995) Central auditory aging: GABA changes in the inferior colliculus. Exp Gerontol 30:349-360.
13. 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.
14. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773-782.
15. Fitzpatrick DC, Batra R, Stanford TR, Kuwada S (1997) A neuronal population code for sound localization. Nature 388:871-874.
16. Friauf E, Kandler K (1990) Auditory projections to the inferior colliculus of the rat are present by birth. Neurosci Lett 120:58-61.
17. Fujita I, Konishi M (1991) The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system. J Neurosci 11:722-739.
18. Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613-636.
19. Gonzalez-Hernandez T, Mantolan-Sarmiento B, Gonzalez-Gonzalez B, Perez-Gonzalez H (1996) Sources of GABAergic input to the inferior colliculus of the rat. J Comp Neurol 372:309-326.
20. Green DM, Swets JA (1966) Signal detection theory and psychophysics. New York: Wiley.
21. Holt GR, Koch C (1997) Shunting inhibition does not have a divisive effect on firing rates. Neural Comput 9:1001-1013.
22. Ingham NJ, McAlpine D (2004) Spike-frequency adaptation in the inferior colliculus. J Neurophysiol 91:632-645.
23. Irvine DRF (1992) Physiology of auditory brainstem pathways. In: Springer handbook of auditory research, Vol 2, The mammalian auditory pathway: neurophysiology (Fay RR, Popper AA, eds), pp 153-231. New York: Springer.
24. Kuwada S, Batra R, Fitzpatrick DC (1997) Neural processing of binaural temporal cues. In: Binaural and spatial hearing in real and virtual environments (Gilkey RH, Anderson TR, eds), pp 399-425. Maywah, NJ: Lawrence Erlbaum Associates.
25. 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.
26. A and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21:7303-7312.
27. McAlpine D, Palmer AR (2002) Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J Neurosci 22:1443-1453.
28. McAlpine D, Jiang D, Shackleton TM, Palmer AR (2000) Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation. J Neurophysiol 83:1356-1365.
29. McAlpine D, Jiang D, Palmer AR (2001) A neural code for low-frequency sound localization in mammals. Nat Neurosci 4:396-401.
30. Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433-445.
31. Ohzawa I, Sclar G, Freeman RD (1982) Contrast gain control in the cat visual cortex. Nature 298:266-268.
32. Ohzawa I, Sclar G, Freeman RD (1985) Contrast gain control in the cat's visual system. J Neurophysiol 54:651-667.
33. Oliver DL (1987) Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction. J Comp Neurol 264:24-46.
34. Oliver DL, Beckius GE (1992) Fine structure of GABA-labeled axonal endings in the inferior colliculus of the cat: immunocytochemistry on deplasticized ultrathin sections. Neuroscience 46:455-463.
35. Oliver DL, Winer JA, Beckius GE, Saint Marie RL (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J Comp Neurol 340:27-42.
36. Oliver DL, Beckius GE, Shneiderman A (1995) Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: a study using electron microscopic autoradiography. J Comp Neurol 360:17-32.
37. Oliver DL, Beckius GE, Bishop DC, Loftus WC, Batra R (2003) Topography of interaural temporal disparity coding in projections of medial superior olive to inferior colliculus. J Neurosci 23:7438-7449.
38. Pena JL, Konishi M (2001) Auditory spatial receptive fields created by multiplication. Science 292:249-252.
39. Pena JL, Konishi M (2002) From postsynaptic potentials to spikes in the genesis of auditory spatial receptive fields. J Neurosci 22:5652-5658.
40. Pollak GD, Park TJ (1993) The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus. Hear Res 65:99-117.
41. Sanes DH, Malone BJ, Semple MN (1998) Role of synaptic inhibition in processing of dynamic binaural level stimuli. J Neurosci 18:794-803.
42. Shackleton TM, Skottun BC, Arnott RH, Palmer AR (2003) Interaural time difference discrimination thresholds for single neurons in the inferior colliculus of guinea pigs. J Neurosci 15:716-724.
43. Spitzer MW, Semple MN (1991) Interaural phase coding in auditory midbrain: influence of dynamic stimulus features. Science 254:721-724.
44. Spitzer MW, Semple MN (1995) Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties. J Neurophysiol 73:1668-1690.
45. Spitzer MW, Semple MN (1998) Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity. J Neurophysiol 80:3062-3076.
46. Sterbing SJ, D'Angelo WR, Ostapoff EM, Kuwada S (2005) The role of GABA-ergic inhibition in the coding of interaural time differences of low-frequency sounds in the inferior colliculus. J Neurophysiol 93:3390-3400.
47. Takahashi TT, Konishi M (1988) Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl. J Comp Neurol 274:190-211.
48. Winer JA, Chernock ML, Larue DT, Cheung SW (2002) Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey. Hear Res 168:181-195.
49. Yin TC, Kuwada S (1983) Binaural interaction in low-frequency neurons in inferior colliculus of the cat. II. Effects of changing rate and direction of interaural phase. J Neurophysiol 50:1000-1019.
50. Yin TC, Chan JC, Carney LH (1987) Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. III. Evidence for cross-correlation. J Neurophysiol 58:562-583.
51. Zhang DX, Li L, Kelly JB, Wu SH (1998) GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat. Hear Res 117:1-12.