Wide-dynamic-range forward suppression in marmoset inferior colliculus neurons is generated centrally and accounts for perceptual masking

Journal of Neuroscience

Volumn 29, Issue 8, 2009, Pages 2553-2562

  Nelson, Paul C ^a,b   Smith, Zachary M ^a   Young, Eric D ^a  

^a Johns Hopkins University   (United States)

^b 505 Traylor Research Building ^*  (United States)

Author keywords

Adaptation; Context dependence; Inferior colliculus; Marmoset; Masking; Suppression

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY MASKING; AUDITORY THRESHOLD; COCHLEAR NERVE; CONTROLLED STUDY; HEARING; INFERIOR COLLICULUS; MARMOSET; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SOUND PRESSURE;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ADAPTATION, PSYCHOLOGICAL; ANIMALS; AUDITORY PATHWAYS; AUDITORY THRESHOLD; CALLITHRIX; INFERIOR COLLICULI; NEURAL INHIBITION; NEURONS; NONLINEAR DYNAMICS; PERCEPTUAL MASKING; PSYCHOACOUSTICS; REACTION TIME; TIME FACTORS; WAKEFULNESS;

EID: 61449122023     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5359-08.2009     Document Type: Article

References (58)

1. Aitkin LM, Webster WR, Veale JL, Crosby DC (1975) Inferior colliculus. I. Comparison of response properties of neurons in central, pericentral, and external nuclei of adult cat. J Neurophysiol 38:1196-1207.
2. Backoff PM, Palombi PS, Caspary DM (1997) Glycinergic and GABAergic inputs affect short-term suppression in the cochlear nucleus. Hear Res 110:155-163.
3. Bartlett EL, Wang X (2005) Long-lasting modulation by stimulus context in primate auditory cortex. J Neurophysiol 94:83-104.
4. Bartlett EL, Wang X (2007) Neural representations of temporally modulated signals in the auditory thalamus of awake primates. J Neurophysiol 97:1005-1017.
5. Bauer EE, Klug A, Pollak GD (2000) Features of contralaterally evoked inhibition in the inferior colliculus. Hear Res 141:80-96.
6. Bleeck S, Sayles M, Ingham NJ, Winter IM (2006) The time course of recovery from suppression and facilitation from single units in the mammalian cochlear nucleus. Hear Res 212:176-184.
7. Boettcher FA, Salvi RJ, Saunders SS (1990) Recoveryfrom short-term adaptation in single neurons in the cochlear nucleus. Hear Res 48:125-144.
8. Brosch M, Schreiner CE (1997) Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol 77:923-943.
9. Brosch M, Schulz A, Scheich H (1999) Processing of sound sequences in macaque auditory cortex: response enhancement. J Neurophysiol 82:1542-1559.
10. Calford MB, Semple MN (1995) Monaural inhibition in cat auditory cortex. J Neurophysiol 73:1876-1891.
11. 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.
12. Delgutte B (1980) Representation of speech-like sounds in the discharge patterns of auditory-nerve fibers. J Acoust Soc Am 68:843-857.
13. DiMattina C, Wang X (2006) Virtual vocalization stimuli for investigating neural representations of species-specific vocalizations. J Neurophysiol 95:1244-1262.
14. Faingold CL, Boersma Anderson CA, Caspary DM (1991) Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear Res 52:201-216.
15. 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.
16. Finlayson PG (1999) Post-stimulatory suppression, facilitation and tuning for delays shape responses of inferior colliculus neurons to sequential pure tones. Hear Res 131:177-194.
17. Finlayson PG, Adam TJ (1997) Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing. Hear Res 103:1-18.
18. Furukawa S, Maki K, Kashino M, Riquimaroux H (2005) Dependency of the interaural phase difference sensitivities ofinferior colliculus neurons on a preceding tone and its implications in neural population coding. J Neurophysiol 93:3313-3326.
19. Harris DM, Dallos P (1979) Forward masking of auditory nerve fiber responses. J Neurophysiol 42:1083-1107.
20. Ingham NJ, Hart HC, McAlpine D (2001) Spatial receptive fields of inferior colliculus neurons to auditory apparent motion in free field. J Neurophysiol 85:23-33.
21. Jesteadt W, Bacon SP, Lehman JR (1982) Forward masking as a function of frequency, masker level, and signal delay. J Acoust Soc Am 71:950-962.
22. Kelly JB, Liscum A, van Adel B, Ito M (1998) Projections from the superior olive and lateral lemniscus to tonotopic regions of the rat's inferior colliculus. Hear Res 116:43-54.
23. Kidd G Jr, Feth LL (1982) Effects of masker duration in pure-tone forward masking. J Acoust Soc Am 72:1384-1386.
24. Kulesza RJ Jr, Berrebi AS (2000) Superior paraolivary nucleus of the rat is a GABAergic nucleus. J Assoc Res Otolaryngol 1:255-269.
25. Kulesza RJ Jr, Spirou GA, Berebbi AS (2003) Physiological response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 89:2299-2312.
26. KuwadaS, BatraR (1999) Coding of sound envelopes byinhibitory rebound in neurons of the superior olivary complex in the unanesthetized rabbit. J Neurosci 19:2273-2287.
27. Kuwada S, Yin TCT, Haberly LB, Wickesburg RE (1980) Binaural interaction in the cat inferior colliculus: physiology and anatomy. In: Psycho-physical, physiological, and behavioral studies in hearing (van den Brink G, Bilsen FA, eds), pp 401-411. Delft, The Netherlands: Delft UP.
28. Kuwada S, Batra R, Yin TC, Oliver DL, Haberly LB, Stanford TR (1997) Intracellular recordings in response to monaural and binaural stimula tion of neurons in the inferior colliculus of the cat. J Neurosci 17:7565-7581.
29. A and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21:7303-7312.
30. Lu T, Liang L, Wang X (2001) Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates. J Neurophysiol 85:2364-2380.
31. Lüscher E, Zwislocki J (1949) Adaptation of the ear to sound stimuli. J Acoust Soc Am 21:135-139.
32. Malone BJ, Semple MN (2001) Effects of auditory stimulus context on the representation of frequency in the gerbil inferior colliculus. J Neurophysiol 86:1113-1130.
33. 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.
34. Moore BC, Glasberg BR (1983) Growth of forward masking for sinusoidal and noise maskers as a function of signal delay; implications for suppression in noise. J Acoust Soc Am 73:1249-1259.
35. Moore BC, Glasberg BR, Plack CJ, Biswas AK (1988) The shape of the ear's temporal window. J Acoust Soc Am 83:1102-1116.
36. Nakamoto KT, Zhang J, Kitzes LM (2006) Temporal nonlinearity during recovery from sequential inhibition by neurons in the cat primary auditory cortex. J Neurophysiol 95:1897-1907.
37. Nelson PG, Erulkar SD (1963) Synaptic mechanisms ofexcitation and inhibition in the central auditory pathway. J Neurophysiol 26:908-923.
38. Oliver DL (2004) Neuronal organization in the inferior colliculus. In: The inferior colliculus (Winer JA, Schreiner CE, eds), pp 69-114. New York: Springer.
39. Oxenham AJ (2001) Forward masking: adaptation or integration? J Acoust Soc Am 109:732-741.
40. Oxenham AJ, Plack CJ (2000) Effects of masker frequency and duration in forward masking: further evidence for the influence of peripheral nonlinearity. Hear Res 150:258-266.
41. Palombi PS, Backoff PM, Caspary DM (1994) Paired tone facilitation in dorsal cochlear nucleus neurons: a short-term potentiation model testable in vivo. Hear Res 75:175-183.
42. Pedemonte M, Torterolo P, Velluti RA (1997) In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs. Brain Res 759:24-31.
43. Plack CJ, Oxenham AJ (1998) Basilar-membrane nonlinearity and the growth of forward masking. J Acoust Soc Am 103:1598-1608.
44. 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.
45. Ramachandran R, Davis KA, May BJ (1999) Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J Neurophysiol 82:152-163.
46. Relkin EM, Doucet JR (1991) Recovery from prior stimulation. I: relationship to spontaneous firing rates of primary auditory neurons. Hear Res 55:215-222.
47. Relkin EM, Pelli DG (1987) Probe tone thresholds in the auditory nerve measured by two-interval forced-choice procedures. J Acoust Soc Am 82:1679-1691.
48. Relkin EM, Turner CW (1988) A reexamination of forward masking in the auditory nerve. J Acoust Soc Am 84:584-591.
49. Sanes DH, Malone BJ, Semple MN (1998) Role of synaptic inhibition in processing of dynamic binaural level stimuli. J Neurosci 18:794-803.
50. Scholl B, Gao X, Wehr M (2008) Level dependence of contextual modulation in auditory cortex. J Neurophysiol 99:1616-1627.
51. Shore SE (1995) Recovery of forward-masked responses in ventral cochlear nucleus neurons. Hear Res 82:31-43.
52. Smith RL (1977) Short-term adaptation in single auditory nerve fibers: some poststimulatory effects. J Neurophysiol 40:1098-1111.
53. Starr A (1965) Suppression of single unit activity in cochlear nucleus of the cat following sound stimulation. J Neurophysiol 28:850-862.
54. Tan ML, Borst JG (2007) Comparison of responses of neurons in the mouse inferior colliculus to current injections, tones of different durations, and sinusoidal amplitude-modulated tones. J Neurophysiol 98:454-466.
55. Wehr M, Zador AM (2005) Synaptic mechanisms offorward suppression in rat auditory cortex. Neuron 47:437-445.
56. Widin GP, Viemeister NF (1979) Intensive and temporal effects in puretone forward masking. J Acoust Soc Am 66:388-395.
57. Xie R, Gittelman JX, Li N, Pollak GD (2008) Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus. Neuroscience 154:245-256.
58. Zilany MS, Bruce IC (2007) Representation of the vowel /ε/ in normal and impaired auditory nerve fibers: model predictions of responses in cats. J Acoust Soc Am 122:402-417.