Impaired auditory temporal selectivity in the inferior colliculus of aged mongolian gerbils

Journal of Neuroscience

Volumn 31, Issue 27, 2011, Pages 9958-9970

  Khouri, Leila ^a,c   Lesica, Nicholas A ^b   Grothe, Benedikt ^a,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Integriertes Forschungs und Behandlungszentrum für Schwindel   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; AUDITORY SYSTEM; BRAIN FUNCTION; CONTROLLED STUDY; CORRELATIONAL STUDY; DOWN REGULATION; FEMALE; GERBIL; HEARING IMPAIRMENT; INFERIOR COLLICULUS; MALE; NERVE CELL MEMBRANE POTENTIAL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RECEPTIVE FIELD; SIGNAL DETECTION; SOUND DETECTION; SPEECH DISCRIMINATION; STIMULUS RESPONSE; TASK PERFORMANCE; TEMPORAL CORTEX;

ACOUSTIC STIMULATION; ACTION POTENTIALS; AGE FACTORS; AGING; ANIMALS; AUDITORY PERCEPTION; AUDITORY PERCEPTUAL DISORDERS; BRAIN MAPPING; ELECTRIC STIMULATION; FEMALE; GERBILLINAE; INFERIOR COLLICULI; MALE; NEURONS; PROBABILITY; PSYCHOACOUSTICS; REACTION TIME; SOUND; STATISTICS, NONPARAMETRIC; TIME FACTORS;

EID: 79960051460     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4509-10.2011     Document Type: Article

References (64)

1. Andoni S, Li N, Pollak GD (2007) Spectrotemporal receptive fields in the inferior colliculus revealing selectivity for spectral motion in conspecific vocalisations. J Neurosci 27:4882-4893.
2. Aronov D (2003) Fast algorithm for the metric-space analysis of simultaneous responses of multiple single neurons. J Neurosci Methods 124:175-179.
3. Atick JJ (1992) Could information theory provide an ecological theory of sensory processing? Network 3:213-251.
4. Banay-Schwartz M, Lajtha A, Palkovits M (1989) Changes with aging in the levels of amino acids in rat CNS structural elements. I. Glutamate and related amino acids. Neurochem Res 14:555-562.
5. Barsz K, Ison JR, Snell KB, Walton JP (2002) Behavioral and neural measures of auditory temporal acuity in aging humans and mice. Neurobiol Aging 23:565-578.
6. Boettcher FA, Mills JH, Swerdloff JL, Holley BL (1996) Auditory evoked potentials in aged gerbils: responses elicited by noises separated by a silent gap. Hear Res 102:167-178.
7. Brand A, Urban R, Grothe B (2000) Duration tuning in the mouse auditory midbrain. J Neurophysiol 84:1790-1799.
8. Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B (2002) Precise inhibition is essential for microsecond interaural time difference coding. Nature 417:543-547.
9. 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.
10. Burianova J, Ouda L, Profant O, Syka J (2009) Age-related changes in GAD levels in the central auditory system of the rat. Exp Gerontol 44:161-169.
11. Caspary DM, Palombi PS, Hughes LF (2002) GABAergic inputs shape responses to amplitude modulated stimuli in the inferior colliculus. Hear Res 168:163-173.
12. Casseday JH, Ehrlich D, Covey E (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264:847-850.
13. Casseday JH, Fremouw T, Covey E (2002) The inferior colliculus: a hub for the central auditory system. In: Integrative functions in the mammalian auditory pathway (Oertel D, Popper AN, Fay RR, eds), pp 238-318. New York: Springer.
14. Chelaru MI, Dragoi V (2008) Efficient coding in heterogeneous neuronal populations. Proc Natl Acad Sci U S A 105:16344-16349.
15. Ehrlich D, Casseday JH, Covey E (1997) Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77:2360-2372.
16. Faingold CL, Boersma Anderson CA, Caspary DM (1991) Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear Res 52:201-216.
17. Frisina RD (2001) Subcortical neural coding mechanisms for auditory temporal processing. Hear Res 158:1-27.
18. Fuzessery ZM, Hall JC (1996) Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol 76:1059-1073.
19. Gleich O, Hamann I, Klump GM, Kittel M, Strutz J (2003) Boosting GABA improves impaired auditory temporal resolution in the gerbil. Neuroreport 14:1877-1880.
20. Goŕdon-Salant S, Fitzgibbons PJ (1993) Temporal factors and speech recognition performance in young and elderly listeners. J Speech Hear Res 36:1276-1285.
21. Grothe B (1994) Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. J Neurophysiol 71:706-721.
22. Grothe B, Covey E, Casseday JH (2001) Medial superior olive of the big brown bat: neuronal responses to pure tones, amplitude modulations, and pulse trains. J Neurophysiol 86:2219-2230.
23. Gustafsson HA, Arlinger SD (1994) Masking of speech by amplitudemodulated noise. J Acoust Soc Am 95:518-529.
24. Hamann I, Gleich O, Klump GM, Kittel MC, Strutz J (2004) Age-dependent changes of gap detection in the Mongolian gerbil (Meriones unguiculatus). J Assoc Res Otolaryngol 5:49-57.
25. Holmstrom LA, Eeuwes LB, Roberts PD, Portfors CV (2010) Efficient encoding of vocalisations in the auditory midbrain. J Neurosci 30:802-819.
26. Hughes LF, Turner JG, Parrish JL, Caspary DM (2010) Processing of broadband stimuli across A1 layers in young and aged rats. Hear Res 264:79-85.
27. Irvine DR, Gago G (1990) Binaural interaction in high-frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences. J Neurophysiol 63:570-591.
28. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitudemodulated sounds. Physiol Rev 84:541-577.
29. Koch U, Grothe B (2000) Interdependence of spatial and temporal coding in the auditory midbrain. J Neurophysiol 83:2300-2314.
30. Krebs B, Lesica NA, Grothe B (2008) The representation of amplitude modulations in the mammalian auditory midbrain. J Neurophysiol 100:1602-1609.
31. Krenning J, Hughes LF, Caspary DM, Helfert RH (1998) Age-related glycine receptor subunit changes in the cochlear nucleus of Fischer-344 rats. Laryngoscope 108:26-31.
32. Krishna BS, Semple MN (2000) Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J Neurophysiol 84:255-273.
33. Kuwada S, Batra R (1999) Coding of sound envelopes by inhibitory rebound in neurons of the superior olivary complex in the unanesthetised rabbit. J Neurosci 19:2273-2287.
34. Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115-142.
35. Langner G, Schreiner CE (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60:1799-1822.
36. LeBeau FE, Malmierca MS, Rees A (2001) Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21:7303-7312.
37. Leventhal AG, Wang Y, Pu M, Zhou Y, Ma Y (2003) GABA and its agonists improved visual cortical function in senescent monkeys. Science 300: 812-815.
38. McAlpine D (2004) Neural sensitivity to periodicity in the inferior colliculus: evidence for the role of cochlear distortions. J Neurophysiol 92:1295-1311.
39. Milbrandt JC, Albin RL, Caspary DM (1994) Age-related decrease in GABAB receptor binding in the Fischer 344 rat inferior colliculus. Neurobiol Aging 15:699-703.
40. Milbrandt JC, Albin RL, Turgeon SM, Caspary DM (1996) GABAAreceptor binding in the aging rat inferior colliculus. Neuroscience 73:449-458.
41. Milbrandt JC, Hunter C, Caspary DM (1997) Alterations of GABAA receptor subunit mRNA levels in the aging Fischer 344 rat inferior colliculus. J Comp Neurol 379:455-465.
42. Milbrandt JC, Holder TM, Wilson MC, Salvi RJ, Caspary DM (2000) GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma. Hear Res 147:251-260.
43. Nadal JP, Parga N (1994) Nonlinear neurons in the low-noise limit: a factorial code maximises information transfer. Network 5:565-581.
44. Oliver DL, Huerta MF (1992) Inferior and superior colliculi. In: The mammalian auditory system: neuroanatomy (Webster DB, Popper AN, Fay RR, eds), pp 168-221. New York: Springer.
45. Pecka M, Brand A, Behrend O, Grothe B (2008) Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J Neurosci 28:6914-6925.
46. 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.
47. Pollak GD, Klug A, Bauer EE (2003a) Processing and representation of species-specific communication calls in the auditory system of bats. Int Rev Neurobiol 56:83-121.
48. Pollak GD, Burger RM, Klug A (2003b) Dissecting the circuitry of the auditory system. Trends Neurosci 26:33-39.
49. Rolls ET, Tovee MJ (1995) Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J Neurophysiol 73:713-726.
50. Rolls ET, Treves A (1990) The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain. Network 1:407-421.
51. Ryan A (1976) Hearing sensitivity of the mongolian gerbil, Meriones unguiculatis. J Acoust Soc Am 59:1222-1226.
52. Schmolesky MT, Wang Y, Pu M, Leventhal AG (2000) Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys. Nat Neurosci 3:384-390.
53. Schuller G, Radtke-Schuller S, Betz M (1986) Astereotaxic method for small animals using experimentally determined reference profiles. J Neurosci Methods 18:339-350.
54. Shaddock Palombi P, Backoff PM, Caspary DM (2001) Responses of young and aged rat inferior colliculus neurons to sinusoidally amplitude modulated stimuli. Hear Res 153:174-180.
55. Shamir M, Sompolinsky H (2006) Implications of neuronal diversity on population coding. Neural Comput 18:1951-1986.
56. Siveke I, Pecka M, Seidl AH, Baudoux S, Grothe B (2006) Binaural response properties of low-frequency neurons in the gerbil dorsal nucleus of the lateral lemniscus. J Neurophysiol 96:1425-1440.
57. Snell KB (1997) Age-related changes in temporal gap detection. J Acoust Soc Am 101:2214-2220.
58. Strouse A, Ashmead DH, Ohde RN, Grantham DW (1998) Temporal processing in the aging auditory system. J Acoust Soc Am 104:2385-2399.
59. van Rossum MC (2001) A novel spike distance. Neural Comput 13:751-763.
60. Vater M, Habbicht H, Kössl M, Grothe B (1992) The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats. J Comp Physiol A 171:541-553.
61. Victor JD, Purpura KP (1996) Nature and precision of temporal coding in visual cortex: a metric-space analysis. J Neurophysiol 76:1310-1326.
62. Walton JP, Simon H, Frisina RD (2002) Age-related alterations in the neural coding of envelope periodicities. J Neurophysiol 88:565-578.
63. Willott JF, Milbrandt JC, Bross LS, Caspary DM (1997) Glycine immunoreactivity and receptor binding in the cochlear nucleus of C57BL/6J and CBA/CaJ mice: effects of cochlear impairment and aging. J Comp Neurol 385:405-414.
64. Woolley SM, Casseday JH (2005) Processing of modulated sounds in the sebra finch auditory midbrain: responses to noise, frequency sweeps, and sinusoidal amplitude modulations. J Neurophysiol 94:1143-1157.