Neural correlates of age-related declines in frequency selectivity in the auditory midbrain

Reduced frequency selectivity is associated with an age-related decline in speech recognition in background noise and reverberant environments. To elucidate neural correlates of age-related alteration in frequency selectivity, the present study examined frequency response areas (FRAs) of multi-unit clusters in the inferior colliculus of young, middle-aged, and old CBA/CaJ mice. The FRAs in middle-aged and old mice were found to be broader and more asymmetric in shape. In addition to a decrease of closed/complex FRAs in both middle age and old groups, there was a transient decrease in V-shaped FRAs and a concomitant increase in multipeak FRAs in middle age. Intensity coding was also affected by age, as observed in an increase of monotonic responses in middle-aged and old mice. While a decline in low-level activity began in middle age, reduced driven rates at suprathreshold levels occurred later in old age. Collectively, these results support the view that aging alters frequency selectivity by widening excitatory FRAs and that these changes begin to appear in middle age.

[1]  Jun Yan,et al.  Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. , 2005, Journal of neurophysiology.

[2]  B. Moore,et al.  Psychoacoustic abilities of subjects with unilateral and bilateral cochlear hearing impairments and their relationship to the ability to understand speech. , 1989, Scandinavian audiology. Supplementum.

[3]  A. Leventhal,et al.  GABA and Its Agonists Improved Visual Cortical Function in Senescent Monkeys , 2003, Science.

[4]  J. Winer,et al.  GABA and glycine in the central auditory system of the mustache bat: Structural substrates for inhibitory neuronal organization , 1995, The Journal of comparative neurology.

[5]  G. Ehret,et al.  Frequency response areas of neurons in the mouse inferior colliculus. I. Threshold and tuning characteristics , 2001, Experimental Brain Research.

[6]  L F Hughes,et al.  Age‐related synaptic changes in the central nucleus of the inferior colliculus of Fischer‐344 rats , 1999, The Journal of comparative neurology.

[7]  C. Schreiner,et al.  Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. , 1991, Journal of neurophysiology.

[8]  D. Caspary,et al.  GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons. , 1996, Journal of neurophysiology.

[9]  D. Caspary,et al.  Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons , 1991, Hearing Research.

[10]  D. Caspary,et al.  Alterations of GABAA receptor subunit mRNA levels in the aging Fischer 344 rat inferior colliculus , 1997, The Journal of comparative neurology.

[11]  D. Caspary,et al.  Physiology of the aged Fischer 344 rat inferior colliculus: responses to contralateral monaural stimuli. , 1996, Journal of neurophysiology.

[12]  G D Pollak,et al.  GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. , 1992, Journal of neurophysiology.

[13]  McGeer Pl,et al.  Aging and neurotransmitter systems. , 1980 .

[14]  R. Felix,et al.  Spectral integration in the inferior colliculus of the CBA/CaJ mouse , 2005, Neuroscience.

[15]  A. J. Moffat,et al.  Inferior colliculus of the house mouse , 1985, Journal of Comparative Physiology A.

[16]  M. Malmierca,et al.  The inferior colliculus of the rat: A quantitative analysis of monaural frequency response areas , 2005, Neuroscience.

[17]  R J Salvi,et al.  Quantitative measures of hair cell loss in CBA and C57BL/6 mice throughout their life spans. , 1997, The Journal of the Acoustical Society of America.

[18]  Manuel S. Malmierca,et al.  Iontophoresis In Vivo Demonstrates a Key Role for GABAA and Glycinergic Inhibition in Shaping Frequency Response Areas in the Inferior Colliculus of Guinea Pig , 2001, The Journal of Neuroscience.

[19]  R. Rajan,et al.  Plasticity of excitation and inhibition in the receptive field of primary auditory cortical neurons after limited receptor organ damage. , 2001, Cerebral cortex.

[20]  D. O. Kim,et al.  Distortion product otoacoustic emissions in the CBA/J mouse model of presbycusis , 1999, Hearing Research.

[21]  D. Naritoku,et al.  Age-related changes in GABAA receptor subunit composition and function in rat auditory system , 1999, Neuroscience.

[22]  Jeremy G. Turner,et al.  Divergent response properties of layer-V neurons in rat primary auditory cortex , 2005, Hearing Research.

[23]  K. Snell,et al.  Age-related changes in temporal gap detection. , 1997, The Journal of the Acoustical Society of America.

[24]  J. C. Hall GABAergic inhibition shapes frequency tuning and modifies response properties in the auditory midbrain of the leopard frog , 1999, Journal of Comparative Physiology A.

[25]  E Borg,et al.  Age-related loss of auditory sensitivity in two mouse genotypes. , 1991, Acta oto-laryngologica.

[26]  E F Evans,et al.  The sharpening of cochlear frequency selectivity in the normal and abnormal cochlea. , 1975, Audiology : official organ of the International Society of Audiology.

[27]  Larry F Hughes,et al.  Affects of aging on receptive fields in rat primary auditory cortex layer V neurons. , 2005, Journal of neurophysiology.

[28]  R G Matschke,et al.  Frequency selectivity and psychoacoustic tuning curves in old age. , 1990, Acta oto-laryngologica. Supplementum.

[29]  S. Arneric,et al.  Age-related changes in brainstem auditory neurotransmitters: Measures of GABA and acetylcholine function , 1994, Hearing Research.

[30]  B. Grothe,et al.  The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats , 2004, Journal of Comparative Physiology A.

[31]  J. Willott,et al.  Aging and the auditory brainstem response in mice with severe or minimal presbycusis , 1987, Hearing Research.

[32]  SungHee Kim,et al.  Effects of age on speech understanding in normal hearing listeners: Relationship between the auditory efferent system and speech intelligibility in noise , 2006, Speech Commun..

[33]  L. Humes,et al.  Erratum: Auditory filter shapes in normal‐hearing, noise‐masked normal, and elderly listeners [J. Acoust. Soc. Am. 93, 2903–2914 (1993)] , 1993 .

[34]  K. Barsz,et al.  Reorganization of receptive fields following hearing loss in inferior colliculus neurons , 2007, Neuroscience.

[35]  D. Caspary,et al.  Response properties in young and old Fischer-344 rat lateral superior olive neurons: A quantitative approach , 1993, Neurobiology of Aging.

[36]  R. Wenthold,et al.  Distribution of putative amino acid transmitters, choline acetyltransferase and glutamate decarboxylase in the inferior colliculus , 1979, Neuroscience.

[37]  R. Felix,et al.  Excitatory, inhibitory and facilitatory frequency response areas in the inferior colliculus of hearing impaired mice , 2007, Hearing Research.

[38]  J. Willott Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice. , 1986, Journal of neurophysiology.

[39]  G A Studebaker,et al.  Age-related changes in monosyllabic word recognition performance when audibility is held constant. , 1997, Journal of the American Academy of Audiology.

[40]  W. Greenough,et al.  A stereotaxic atlas of the albino mouse forebrain. , 1980 .

[41]  Peter C. Cheeseman,et al.  Bayesian Classification (AutoClass): Theory and Results , 1996, Advances in Knowledge Discovery and Data Mining.

[42]  Jos J. Eggermont,et al.  Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss , 2002, Hearing Research.

[43]  C Roup,et al.  Normal and hearing-impaired word recognition scores for monosyllabic words in quiet and noise. , 1997, British journal of audiology.

[44]  M. Sutter Shapes and level tolerances of frequency tuning curves in primary auditory cortex: quantitative measures and population codes. , 2000, Journal of neurophysiology.

[45]  L E Humes,et al.  Auditory filter shapes in normal-hearing, noise-masked normal, and elderly listeners. , 1993, The Journal of the Acoustical Society of America.

[46]  K. A. Davis Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus. , 2002, Journal of neurophysiology.

[47]  Robert D. Frisina,et al.  Contralateral suppression of distortion‐product otoacoustic emissions declines with age: A comparison of findings in CBA mice with human listeners , 2003, The Laryngoscope.

[48]  M. Liberman,et al.  Response properties of single auditory nerve fibers in the mouse. , 2005, Journal of neurophysiology.

[49]  K. Parham,et al.  Response properties of inferior colliculus neurons in young and very old CBA/J mice , 1988, Hearing Research.

[50]  W. O'Neill,et al.  Age-Related Alteration in Processing of Temporal Sound Features in the Auditory Midbrain of the CBA Mouse , 1998, The Journal of Neuroscience.

[51]  D. Caspary,et al.  Physiology of the young adult Fischer 344 rat inferior colliculus: responses to contralateral monaural stimuli , 1996, Hearing Research.

[52]  L. Hughes,et al.  Age-Related Changes in the Inhibitory Response Properties of Dorsal Cochlear Nucleus Output Neurons: Role of Inhibitory Inputs , 2005, The Journal of Neuroscience.

[53]  A R Palmer,et al.  Rate-intensity functions and their modification by broadband noise for neurons in the guinea pig inferior colliculus. , 1988, The Journal of the Acoustical Society of America.

[54]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[55]  A. Lajtha,et al.  Changes with aging in the levels of amino acids in rat CNS structural elements I. Glutamate and related amino acids , 1989, Neurochemical Research.

[56]  D. Caspary,et al.  Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus: implications for neural presbycusis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  Robert D Frisina,et al.  Speech recognition in noise and presbycusis: relations to possible neural mechanisms , 1997, Hearing Research.

[58]  R. Patterson,et al.  The deterioration of hearing with age: frequency selectivity, the critical ratio, the audiogram, and speech threshold. , 1982, The Journal of the Acoustical Society of America.