Abstract
Aging is accompanied by the deterioration of hearing that complicates our understanding of speech, especially in noisy environments. This deficit is partially caused by the loss of hair cells as well as by the dysfunction of the stria vascularis. However, the central part of the auditory system is also affected by processes accompanying aging that may run independently of those affecting peripheral receptors. Here, we review major changes occurring in the central part of the auditory system during aging. Most of the information that is focused on age-related changes in the central auditory system of experimental animals arises from experiments using immunocytochemical targeting on changes in the glutamic-acid-decarboxylase, parvalbumin, calbindin and calretinin. These data are accompanied by information about age-related changes in the number of neurons as well as about changes in the behavior of experimental animals. Aging is in principle accompanied by atrophy of the gray as well as white matter, resulting in the enlargement of the cerebrospinal fluid space. The human auditory cortex suffers not only from atrophy but also from changes in the content of some metabolites in the aged brain, as shown by magnetic resonance spectroscopy. In addition to this, functional magnetic resonance imaging reveals differences between activation of the central auditory system in the young and old brain. Altogether, the information reviewed in this article speaks in favor of specific age-related changes in the central auditory system that occur mostly independently of the changes in the inner ear and that form the basis of the central presbycusis.
Similar content being viewed by others
Abbreviations
- AC:
-
Auditory cortex
- AI:
-
Primary auditory cortex
- ASR:
-
Acoustic startle reflex
- C57:
-
C57/BL/6J mouse strain
- CB:
-
Calbindin
- CB(PV/CR)−/−:
-
CB(PV/CR)-deficient strain of mice
- CBA:
-
CBA/CaJ mouse strain
- CBP(s):
-
Calcium binding protein(s)
- CL:
-
Caudolateral auditory field
- CNs:
-
Cochlear nuclei
- CR:
-
Calretinin
- Cr:
-
Creatine
- CSF:
-
Cerebrospinal fluid
- DCN:
-
Dorsal cochlear nucleus
- DTI:
-
Diffusion tensor imaging
- EP:
-
Elderly subjects with expressed presbycusis
- F344:
-
Fischer 344 rat strain
- FA:
-
Fractional anisotropy
- fMRI:
-
Functional magnetic resonance imaging
- GABA:
-
Gamma aminobutyric acid
- GAD67:
-
Glutamate-decarboxylase (isoform 67)
- GM:
-
Gray matter
- GrayVol:
-
Gray matter volume
- HG:
-
Heschl’s gyrus
- IC:
-
Inferior colliculus
- Ins:
-
Myo-inositol
- -ir:
-
Immunoreactive
- Long-Evans:
-
Long-Evans rat strain
- MCI:
-
Mild cognitive impairment
- MD:
-
Mean diffusivity
- MGB:
-
Medial geniculate body
- MMN:
-
Mismatch negativity
- MNTB:
-
Medial nucleus of trapezoid body
- MP:
-
Elderly subjects with mild presbycusis
- MRM:
-
Magnetic resonance morphometry
- MRS:
-
Magnetic resonance spectroscopy
- MRs:
-
MR spectroscopy
- NAA:
-
N-acetylaspartate
- NADPH-d:
-
Nicotinamide adenine dinucleotide hydrogen phosphate diaphorase
- PCr:
-
Phosphocreatine
- PET:
-
Positron emission tomography
- PPI:
-
Prepulse inhibition
- PT:
-
Planum temporale
- PV:
-
Parvalbumin
- ROI:
-
Region of interest
- SNHL:
-
Sensorineural hearing loss
- VCN:
-
Ventral cochlear nucleus
- VOI:
-
Volume of interest
- VOT:
-
Varying voice onset times
- WM:
-
White matter
- WML:
-
White matter lesion
- YC:
-
Young subjects with physiologic hearing
References
Abe O, Yamasue H, Yamada H, Masutani Y, Kabasawa H, Sasaki H, Takei K, Suga M, Kasai K, Aoki S, Ohtomo K (2010) Sex dimorphism in gray/white matter volume and diffusion tensor during normal aging. NMR Biomed 23:446–458
Aboitiz F, Rodriguez E, Olivares R, Zaidel E (1996) Age-related changes in fibre composition of the human corpus callosum: Sex differences. Neuroreport 7:1761–1764
Achard S, Bullmore ET (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:174–183
Aine CJ, Bryant JE, Knoefel JE, Adair JC, Hart B, Donahue CH, Montano R, Hayek R, Qualls C, Ranken D, Stephen JM (2010) Different strategies for auditory word recognition in healthy versus normal aging. Neuroimage 49:3319–3330
Alain C, McDonald KL, Ostroff JM, Schneider B (2001) Age-related changes in detecting a mistuned harmonic. J Acoust Soc Am 109:2211–2216
Alibardi L (1999) Fine structure, synaptology and immunocytochemistry of large neurons in the rat dorsal cochlear nucleus connected to the inferior colliculus. J Hirnforsch 39:429–439
Allen PD, Eddins DA (2010) Presbycusis phenotypes form a heterogeneous continuum when ordered by degree and configuration of hearing loss. Hear Res 264:10–20
Allen JS, Bruss J, Brown CK, Damasio H (2005) Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiol Aging 26:1245–1260
Alzheimer’s Association (2011) 2011 Alzheimer’s disease facts and figures. Alzheimers Dement 7:208–244
Amenedo E, Diaz F (1998) Automatic and effortful processes in auditory memory reflected by event-related potentials. Age-related findings. Electroencephalogr Clin Neurophysiol 108:361–369
Andres P, Parmentier FBR, Escera C (2006) The effect of age on involuntary capture of attention by irrelevant sounds: a test of the frontal hypothesis of aging. Neuropsychologia 44:2564–2568
Angelie E, Bonmartin A, Boudraa A, Gonnaud PM, Mallet JJ, Sappey-Marinier D (2001) Regional differences and metabolic changes in normal aging of the human brain: proton MR spectroscopic imaging study. Am J Neuroradiol 22:119–127
Appelman APA, Exalto LG, van der Graaf Y, Biessels GJ, Mali W, Geerlings MI (2009) White matter lesions and brain atrophy: more than shared risk factors? A systematic review. Cerebrovasc Dis 28:227–242
Ardekani S, Kumar A, Bartzokis G, Sinha U (2007) Exploratory voxel-based analysis of diffusion indices and hemispheric asymmetry in normal aging. Magn Reson Imaging 25:154–167
Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G et al (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568
Aydin K, Ciftci K, Terzibasioglu E, Ozkan M, Demirtas A, Sencer S, Minareci O (2005) Quantitative proton MR spectroscopic findings of cortical reorganization in the auditory cortex of musicians. Am J Neuroradiol 26:128–136
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
Bao SW, Chang EF, Woods J, Merzenich MM (2004) Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat Neurosci 7:974–981
Beierlein M, Gibson J, Connors B (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3:904–910
Bellis TJ, Nicol T, Kraus N (2000) Aging affects hemispheric asymmetry in the neural representation of speech sounds. J Neurosci 20:791–797
Bertoli S, Smurzynski J, Probst R (2002) Temporal resolution in young and elderly subjects as measured by mismatch negativity and a psychoacoustic gap detection task. Clin Neurophysiol 113:396–406
Bertoli S, Smurzynski J, Probst R (2005) 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
Bigler ED, Andersob CV, Blatter DD (2002) Temporal lobe morphology in normal aging and traumatic brain injury. Am J Neuroradiol 23:255–266
Bischkopf J, Busse A, Angermeyer MC (2002) Mild cognitive impairment - a review of prevalence, incidence and outcome according to current approaches. Acta Psychiatr Scand 106:403–414
Boyen K, Langers DRM, de Kleine E, van Dijk P (2013) Gray matter in the brain: differences associated with tinnitus and hearing loss. Hear Res 295:67–78
Bredberg G (1968) Cellular pattern and nerve supply of the human organ of Corti. Acta Otolaryngol. Suppl 236:1+
Browndyke JN, Giovanello K, Petrella J, Hayden K, Chiba-Falek O, Tucker KA, Burke JR, Welsh-Bohmer KA (2013) Phenotypic regional functional imaging patterns during memory encoding in mild cognitive impairment and Alzheimer’s disease. Alzheimers Dement 9:284–294
Bu J, Sathyendra V, Nagykery N, Geula C (2003) Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp Neurol 182:220–231
Buckiova D, Popelar J, Syka J (2006) Collagen changes in the cochlea of aged Fischer 344 rats. Exp Gerontol 41:296–302
Buckiova D, Popelar J, Syka J (2007) Aging cochleas in the F344 rat: morphological and functional changes. Exp Gerontol 42:629–638
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
Burkard RF, Sims D (2001) The human auditory brainstem response to high click rates: aging effects. Am J Audiol 10:53–61
Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929
Casey MA, Feldman ML (1982) Aging in the rat medial nucleus of the trapezoid body. I. Light microscopy. Neurobiol Aging 3:187–195
Casey MA, Feldman ML (1988) Age-related loss of synaptic terminals in the rat medial nucleus of the trapezoid body. Neuroscience 24:189–194
Caspary DM, Finlayson PG (1991) Superior olivary complex: functional neuropharmacology of the principal cell types. In: Altschuler RA, Hoffman DW, Bobbin RP, Clopton B (eds) Neurobiology of hearing, Vol. II: the central auditory system. Raven, New York, pp 141–162
Caspary DM, Raza A, Lawhorn Armour BA, Pippin J, Arneric SP (1990) Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus: implications for neural presbycusis. J Neurosci 10:2363–2372
Caspary DM, Milbrandt JC, Helfert RH (1995) Central auditory aging: GABA changes in the inferior colliculus. Exp Gerontol 30:349–360
Caspary DM, Holder TM, Hughes LF, Milbrandt JC, McKernan RM, Naritoku DK (1999) Age-related changes in GABAA receptor subunit composition and function in rat auditory system. Neuroscience 93:307–312
Caspary DM, Schatteman TA, Hughes LF (2005) Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs. J Neurosci 25:10952–10959
Caspary DM, Ling L, Turner JG, Hughes LF (2008) Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211:1781–1791
Caspary DM, Hughes LF, Ling LL (2013) Age-related GABAA receptor changes in rat auditory cortex. Neurobiol Aging 34:1486–1496
Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475
Ceyhan E, Beg MF, Ceritoglu C, Wang L, Morris JC, Csernansky JG, Miller MI, Ratnanather JT (2011) Quantization and analysis of hippocampal morphometric changes due to dementia of Alzheimer type using metric distances based on large deformation diffeomorphic metric mapping. Comput Med Imaging Graph 35:275–293
Chang L, Ernst T, Poland RE, Jenden DJ (1996) In vivo proton magnetic resonance spectroscopy of the normal aging human brain. Life Sci 58:2049–2056
Chang YM, Lee SH, Lee YJ, Hwang MJ, Bae SJ, Kim MN, Lee JM, Woo SK, Lee HJ, Kang DS (2004) Auditory neural pathway evaluation on sensorineural hearing loss using diffusion tensor imaging. Neuroreport 15:1699–1703
Chang L, Jiang CS, Ernst T (2009) Effects of age and sex on brain glutamate and other metabolites. Magn Reson Imaging 27:142–145
Chen XM, Liang YH, Deng YH, Li JZ, Chen SY, Wang CX, Luo P (2013) Age-associated reduction of asymmetry in human central auditory function: a 1H-magnetic resonance spectroscopy study. Neural Plast. doi:10.1155/2013/735290
Courchesne E, Chisum HJ, Townsend J, Cowles A, Covington J, Egaas B, Harwood M, Hinds S, Press GA (2000) Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 216:672–682
Cruikshank SJ, Killackey HP, Metherate R (2001) Parvalbumin and calbindin are differentially distributed within primary and secondary subregions of the mouse auditory forebrain. Neuroscience 105:553–569
Cumming GS (1996) Mantis movements by night and the interactions of sympatric bats and mantises. Can J Zool 74:1771–1774
Davis M, Gendelman D, Tischler M, Gendelman P (1982) A primary acoustic startle circuit: lesion and stimulation studies. J Neurosci 6:791–805
De Felipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1–19
De Villers-Sidani E, Alzghoul L, Zhou X, Simpson KL, Lin RC, Merzenich MM (2010) Recovery of functional and structural age-related changes in the rat primary auditory cortex with operant training. Proc Natl Acad Sci U S A 107:13900–13905
Di Loreto JD, Cox C, Grover DA, Lazar E, del Cerro C, del Cerro M (1994) The influences of age, retinal topography, and gender on retinal degeneration in the Fischer 344 rat. Brain Res 647:181–191
Dias R, Robbins TW, Roberts AC (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69–72
Dickerson BC, Sperling RA (2008) Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer’s disease: Insights from functional MRI studies. Neuropsychologia 46:1624–1635
Ding N, Simon JZ (2012) Emergence of neural encoding of auditory objects while listening to competing speakers. Proc Natl Acad Sci U S A 109:11854–11859
Driscoll I, Hamilton DA, Petropoulos H, Yeo RA, Brooks WM, Baumgartner RN, Sutherland RJ (2003) The aging hippocampus: cognitive, biochemical and structural findings. Cereb Cortex 13:1344–1351
Du AT, Schuff N, Chao LL, Kornak J, Jagust WJ, Kramer JH, Reed BR, Miller BL, Norman D, Chui HC, Weiner MW (2006) Age effects on atrophy rates of entorhinal cortex and hippocampus. Neurobiol Aging 27:733–740
Eckert MA, Walczak A, Ahlstrom J, Denslow S, Horwitz A, Dubno JR (2008) Age-related effects on word recognition: reliance on cognitive control systems with structural declines in speech-responsive cortex. J Assoc Res Otolaryngol 9:252–259
Emir UE, Raatz S, McPherson S, Hodges JS, Torkelson C, Tawfik P, White T, Terpstra M (2011) Noninvasive quantification of ascorbate and glutathione concentration in the elderly human brain. NMR Biomed 24:888–894
Engle JR, Recanzone GH (2013) Characterizing spatial tuning functions of neurons in the auditory cortex of young and aged monkeys: a new perspective on old data. Front Aging Neurosci 4:36
Engle JR, Gray DT, Turner H, Udell JB, Recanzone GH (2014) Age-related neurochemical changes in the rhesus macaque inferior colliculus. Front Aging Neurosci 6:73
Fanselow EE, Richardson KA, Connors BW (2008) Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100:2640–2652
Felix RA 2nd, Portfors CV (2007) Excitatory, inhibitory and facilitatory frequency response areas in the inferior colliculus of hearing impaired mice. Hear Res 228:212–229
Fisher JP, Hartwich D, Seifert T, Olesen ND, McNulty CL, Nielsen HB, van Lieshout JJ, Secher NH (2013) Cerebral perfusion, oxygenation and metabolism during exercise in young and elderly individuals. J Physiol 591:1859–1870
Fitzgibbons PJ, Gordon-Salant S (1994) Age effects on measures of auditory duration discrimination. J Speech Hear Res 37:662–670
Fitzgibbons PJ, Gordon-Salant S (2001) Aging and temporal discrimination in auditory sequences. J Acoust Soc Am 109:2955–2963
Fitzgibbons PJ, Gordon-Salant S (2010) Age-related differences in discrimination of temporal intervals in accented tone sequences. Hear Res 264:41–47
Fitzgibbons PJ, Gordon-Salant S, Barrett J (2007) Age-related differences in discrimination of an interval separating onsets of successive tone bursts as a function of interval duration. J Acoust Soc Am 122:458–466
Frahm J, Kruger G, Merboldt KD, Kleinschmidt A (1996) Dynamic uncoupling and recoupling of perfusion and oxidative metabolism during focal brain activation in man. Magn Reson Med 35:143–148
Fredrich M, Reisch A, Illing RB (2009) Neuronal subtype identity in the rat auditory brainstem as defined by molecular profile and axonal projection. Exp Brain Res 195:241–260
Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470
Fries P, Schroder JH, Roelfsema PR, Singer W, Engel AK (2002) Oscillatory neuronal synchronization in primary visual cortex as a correlate of stimulus selection. J Neurosci 22:3739–3754
Frisina RD (2001) Subcortical neural coding mechanisms for auditory temporal processing. Hear Res 158:1–27
Frisina RD (2010) Aging changes in the central auditory system. In: Rees A, Palmer A (eds) Handbook of auditory science: the auditory brain. Oxford University Press, Oxford, pp 415–436
Frisina DR, Frisina RD (1997) Speech recognition in noise and presbycusis: relations to possible neural mechanisms. Hear Res 106:95–104
Gai Y, Carney LH (2008) Influence of inhibitory inputs on rate and timing of responses in the anteroventral cochlear nucleus. J Neurophysiol 99:1077–1095
Gao F, Edden RAE, Li MW, Puts NAJ, Wang GB, Liu C, Zhao B, Wang HQ, Bai X, Zhao C, Wang X, Barker PB (2013) Edited magnetic resonance spectroscopy detects an age-related decline in brain GABA levels. Neuroimage 78:75–82
Garcia-Alloza M, Tsang SW, Gil-Bea FJ, Francis PT, Lai MK, Marcos B, Chen CP, Ramirez MJ (2006) Involvement of the GABAergic system in depressive symptoms of Alzheimer’s disease. Neurobiol Aging 27:1110–1117
Gates GA, Cobb JL, Linn RT, Rees T, Wolf PA, Dagostino RB (1996) Central auditory dysfunction, cognitive dysfunction, and dementia in older people. Arch Otolaryngol Head Neck Surg 122:161–167
Gates GA, Gibbons LE, McCusrry SM, Crane PK, Feeney MP, Larson EB (2010) Executive dysfunction and presbycusis in older persons with and without memory loss and dementia. Cogn Behav Neurol 23:218–223
Geyer MA, Braff DL (1987) Startle habituation and sensorimotor gating in schizophrenia and related animal models. Schizophr Bull 13:643–668
Gleich O, Netz J, Strutz J (2014) Comparing the inferior colliculus of young and old gerbils (Meriones unguiculatus) with an emphasis on GABA. Exp Gerontol 57:155–162
Gonchar Y, Burkhalter A (1997) Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7:347–358
Gonchar Y, Wang Q, Burkhalter A (2007) Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat 1:1–11
Gonoi W, Abe O, Yamasue H, Yamada H, Masutani Y, Takao H, Kasai K, Aoki S, Ohtomo K (2010) Age-related changes in regional brain volume evaluated by atlas-based method. Neuroradiology 52:865–873
Gordon-Salant S, Fitzgibbons PJ (1993) Temporal factors and speech recognition performance in young and elderly listeners. J Speech Hear Res 36:1276–1285
Gordon-Salant S, Yeni-Komshian GH, Fitzgibbons PJ (2010) Recognition of accented English in quiet and noise by younger and older listeners. J Acoust Soc Am 128:3152–3160
Grachev ID, Apkarian AV (2001) Chemical network of the living human brain - evidence of reorganization with aging. Brain Res Cogn Brain Res 11:185–197
Grafton ST, Sumi SM, Stimac GK, Alvord EC, Shaw CM, Nochlin D (1991) Comparison of postmortem magnetic resonance imaging and neuropathologic findings in the cerebral white matter. Arch Neurol 48:293–298
Gray DT, Engle JR, Recanzone GH (2013a) Age-related neurochemical changes in the rhesus macaque superior olivary complex. J Comp Neurol 522:573–591
Gray DT, Rudolph ML, Engle JR, Recanzone GH (2013b) Parvalbumin increases in the medial and lateral geniculate nuclei of aged rhesus macaques. Front Aging Neurosci 5:69
Gray DT, Engle JR, Recanzone GH (2014a) Age-related neurochemical changes in the rhesus macaque cochlear nucleus. J Comp Neurol 522:1527–1541
Gray DT, Engle JR, Rudolph ML, Recanzone GH (2014b) Regional and age-related differences in GAD67 expression of parvalbumin- and calbindin-expressing neurons in the rhesus macaque auditory midbrain and brainstem. J Comp Neurol 522:4074–4084
Grimault N, Micheyl C, Carlyon RP, Arthaud P, Collet L (2000) Influence of peripheral resolvability on the perceptual segregation of harmonic complex tones differing in fundamental frequency. J Acoust Soc Am 108:263–271
Grose JH, Mamo SK (2010) Processing of temporal fine structure as a function of age. Ear Hear 31:755–760
Gruber S, Pinker K, Riederer F, Chmelik M, Stadlbauer A, Bittsansky M, Mlynarik V, Frey R, Serles W, Bodamer O, Moser E (2008) Metabolic changes in the normal ageing brain: consistent findings from short and long echo time proton spectroscopy. Eur J Radiol 68:320–327
Gujar SK, Maheshwari S, Bjorkman-Burtscher I, Sundgren PC (2005) Magnetic resonance spectroscopy. J Neuroophthalmol 25:217–226
Guo XX, Skoog I, Idrizbegovic E, Pantoni L, Simoni M, Rosenhall U (2008) Hearing loss and cortical atrophy in a population-based study on non-demented women. Age Ageing 37:333–336
Gutiérrez A, Khan ZU, Morris SJ, De Blas AL (1994) Age-related decrease of GABAA receptor subunits and glutamic acid decarboxylase in the rat inferior colliculus. J Neurosci 14:7469–7477
Harker KT, Whishaw IQ (2002) Place and matching-to-place spatial learning affected by rat inbreeding (Dark-Agouti, Fischer 344) and albinism (Wistar, Sprague–Dawley) but not domestication (wild rat vs. Long-Evans, Fischer-Norway). Behav Brain Res 134:467–477
Harris KC, Eckert MA, Ahlstrom JB, Dubno JR (2010) Age-related differences in gap detection: effects of task difficulty and cognitive ability. Hear Res 264:21–29
He NJ, Dubno JR, Mills JH (1998) Frequency and intensity discrimination measured in a maximum-likelihood procedure from young and aged normal-hearing subjects. J Acoust Soc Am 103:553–565
Helfert RH, Sommer TJ, Meeks J, Hofstetter P, Hughes LF (1999) Age-related synaptic changes in the central nucleus of the inferior colliculus of Fischer-344 rats. J Comp Neurol 406:285–298
Hendry SH, Schwark HD, Jones EG, Yan J (1987) Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7:1503–1519
Hickok G, Poeppel D (2007) Opinion - the cortical organization of speech processing. Nat Rev Neurosci 8:393–402
Hollen LI, Manser MB (2006) Ontogeny of alarm call responses in meerkats, Suricata suricatta: the roles of age, sex and nearby conspecifics. Anim Behav 72:1345–1353
Hua T, Kao C, Sun Q, Li X, Zhou Y (2008) Decreased proportion of GABA neurons accompanies age-related degradation of neuronal function in cat striate cortex. Brain Res Bull 75:119–125
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
Humes LE, Dubno JR (2010) Factors affecting speech understanding in older adults. In: Gordon-Slant S, Frisina R, Popper AN, Fay RR (eds) The aging auditory system. Springer, New York
Humes LE, Dubno JR, Gordon-Salant S, Lister JJ, Cacace AT, Cruickshanks KJ, Gates GA, Wilson RH, Wingfield A (2012) Central presbycusis: a review and evaluation of the evidence. J Am Acad Audiol 23:635–666
Husain FT, Medina RE, Davis CW, Szymko-Bennett Y, Simonyan K, Pajor NM, Horwitz B (2011) Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res 1369:74–88
Ibrahim I, Horacek J, Bartos A, Hajek M, Ripova D, Brunovsky M, Tintera J (2009) Combination of voxel based morphometry and diffusion tensor imaging in patients with Alzheimer’s disease. Neuroendocrinol Lett 30:39–45
Idrizbegovic E, Canlon B, Bross LS, Willott JF, Bogdanovic N (2001) The total number of neurons and calcium binding protein positive neurons during aging in the cochlear nucleus of CBA/CaJ mice: a quantitative study. Hear Res 158:102–115
Idrizbegovic E, Bogdanovic N, Viberg A, Canlon B (2003) Auditory peripheral influences on calcium binding protein immunoreactivity in the cochlear nucleus during aging in the C57BL/6J mouse. Hear Res 179:33–42
Idrizbegovic E, Bogdanovic N, Willott JF, Canlon B (2004) Age-related increases in calcium-binding protein immunoreactivity in the cochlear nucleus of hearing impaired C57BL/6J mice. Neurobiol Aging 25:1085–1093
Idrizbegovic E, Salman H, Niu X, Canlon B (2006) Presbyacusis and calcium-binding protein immunoreactivity in the cochlear nucleus of BALB/c mice. Hear Res 216–217:198–206
Irish M, Piguet O, Hodges JR, Hornberger M (2014) Common and unique gray matter correlates of episodic memory dysfunction in frontotemporal dementia and Alzheimer’s disease. Hum Brain Mapp 35:1422–1435
Jerger J, Jordan C (1992) Age-related asymmetry on a cued-listening task. Ear Hear 13:272–277
Jernigan TL, Archibald SL, Fennema-Notestine C, Gamst AC, Stout JC, Bonner J, Hesselink JR (2001) Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol Aging 22:581–594
Jilek M, Suta D, Syka J (2014) Reference hearing thresholds in an extended frequency range as a function of age. J Acoust Soc Am 136:1821
Jinno S, Kosaka T (2002) Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J Comp Neurol 449:1–25
Johnsson LG, Hawkins JE Jr (1972) Vascular changes in the human inner ear associated with aging. Ann Otol Rhinol Laryngol 81:364–376
Jones EG (2003) Chemically defined parallel pathways in the monkey auditory system. Ann N Y Acad Sci 999:218–233
Joo HJ, Ma JY, Choo YG, Choi BK, Jung KY (1999) Age-related alteration of intracellular ATP maintenance in the cell suspensions of mice cerebral cortex. Mech Ageing Dev 110:1–12
Juarez-Salinas DL, Engle JR, Navarro XO, Recanzone GH (2010) Hierarchical and serial processing in the spatial auditory cortical pathway is degraded by natural aging. J Neurosci 30:14795–14804
Kaiser LG, Schuff N, Cashdollar N, Weiner MW (2005) Age-related glutamate and glutamine concentration changes in normal human brain: H-1 MR spectroscopy study at 4T. Neurobiol Aging 26:665–672
Kamal B, Holman C, de Villers-Sidani E (2013) Shaping the aging brain: role of auditory input patterns in the emergence of auditory cortical impairments. Front Syst Neurosci 7:52
Kamba M, Inoue Y, Higami S, Suto Y (2003) Age-related changes in cerebral lactate metabolism in sleep-disordered breathing. Neurobiol Aging 24:753–760
Kantarci K (2013) Magnetic resonance spectroscopy in common dementias. Neuroimaging Clin N Am 23:393–406
Kantarci K, Parisi JE, Dickson DW, Petersen RC, Boeve BF, Knopman DS, Edland SD, Smith GE, Ivnik RJ, Jack CR (2004) Myo-inositol/creatine ratio correlates with the neuropathological involvement in Alzheimer’s disease. Neurobiol Aging 25:S372–S372
Karas GB, Scheltens P, Rombouts S, Visser PJ, van Schijndel RA, Fox NC, Barkhof F (2004) Global and local gray matter loss in mild cognitive impairment and Alzheimer’s disease. Neuroimage 23:708–716
Karas G, Sluimer J, Goekoop R, van der Flier W, Rombouts S, Vrenken H, Scheltens P, Fox N, Barkhof F (2008) Amnestic mild cognitive impairment: structural MR imaging findings predictive of conversion to Alzheimer disease. Am J Neuroradiol 29:944–949
Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476–486
Kelley P, Frisina RD, Zettel ML, Walton JP (1992) Differential calbindin immunoreactivity in the brainstem auditory system of the chinchilla. J Comp Neurol 320:196–212
Kerlin JR, Shahin AJ, Miller LM (2010) Attentional gain control ofongoing cortical speech representations in a ‘‘cocktail party’’. J Neurosci30:620–628
Kim DJ, Park SY, Kim J, Lee DH, Park HJ (2009) Alterations of white matter diffusion anisotropy in early deafness. Neuroreport 20:1032–1036
Kirov II, Fleysher L, Fleysher R, Patil V, Liu S, Gonen O (2008) Age dependence of regional proton metabolites T-2 relaxation times in the human brain at 3T. Magn Reson Med 60:790–795
Klug A, Bauer EE, Hanson JT, Hurley L, Meitzen J, Pollak GD (2002) Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition. J Neurophysiol 88:1941–1954
Koch M (1999) The neurobiology of startle. Prog Neurobiol 59:107–128
Kochunov P, Thompson PM, Lancaster JL, Bartzokis G, Smith S, Coyle T, Royall DR, Laird A, Fox PT (2007) Relationship between white matter fractional anisotropy and other indices of cerebral health in normal aging: tract-based spatial statistics study of aging. Neuroimage 35:478–487
Kral A, Tillein J, Heid S, Hartmann R, Klinke R (2005) Postnatal cortical development in congenital auditory deprivation. Cereb Cortex 15:552–562
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
Kubota Y, Hattori R, Yui Y (1994) Three distinct subpopulations of GABA-ergic neurons in rat frontal agranular cortex. Brain Res 649:159–173
Kuwabara T, Watanabe H, Tsuji S, Yuasa T (1995) Lactate rise in the basal ganglia accompanying finger movements: a localized 1H-MRS study. Brain Res 670:326–328
Laplante-Levesque A, Hickson L, Worrall L (2010) Rehabilitation of older adults with hearing impairment: a critical review. J Aging Health 22:143–153
Leary SM, Brex PA, MacManus DG, Parker GJM, Barker GJ, Miller DH, Thompson AJ (2000) A H-1 magnetic resonance spectroscopy study of aging in parietal white matter: implications for trials in multiple sclerosis. Magn Reson Imaging 18:455–459
Lee JE, Park HJ, Song SK, Sohn YH, Lee JD, Lee PH (2010) Neuroanatomic basis of amnestic MCI differs in patients with and without Parkinson disease. Neurology 75:2009–2016
Lemaitre H, Goldman AL, Sambataro F, Verchinski BA, Meyer-Lindenberg A, Weinberger DR, Mattay VS (2012) Normal age-related brain morphometric changes: nonuniformity across cortical thickness, surface area and gray matter volume? Neurobiol Aging 33:617.e1–9
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
Li WJ, Li JH, Xian JF, Lv B, Li M, Wang CH, Li Y, Liu ZH, Liu S, Wang ZC, He HG, Sabel BA (2013) Alterations of grey matter asymmetries in adolescents with prelingual deafness: a combined VBM and cortical thickness analysis. Restor Neurol Neurosci 31:1–17
Lin Y, Wang J, Wu C, Wai Y, Yu J, Ng S (2008) Diffusion tensor imaging of the auditory pathway in sensorineural hearing loss: changes in radial diffusivity and diffusion anisotropy. J Magn Reson Imaging 28:598–603
Lin FR, Thorpe R, Gordon-Salant S, Ferrucci L (2011) Hearing loss prevalence and risk factors among older adults in the United States. J Gerontol A 66:582–590
Lin JFL, Imada T, Kuhl PK (2012) Mental addition in bilinguals: An fMRI study of task-related and performance-related activation. Cereb Cortex 22:1851–1861
Ling LL, Hughes LF, Caspary DM (2005) Age-related loss of the GABA synthetic enzyme glutamic acid decarboxylase in rat primary auditory cortex. Neuroscience 132:1103–1113
Litovsky RY, Delgutte B (2002) Neural correlates of the precedence effect in the inferior colliculus: effect of localization cues. J Neurophysiol 87:976–994
Lohmann C, Friauf E (1996) Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J Comp Neurol 367:90–109
Lutz J, Hemminger F, Stahl R, Dietrich O, Hempel M, Reiser M, Jager L (2007) Evidence of subcortical and cortical aging of the acoustic pathway: a diffusion tensor imaging (DTI) study. Acad Radiol 14:692–700
Madden DJ, Bennett IJ, Burzynska A, Potter GG, Chen NK, Song AW (2012) Diffusion tensor imaging of cerebral white matter integrity in cognitive aging. Biochim Biophys Acta 1822:386–400
Madsen PL, Cruz NF, Sokoloff L, Dienel GA (1999) Cerebral oxygen/glucose ratio is low during sensory stimulation and rises above normal during recovery: excess glucose consumption during stimulation is not accounted for by lactate efflux from or accumulation in brain tissue. J Cereb Blood Flow Metab 19:393–400
Maillet D, Rajah MN (2013) Association between prefrontal activity and volume change in prefrontal and medial temporal lobes in aging and dementia: a review. Ageing Res Rev 12:479–489
Manly JJ, Touradji P, Tang MX, Stern Y (2003) Literacy and memory decline among ethnically diverse elders. J Clin Exp Neuropsychol 25:680–690
Manschot SM, Brands AMA, van der Grond J, Kessels RPC, Algra A, Kappelle LJ, Biessels GJ, Utrecht Diabetic Encephalopathy S (2006) Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes 55:1106–1113
Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793–807
Martin del Campo HN, Measor KR, Razak KA (2012) Parvalbumin immunoreactivity in the auditory cortex of a mouse model of presbycusis. Hear Res 294:31–39
Martin JS, Jerger JF (2005) Some effects of aging on central auditory processing. J Rehabil Res Dev 42:25–43
Martinez-Bisbal MC, Celda B (2009) Proton magnetic resonance spectroscopy imaging in the study of human brain cancer. Q J Nucl Med Mol Imaging 53:618–630
Mazelová J, Popelar J, Syka J (2003) Auditory function in presbycusis: peripheral vs. central changes. Exp Gerontol 38:87–94
McCormick DA (1989) GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 62:1018–1027
McIntyre DJO, Charlton RA, Markus HS, Howe FA (2007) Long and short echo time proton magnetic resonance spectroscopic Imaging of the healthy aging brain. J Magn Reson Imaging 26:1596–1606
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
Merrill DA, Chiba AA, Tuszynski MH (2001) Conservation of neuronal number and size in the entorhinal cortex of behaviorally characterized aged rats. J Comp Neurol 438:445–456
Miao W, Li J, Tang M, Xian J, Li W, Liu Z, Liu S, Sabel BA, Wang Z, He H (2013) Altered white matter integrity in adolescents with prelingual deafness: a high-resolution tract-based spatial statistics imaging study. Am J Neuroradiol 34:1264–1270
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
Milbrandt JC, Hunter C, Caspary DM (1997) Alterations of GABAA receptor subunit mRNA levels in the aging Fisher 344 rat inferior colliculus neurons. J Comp Neurol 379:455–465
Milham MP, Erickson KI, Banich MT, Kramer AF, Webb A, Wszalek T, Cohen NJ (2002) Attentional control in the aging brain: insights from an fMRI study of the stroop task. Brain Cogn 49:277–296
Moffat SD, Elkins W, Resnick SM (2006) Age differences in the neural systems supporting human allocentric spatial navigation. Neurobiol Aging 27:965–972
Moore BCJ, Glasberg BR (1988) Gap detection with sinusoids and noise in normal, impaired, and electrically stimulated ears. J Acoust Soc Am 83:1093–1101
Muller M, Appelman APA, van der Graaf Y, Vincken KL, Mali W, Geerlings MI, Grp SS (2011) Brain atrophy and cognition: Interaction with cerebrovascular pathology? Neurobiol Aging 32:885–893
Munoz-Ruiz MA, Hartikainen P, Koikkalainen J, Wolz R, Julkunen V, Niskanen E, Herukka SK, Kivipelto M, Vanninen R, Rueckert D, Liu YW, Lotjonen J, Soininen H (2012) Structural MRI in frontotemporal dementia: comparisons between hippocampal volumetry, tensor-based morphometry and voxel-based morphometry. PLoS ONE 7:e52531
Mutter SA, Haggbloom SJ, Plumlee LF, Schirmer AR (2006) Aging, working memory, and discrimination learning. Q J Exp Psychol (Hove) 59:1556–1566
Narayan R, Ergün A, Sen K (2005) Delayed inhibition in cortical receptive fields and the discrimination of complex stimuli. J Neurophysiol 94:2970–2975
Nodal FR, López DE (2003) Direct input from cochlear root neurons to pontine reticulospinal neurons in albino rat. J Comp Neurol 460:80–93
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
Oliver DL, Izquierdo MA, Malmierca MS (2011) Persistent effects of early augmented acoustic environment on the auditory brainstem. Neuroscience 184:75–87
O’Neill WE, Zettel ML, Whittemore KR, Frisina RD (1997) Calbindin D-28k immunoreactivity in the medial nucleus of the trapezoid body declines with age in C57BL/6, but not CBA/CaJ, mice. Hear Res 112:158–166
Ouda L, Syka J (2012) Immunocytochemical profiles of inferior colliculus neurons in the rat and their changes with aging. Front Neural Circ 6:68
Ouda L, Druga R, Syka J (2008) Changes in parvalbumin immunoreactivity with aging in the central auditory system of the rat. Exp Gerontol 43:782–789
Ouda L, Burianova J, Syka J (2012) Age-related changes in calbindin and calretinin immunoreactivity in the central auditory system of the rat. Exp Gerontol 47:497–506
Ouellet L, de Villers-Sidani E (2014) Trajectory of the main GABAergic interneuron populations from early development to old age in the rat primary auditory cortex. Front Neuroanat 8:40
Pakkenberg B, Gundersen HJ (1997) Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 384:312–320
Pakkenberg B, Pelvig D, Marner L, Bundgaard MJ, Gundersen HJG, Nyengaard JR, Regeur L (2003) Aging and the human neocortex. Exp Gerontol 38:95–99
Palombi PS, Caspary DM (1996) Physiology of the aged Fischer 344 ratinferior colliculus: responses to contralateral monaural stimuli. J Neurophysiol 5:3114–3121
Parham K (1997) Distortion product otoacoustic emissions in the C57BL/6J mouse model of age-related hearing loss. Hear Res 112:216–234
Pecka M, Zahn TP, Saunier-Rebori B, Siveke I, Felmy F, Wiegrebe L, Klug A, Pollak GD, Grothe B (2007) Inhibiting the inhibition: a neuronal network for sound localization in reverberant environments. J Neurosci 27:1782–1790
Pekkonen E (2000) Mismatch negativity in aging and in Alzheimer’s and Parkinson’s diseases. Audiol Neuro Otol 5:216–224
Penhune VB, Cismaru R, Dorsaint-Pierre R, Petitto LA, Zatorre RJ (2003) The morphometry of auditory cortex in the congenitally deaf measured using MRI. Neuroimage 20:1215–1225
Persad CC, Abeles N, Zacks RT, Denburg NL (2002) Inhibitory changes after age 60 and their relationship to measures of attention and memory. J Gerontol B 57:P223–P232
Peters CA, Potter JF, Scholer SG (1988) Hearing impairment as a predictor of cognitive decline in dementia. J Am Geriatr Soc 36:981–986
Peters A, Sethares C, Moss MB (1998) The effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey. Cereb Cortex 8:671–684
Pfefferbaum A, Adalsteinsson E, Spielman D, Sullivan EV, Lim KO (1999) In vivo spectroscopic quantification of the N-acetyl moiety, creatine, and choline from large volumes of brain gray and white matter: effects of normal aging. Magn Reson Med 41:276–284
Pfefferbaum A, Sullivan EV, Carmelli D (2004) Morphological changes in aging brain structures are differentially affected by time-linked environmental influences despite strong genetic stability. Neurobiol Aging 25:175–183
Poe BH, Linville C, Brunso-Bechtold J (2001) Age-related decline of presumptive inhibitory synapses in the sensorimotor cortex as revealed by the physical disector. J Comp Neurol 406:285–298
Popelar J, Groh D, Mazelova J, Syka J (2003) Cochlear function in young and adult Fischer 344 rats. Hear Res 186:75–84
Popelar J, Groh D, Pelanova J, Canlon B, Syka J (2006) Age-related changes in cochlear and brainstem auditory functions in Fischer 344 rats. Neurobiol Aging 27:490–500
Portfors CV, Wenstrup JJ (2001) Topographical distribution of delay-tuned responses in the mustached bat inferior colliculus. Hear Res 151:95–105
Prieto JJ, Peterson BA, Winer JA (1994a) Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). J Comp Neurol 344:349–382
Prieto JJ, Peterson BA, Winer JA (1994b) Laminar distribution and neuronal targets of GABAergic axon terminals in cat primary auditory cortex (AI). J Comp Neurol 344:383–402
Profant O, Balogová Z, Dezortová M, Wagnerová D, Hájek M, Syka J (2013) Metabolic changes in the auditory cortex in presbycusis demonstrated by MR spectroscopy. Exp Gerontol 48:795–800
Profant O, Skoch A, Balogová Z, Tintěra J, Hlinka J, Syka J (2014a) Diffusion tensor imaging and MR morphometry of the central auditory pathway and auditory cortex in aging. Neuroscience 260:87–97
Profant O, Tintěra J, Balogová Z, Ibrahim I, Jilek M, Syka J (2014b) Functional changes in the human auditory cortex in ageing. PLoS ONE (in press)
Puts NAJ, Edden RAE (2012) In vivo magnetic resonance spectroscopy of GABA: a methodological review. Prog Nucl Magn Reson Spectrosc 60:29–41
Puts NAJ, Edden RAE, Evans CJ, McGlone F, McGonigle DJ (2011) Regionally specific human GABA concentration correlates with tactile discrimination thresholds. J Neurosci 31:16556–16560
Qiu CX, Winblad B, Fratiglioni L (2005) The age-dependent relation of blood pressure to cognitive function and dementia. Lancet Neurol 4:487–499
Radvansky GA, Dijkstra K (2007) Aging and situation model processing. Psychon Bull Rev 14:1027–1042
Raji CA, Lopez OL, Kuller LH, Carmichael OT, Longstreth WT, Gach HM, Boardman J, Bernick CB, Thompson PM, Becker JT (2012) White matter lesions and brain gray matter volume in cognitively normal elders. Neurobiol Aging 33:834.e7–834.e16
Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689
Raz N, Rodrigue KM, Kennedy KM, Acker JD (2007) Vascular health and longitudinal changes in brain and cognition in middle-aged and older adults. Neuropsychology 21:149–157
Raza A, Milbrandt JC, Arneric SP, Caspary DM (1994) Age-related changes in brainstem auditory neurotransmitters: measures of GABA and acetylcholine function. Hear Res 77:221–230
Reyngoudt H, Claeys T, Vlerick L, Verleden S, Acou M, Deblaere K, De Deene Y, Audenaert K, Goethals I, Achten E (2012) Age-related differences in metabolites in the posterior cingulate cortex and hippocampus of normal ageing brain: a H-1-MRS study. Eur J Radiol 81:E223–E231
Richards TL, Gates GA, Gardner JC, Merrill T, Hayes CE, Panagiotides H, Serafini S, Rubel EW (1997) Functional MR spectroscopy of the auditory cortex in healthy subjects and patients with sudden hearing loss. Am J Neuroradiol 18:611–620
Richardson BD, Ling LL, Uteshev VV, Caspary DM (2011) Extrasynaptic GABA(A) receptors and tonic inhibition in rat auditory thalamus. PLoS ONE 6:e16508
Rodriguez-Aranda C, Martinussen M (2006) Age-related differences in performance of phonemic verbal fluency measured by controlled oral word association task (COWAT): a meta-analytic study. Dev Neuropsychol 30:697–717
Ross AJ, Sachdev PS, Wen W, Valenzuela MJ, Brodaty H (2005) Cognitive correlates of H-1 MRS measures in the healthy elderly brain. Brain Res Bull 66:9–16
Ross JM, Öberg J, Brené S, Coppotelli G, Terzioglu M, Pernold K, Goiny M, Sitnikov R, Kehr J, Trifunovic A, Larsson NG, Hoffer BJ, Olson L (2010) High brain lactate is a hallmark of aging and caused by a shift in the lactate dehydrogenase A/B ratio. Proc Natl Acad Sci U S A 107:20087–20092
Roth TN, Hanebuth D, Probst R (2011) Prevalence of age-related hearing loss in Europe: a review. Eur Arch Otorhinolaryngol 268:1101–1107
Rudy B, Fishell G, Lee S, Hjerling-Leffler J (2011) Three groups of interneurons account for nearly 100 % of neocortical GABAergic neurons. Dev Neurobiol 71:45–61
Rybalko N, Suta D, Nwabueze-Ogbo F, Syka J (2006) Effect of auditory cortex lesions on the discrimination of frequency-modulated tones in rats. Eur J Neurosci 23:1614–1622
Rybalko N, Suta D, Popelár J, Syka J (2010) Inactivation of the left auditory cortex impairs temporal discrimination in the rat. Behav Brain Res 209:123–130
Rybalko N, Bureš Z, Burianová J, Popelář J, Poon PW, Syka J (2012) Age-related changes in the acoustic startle reflex in Fischer 344 and Long Evans rats. Exp Gerontol 47:966–973
Scheltens P, Barkhof F, Leys D, Wolters EC, Ravid R, Kamphorst W (1995) Histopathologic correlates of white matter changes on MRI in Alzheimer’s disease and normal aging. Neurology 45:883–888
Schmidt R, Schmidt H, Fazekas F (2000) Vascular risk factors in dementia. J Neurol 247:81–87
Schmidt S, Redecker C, Bruehl C, Witte OW (2008) Age-related decline of functional inhibition in rat cortex. Neurobiol Aging 31:504–511
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
Schneider BA, Pichora-Fuller K, Daneman M (2010) Effects of senescent changes in audition and cognition on spoken language comprehension. In: Gordon-Slant S, Frisina R, Popper AN, Fay RR (eds) The aging auditory system. Springer, New York
Schonwiesner M, Krumbholz K, Rubsamen R, Fink GR, von Cramon DY (2007) Hemispheric asymmetry for auditory processing in the human auditory brain stem, thalamus, and cortex. Cereb Cortex 17:492–499
Schubert F, Gallinat J, Seifert F, Rinneberg H (2004) Glutamate concentrations in human brain using single voxel proton magnetic resonance spectroscopy at 3 Tesla. Neuroimage 21:1762–1771
Schuff N, Ezekiel F, Gamst AC, Amend DL, Capizzano AA, Maudsley AA, Weiner MW (2001) Region and tissue differences of metabolites in normally aged brain using multislice 1H magnetic resonance spectroscopic imaging. Magn Reson Med 45:899–907
Schuknecht HF (1974) Pathology of the Ear. Harvard University Press, Cambridge
Schwaller B (2010) Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol 2:a004051
Schwaller B, Meyer M, Schiffmann S (2002) ‘New’ functions for ‘old’ proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1:241–258
Seifert T, Secher NH (2011) Sympathetic influence on cerebral blood flow and metabolism during exercise in humans. Prog Neurobiol 95:406–426
Shamy JLT, Buonocore MH, Makaron LM, Amaral DG, Barnes CA, Rapp PR (2006) Hippocampal volume is preserved and fails to predict recognition memory impairment in aged rhesus monkeys (Macaca mulatta). Neurobiol Aging 27:1405–1415
Shamy JL, Habeck C, Hof PR, Amaral DG, Fong SG, Buonocore MH, Stern Y, Barnes CA, Rapp PR (2011) Volumetric correlates of spatiotemporal working and recognition memory impairment in aged rhesus monkeys. Cereb Cortex 21:1559–1573
Sharma V, Nag TC, Wadhwa S, Roy TS (2009) Stereological investigation and expression of calcium-binding proteins in developing human inferior colliculus. J Chem Neuroanat 37:78–86
Sharp DJ, Scott SK, Mehra MA, Wise RJS (2006) The neural correlates of declining performance with age: evidence for age-related changes in cognitive control. Cereb Cortex 16:1739–1749
Sheppard JP, Wang JP, Wong PCM (2011) Large-scale cortical functional organization and speech perception across the lifespan. PLoS ONE 6:e16510
Shinno H, Inagaki T, Miyaoka T, Okazaki S, Kawamukai T, Utani E, Inami Y, Horiguchi J (2007) A decrease in N-acetylaspartate and an increase in myoinositol in the anterior cingulate gyrus are associated with behavioral and psychological symptoms in Alzheimer’s disease. J Neurol Sci 260:132–138
Silberberg G, Markram H (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53:735–746
Simon H, Frisina RD, Walton JP (2004) Age reduces response latency of mouse inferior colliculus neurons to AM sounds. J Acoust Soc Am 116:469–477
Sisneros JA, Bass AH (2005) Ontogenetic changes in the response properties of individual, primary auditory afferents in the vocal plainfin midshipman fish Porichthys notatus Girard. J Exp Biol 208:3121–3131
Smith KM, Mecoli MD, Altaye M, Komlos M, Maitra R, Eaton KP, Egelhoff JC, Holland SK (2011) Morphometric differences in the heschl’s gyrus of hearing impaired and normal hearing infants. Cereb Cortex 21:991–998
Snell KB, Frisina DR (2000) Relationships among age-related differences in gap detection and word recognition. J Acoust Soc Am 107:1615–1626
Somogyi P, Tamas G, Lujan R, Buhl EH (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26:113–135
Spongr VP, Flood DG, Frisina RD, Salvi RJ (1997) Quantitative measures of hair cell loss in CBA and C57BL/6 mice throughout their life spans. J Acoust Soc Am 101:3546–3553
Stanley DP, Shetty AK (2004) Aging in the rat hippocampus is associated with widespread reductions in the number of glutamate decarboxylase-67 positive interneurons but not interneuron degeneration. J Neurochem 89:204–216
Stanley EM, Fadel JR, Mott DD (2012) Interneuron loss reduces dendritic inhibition and GABA release in hippocampus of aged rats. Neurobiol Aging 33:431e1–431e13
Sullivan EV, Pfefferbaum A (2007) Neuroradiological characterization of normal adult ageing. Br J Radiol 80:S99–S108
Sullivan EV, Adalsteinsson E, Hedehus M, Ju C, Moseley M, Lim KO, Pfefferbaum A (2001) Equivalent disruption of regional white matter microstructure in ageing healthy men and women. Neuroreport 12:99–104
Sullivan EV, Marsh L, Pfefferbaum A (2005) Preservation of hippocampal volume throughout adulthood in healthy men and women. Neurobiol Aging 26:1093–1098
Sumner P, Edden RAE, Bompas A, Evans CJ, Singh KD (2010) More GABA, less distraction: a neurochemical predictor of motor decision speed. Nat Neurosci 13:825–827
Suta D, Rybalko N, Pelánová J, Popelář J, Syka J (2011) Age-related changes in auditory temporal processing in the rat. Exp Gerontol 46:739–746
Swerdlow NR, Geyer MA, Braff DL (2001) Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology 156:194–215
Syka J (2002) Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol Rev 82:601–636
Syka J (2010) The Fischer 344 rat as a model of presbycusis. Hear Res 264:70–78
Tadros SF, Frisina ST, Mapes F, Kim S, Frisina DR, Frisina RD (2005) Loss of peripheral right-ear advantage in age-related hearing loss. Audiol Neuro Otol 10:44–52
Takahashi T, Murata T, Omori M, Kosaka H, Takahashi K, Yonekura Y, Wada Y (2004) Quantitative evaluation of age-related white matter microstructural changes on MRI by multifractal analysis. J Neurol Sci 225:33–37
Taki Y, Thyreau B, Kinomura S, Sato K, Goto R, Wu K, Kawashima R, Fukuda H (2013) A longitudinal study of age- and gender-related annual rate of volume changes in regional gray matter in healthy adults. Hum Brain Mapp 34:2292–2301
Tardif E, Chiry O, Probst A, Magistretti PJ, Clarke S (2003) Patterns of calcium-binding proteins in human inferior colliculus: identification of subdivisions and evidence for putative parallel systems. Neuroscience 116:1111–1121
Toescu EC, Verkhratsky A, Landfield PW (2004) Ca2+ regulation and gene expression in normal brain aging. Trends Neurosci 27:614–620
Tramo MJ, Cariani PA, Koh CK, Makris N, Braida LD (2005) Neurophysiology and neuroanatomy of pitch perception: auditory cortex. Neurosciences and music Ii: from perception to performance. Ann N Y Acad Sci 1060:148–174
Tremblay KL, Piskosz M, Souza P (2003) Effects of age and age-related hearing loss on the neural representation of speech cues. Clin Neurophysiol 114:1332–1343
Tremblay MÈ, Zettel ML, Ison JR, Allen PD, Majewska AK (2012) Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices. Glia 60:541–558
Tucker-Drob EM (2011) Neurocognitive functions and everyday functions change together in old age. Neuropsychology 25:368–377
Turner JG, Hughes LF, Caspary DM (2005a) Effects of aging on receptive fields in rat primary auditory cortex layer V neurons. J Neurophysiol 94:2738–2747
Turner JG, Hughes LF, Caspary DM (2005b) Divergent response properties of layer-V neurons in rat primary auditory cortex. Hear Res 202:129–140
Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97–107
Urrila AS, Hakkarainen A, Heikkinen S, Vuori K, Stenberg D, Hakkinen AM, Lundbom N, Porkka-Heiskanen T (2003) Metabolic imaging of human cognition: an fMRI/H-1-MRS study of brain lactate response to silent word generation. J Cereb Blood Flow Metab 23:942–948
Valenzuela MJ, Sachdev P (2001) Magnetic resonance spectroscopy in AD. Neurology 56:592–598
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
Vela J, Gutierrez A, Vitorica J, Ruano D (2003) Rat hippocampal GABAergic molecular markers are differentially affected by ageing. J Neurochem 85:368–377
Verkhratsky A, Toescu EC (1998) Calcium and neuronal ageing. Trends Neurosci 21:2–7
Vongpoisal T, Pichora-Fuller MK (2007) Effect of age on F-0 difference limen and concurrent vowel identification. J Speech Lang Hear Res 50:1139–1156
Waldman ADB, Rai GS, McConnell JR, Chaudry M, Grant D (2002) Clinical brain proton magnetic resonance spectroscopy for management of Alzheimer’s and sub-cortical ischemic vascular dementia in older people. Arch Gerontol Geriatr 35:137–142
Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Eilertsen DE, Quinn BT, Salat D, Makris N, Fischl B (2005) Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26:1261–1270
Walton JP (2010) Timing is everything: temporal processing deficits in the aged auditory brainstem. Hear Res 264:63–69
Walton JP, Frisina RD, Ison JE, O’Neill WE (1997) Neural correlates of behavioral gap detection in the inferior colliculus of the young CBA mouse. J Comp Physiol A 181:161–176
Walton JP, Frisina RD, O’Neill WE (1998) Age-related alteration in processing of temporal sound features in the auditory midbrain of the CBA mouse. J Neurosci 18:2764–2776
Walton JP, Simon H, Frisina RD (2002) Age-related alterations in the neural coding of envelope periodicities. J Neurophysiol 88:565–578
Wang ZQ, Guo XJ, Qi ZG, Yao L, Li KC (2010) Whole-brain voxel-based morphometry of white matter in mild cognitive impairment. Eur J Radiol 75:129–133
Weaver KE, Richards TL, Saenz M, Petropoulos H, Fine I (2013) Neurochemical changes within human early blind occipital cortex. Neuroscience 252:222–233
Webster DB, Webster M (1971) Adaptive value of hearing and vision in kangaroo rat predator avoidance. Brain Behav Evol 4:310–322
Wetzel W, Wagner T, Ohl FW, Scheich H (1998) Categorical discrimination of direction in frequency-modulated tones by Mongolian gerbils. Behav Brain Res 91:29–39
Willott JF (1991) Aging and the auditory system. Singular, San Diego
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
Winer JA, Larue DT (1996) Evolution of GABAergic circuitry in the mammalian medial geniculate body. Proc Natl Acad Sci U S A 93:3083–3087
Wong PCM, Uppunda AK, Parrish TB, Dhar S (2008) Cortical mechanisms of speech perception in noise. J Speech Lang Hear Res 51:1026–1041
Wong PCM, Jin JXM, Gunasekera GM, Abel R, Lee ER, Dhar S (2009) Aging and cortical mechanisms of speech perception in noise. Neuropsychologia 47:693–703
Wong PCM, Ettlinger M, Sheppard JP, Gunasekera GM, Dhar S (2010) Neuroanatomical characteristics and speech perception in noise in older adults. Ear Hear 31:471–479
Woods TM, Lopez SE, Long JH, Rahman JE, Recanzone GH (2006) Effects of stimulus azimuth and intensity on the single-neuron activity in the auditory cortex of the alert macaque monkey. J Neurophysiol 96:3323–3337
Wu CM, Ng SH, Wang JJ, Liu TC (2009) Diffusion tensor imaging of the subcortical auditory tract in subjects with congenital cochlear nerve deficiency. Am J Neuroradiol 30:1773–1777
Yan J, Suga N (1996) The midbrain creates and the thalamus sharpens echodelay tuning for the cortical representation of target-distance information in the mustached bat. Hear Res 93:102–110
Yildiz-Yesiloglu A, Ankerst DP (2006) Neurochemical alterations of the brain in bipolar disorder and their implications for pathophysiology: a systematic review of the in vivo proton magnetic resonance spectroscopy findings. Prog Neuropsychopharmacol Biol Psychiatry 30:969–995
Yuan K, Shih JY, Winer JA, Schreiner CE (2011) Functional networks of parvalbumin-immunoreactive neurons in cat auditory cortex. J Neurosci 31:13333–13342
Zaehle T, Wustenberg T, Meyer M, Jancke L (2004) Evidence for rapid auditory perception as the foundation of speech processing: a sparse temporal sampling fMRI study. Eur J Neurosci 20:2447–2456
Zarow C, Vinters HV, Ellis WG, Weiner MW, Mungas D, White L, Chui HC (2005) Correlates of hippocampal neuron number in Alzheimer’s disease and ischemic vascular dementia. Ann Neurol 57:896–903
Zettel ML, Frisina RD, Haider SE, O’Neill WE (1997) Age-related changes in calbindin D-28k and calretinin immunoreactivity in the inferior colliculus of CBA/CaJ and C57Bl/6 mice. J Comp Neurol 386:92–110
Zettel ML, O’Neill WE, Trang TT, Frisina RD (2001) Early bilateral deafening prevents calretinin up-regulation in the dorsal cortex of the inferior colliculus of aged CBA/CaJ mice. Hear Res 158:131–138
Acknowledgment
This study was supported by the Grant Agency of the Czech Republic P304/12/G069 and P304/12/1342.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ouda, L., Profant, O. & Syka, J. Age-related changes in the central auditory system. Cell Tissue Res 361, 337–358 (2015). https://doi.org/10.1007/s00441-014-2107-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-014-2107-2