Stimulus-specific adaptation in auditory thalamus of young and aged awake rats

Journal of Neurophysiology

Volumn 110, Issue 8, 2013, Pages 1892-1902

  Richardson, Ben D ^a   Hancock, Kenneth E ^b,c   Caspary, Donald M ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Aging; Auditory thalamus; Awake animals; Medial geniculate body; Stimulus specific adaptation

Indexed keywords

AGING; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; AUDITORY SYSTEM FUNCTION; CONTROLLED STUDY; FISCHER/BROWN NORWAY RAT; MEDIAL GENICULATE BODY; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; STIMULUS SPECIFIC ADAPTATION; WAKEFULNESS;

AGING; AUDITORY THALAMUS; AWAKE ANIMALS; MEDIAL GENICULATE BODY; STIMULUS-SPECIFIC ADAPTATION;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; ANESTHESIA; ANIMALS; EVOKED POTENTIALS, AUDITORY; GENICULATE BODIES; MODELS, NEUROLOGICAL; RATS; WAKEFULNESS;

EID: 84885656873     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00403.2013     Document Type: Article

References (61)

1. Aitkin LM, Dunlop CW. Interplay of excitation and inhibition in the cat medial geniculate body. J Neurophysiol 31: 44-61, 1968.
2. Alain C, Woods DL. Age-related changes in processing auditory stimuli during visual attention: evidence for deficits in inhibitory control and sensory memory. Psychol Aging 14: 507-519, 1999.
3. Anderson LA, Christianson GB, Linden JF. Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29: 7359-7363, 2009.
4. Anderson LA, Malmierca MS. The effect of auditory cortex deactivation on stimulus-specific adaptation in the inferior colliculus of the rat. Eur J Neurosci 37: 52-62, 2013.
5. Antunes FM, Malmierca MS. Effect of auditory cortex deactivation on stimulus-specific adaptation in the medial geniculate body. J Neurosci 31: 17306-17316, 2011.
6. Antunes FM, Nelken I, Covey E, Malmierca MS. Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS One 5: e14071, 2010.
7. Ayala YA, Malmierca MS. Stimulus-specific adaptation and deviance detection in the inferior colliculus. Front Neural Circuits 6: 89, 2012.
8. Ayala YA, Pérez-González D, Duque D, Nelken I, Malmierca MS. Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus. Front Neural Circuits 6: 119, 2012.
9. Bäuerle P, von der Behrens W, Kössl M, Gaese BH. Stimulus-specific adaptation in the gerbil primary auditory thalamus is the result of a fast frequency-specific habituation and is regulated by the corticofugal system. J Neurosci 31: 9708-9722, 2011.
10. Bertoli S, Smurzynski J, Probst R. Effects of age, age-related hearing loss, and contralateral cafeteria noise on the discrimination of small frequency changes: psychoacoustic and electrophysiological measures. J Assoc Res Otolaryngol 6: 207-222, 2005.
11. Bertoli S, Smurzynski J, Probst R. Temporal resolution in young and elderly subjects as measured by mismatch negativity and a psychoacoustic gap detection task. Clin Neurophysiol 113: 396-406, 2002.
12. Bibikov NG. ["Novelty" neurons in the frog auditory system]. Zh Vyssh Nerv Deiat Im I P Pavlova 27: 1075-1082, 1977.
13. Calford MB, Aitkin LM. Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3: 2365-2380, 1983.
14. Caspary DM, Ling L, Turner JG, Hughes LF. Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211: 1781-1791, 2008.
15. Caspary DM, Schatteman TA, Hughes LF. Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs. J Neurosci 25: 10952-10959, 2005.
16. Crick F. Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci USA 81: 4586-4590, 1984.
17. de Villers-Sidani E, Alzghoul L, Zhou X, Simpson KL, Lin RC, Merzenich MM. Recovery of functional and structural age-related changes in the rat primary auditory cortex with operant training. Proc Natl Acad Sci USA 107: 13900-13905, 2010.
18. Du Y, Kong L, Wang Q, Wu X, Li L. Auditory frequency-following response: a neurophysiological measure for studying the "cocktail-party problem. " Neurosci Biobehav Rev 35: 2046-2057, 2011.
19. Duque D, Malmierca MS, Caspary DM. Modulation of stimulus-specific adaptation by the GABAergic system in the medial geniculate body of the anesthetized rat. J Physiol, 2013.
20. Duque D, Pérez-González D, Ayala YA, Palmer AR, Malmierca MS. Topographic distribution, frequency, and intensity dependence of stimulusspecific adaptation in the inferior colliculus of the rat. J Neurosci 32: 17762-17774, 2012.
21. Farley BJ, Quirk MC, Doherty JJ, Christian EP. Stimulus-specific adaptation in auditory cortex is an NMDA-independent process distinct from the sensory novelty encoded by the mismatch negativity. J Neurosci 30: 16475-16484, 2010.
22. Gaeta H, Friedman D, Ritter W, Cheng J. An event-related potential study of age-related changes in sensitivity to stimulus deviance. Neurobiol Aging 19: 447-459, 1998.
23. Gifford RH, Bacon SP, Williams EJ. An examination of speech recognition in a modulated background and of forward masking in younger and older listeners. J Speech Lang Hear Res 50: 857-864, 2007.
24. Gordon-Salant S, Fitzgibbons PJ. Comparing recognition of distorted speech using an equivalent signal-to-noise ratio index. J Speech Hear Res 38: 706-713, 1995a.
25. Gordon-Salant S, Fitzgibbons PJ. Recognition of multiply degraded speech by young and elderly listeners. J Speech Hear Res 38: 1150-1156, 1995b.
26. Grimault N, Micheyl C, Carlyon RP, Arthaud P, Collet L. Perceptual auditory stream segregation of sequences of complex sounds in subjects with normal and impaired hearing. Br J Audiol 35: 173-182, 2001.
27. Grimm S, Escera C, Slabu L, Costa-Faidella J. Electrophysiological evidence for the hierarchical organization of auditory change detection in the human brain. Psychophysiology 48: 377-384, 2011.
28. Gross NB, Thurlow WR. Microelectrode studies of neural auditory activity of cat. II. Medial geniculate body. J Neurophysiol 14: 409-422, 1951.
29. Guillery RW, Feig SL, Lozsadi DA. Paying attention to the thalamic reticular nucleus. Trends Neurosci 21: 28-32, 1998.
30. Hara K, Harris RA. The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg 94: 313-318, 2002.
31. Harris KC, Eckert MA, Ahlstrom JB, Dubno JR. Age-related differences in gap detection: effects of task difficulty and cognitive ability. Hear Res 264: 21-29, 2010.
32. Hughes LF, Turner JG, Parrish JL, Caspary DM. Processing of broadband stimuli across A1 layers in young and aged rats. Hear Res 264: 79-85, 2010.
33. Jones S, Mill R, Denham S, Klump G. Stimulus-specific adaptation in the inferior colliculus of the awake gerbil in response to Markov chain tone sequences (Abstract). In: Association for Research in Otolaryngology (ARO) Midwinter Meeting, San Diego, CA, 795, 2012.
34. Juarez-Salinas DL, Engle JR, Navarro XO, Recanzone GH. Hierarchical and serial processing in the spatial auditory cortical pathway is degraded by natural aging. J Neurosci 30: 14795-14804, 2010.
35. Kimura A, Yokoi I, Imbe H, Donishi T, Kaneoke Y. Auditory thalamic reticular nucleus of the rat: anatomical nodes for modulation of auditory and cross-modal sensory processing in the loop connectivity between the cortex and thalamus. J Comp Neurol 520: 1457-1480, 2012.
36. Kraus N, McGee T, Littman T, Nicol T, King C. Nonprimary auditory thalamic representation of acoustic change. J Neurophysiol 72: 1270-1277, 1994.
37. Ling LL, Hughes LF, Caspary DM. Age-related loss of the GABA synthetic enzyme glutamic acid decarboxylase in rat primary auditory cortex. Neuroscience 132: 1103-1113, 2005.
38. Lumani A, Zhang H. Responses of neurons in the rat's dorsal cortex of the inferior colliculus to monaural tone bursts. Brain Res 1351: 115-129, 2010.
39. Malmierca MS, Cristaudo S, Perez-Gonzalez D, Covey E. Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29: 5483-5493, 2009.
40. McAlonan K, Cavanaugh J, Wurtz RH. Attentional modulation of thalamic reticular neurons. J Neurosci 26: 4444-4450, 2006.
41. Naatanen R, Paavilainen P, Rinne T, Alho K. The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118: 2544-2590, 2007.
42. Nelken I, Antunes F, Hershenhoren I, Khouri L, Yarden T, Yaron A. Stimulus-specific adaptation in real and model neurons (Abstract). In: Association for Research in Otolaryngology (ARO) Midwinter Meeting, Baltimore, MD, 366, 2013.
43. Paxinos W, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1998.
44. Pérez-González D, Hernández O, Covey E, Malmierca MS. GABAAmediated inhibition modulates stimulus-specific adaptation in the inferior colliculus. PLoS One 7: e34297, 2012.
45. Pérez-González D, Malmierca MS. Variability of the time course of stimulus-specific adaptation in the inferior colliculus. Front Neural Circuits 6: 107, 2012.
46. Pérez-González D, Malmierca MS, Covey E. Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22: 2879-2885, 2005.
47. Pinault D. The thalamic reticular nucleus: structure, function and concept. Brain Res Rev 46: 1-31, 2004.
48. Rajan R, Cainer KE. Ageing without hearing loss or cognitive impairment causes a decrease in speech intelligibility only in informational maskers. Neuroscience 154: 784-795, 2008.
49. Richardson BD, Ling LL, Uteshev VV, Caspary DM. Reduced GABAA receptor-mediated tonic inhibition in aged rat auditory thalamus. J Neurosci 33: 1218-1227, 2013.
50. Slabu L, Escera C, Grimm S, Costa-Faidella J. Early change detection in humans as revealed by auditory brainstem and middle-latency evoked potentials. Eur J Neurosci 32: 859-865, 2010.
51. Slabu L, Grimm S, Escera C. Novelty detection in the human auditory brainstem. J Neurosci 32: 1447-1452, 2012.
52. Szymanski FD, Garcia-Lazaro JA, Schnupp JW. Current source density profiles of stimulus-specific adaptation in rat auditory cortex. J Neurophysiol 102: 1483-1490, 2009.
53. Ter-Mikaelian M, Sanes DH, Semple MN. Transformation of temporal properties between auditory midbrain and cortex in the awake Mongolian gerbil. J Neurosci 27: 6091-6102, 2007.
54. Ulanovsky N, Las L, Farkas D, Nelken I. Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24: 10440-10453, 2004.
55. Ulanovsky N, Las L, Nelken I. Processing of low-probability sounds by cortical neurons. Nat Neurosci 6: 391-398, 2003.
56. von der Behrens W, Bauerle P, Kossl M, Gaese BH. Correlating stimulusspecific adaptation of cortical neurons and local field potentials in the awake rat. J Neurosci 29: 13837-13849, 2009.
57. Wang H, Turner JG, Ling L, Parrish JL, Hughes LF, Caspary DM. Age-related changes in glycine receptor subunit composition and binding in dorsal cochlear nucleus. Neuroscience 160: 227-239, 2009.
58. Yang Y, Liang Z, Li G, Wang Y, Zhou Y, Leventhal AG. Aging affects contrast response functions and adaptation of middle temporal visual area neurons in rhesus monkeys. Neuroscience 156: 748-757, 2008.
59. Yang Y, Zhang J, Liang Z, Li G, Wang Y, Ma Y, Zhou Y, Leventhal AG. Aging affects the neural representation of speed in macaque area MT. Cereb Cortex 19: 1957-1967, 2009.
60. Yu XJ, Xu XX, He S, He J. Change detection by thalamic reticular neurons. Nat Neurosci 12: 1165-1170, 2009.
61. Zhao L, Liu Y, Shen L, Feng L, Hong B. Stimulus-specific adaptation and its dynamics in the inferior colliculus of rat. Neuroscience 181: 163-174, 2011.