Diffusion tensor imaging and MR morphometry of the central auditory pathway and auditory cortex in aging

Neuroscience

Volumn 260, Issue , 2014, Pages 87-97

  Profant, O ^a,d   Skoch A ^b   Balogova Z ^a,d   Tintera J ^b   Hlinka, J ^c   Syka, J ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^b INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

^c INSTITUTE OF COMPUTER SCIENCE   (Czech Republic)

^d CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Aging; Auditory cortex; Auditory pathway; Diffusion tensor imaging; MR morphometry; Presbycusis

Indexed keywords

AGED; AGING; ARTICLE; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; BRAIN ASYMMETRY; BRAIN SIZE; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DIFFUSION TENSOR IMAGING; FEMALE; FRONTAL GYRUS; GRAY MATTER; HEARING ACUITY; HUMAN; INFERIOR COLLICULUS; MALE; MORPHOMETRICS; NUCLEAR MAGNETIC RESONANCE IMAGING; PRESBYACUSIS; PRIORITY JOURNAL; STRIATE CORTEX; WHITE MATTER;

AC; AGING; AP; AUDITORY CORTEX; AUDITORY PATHWAY; AUDITORY PATHWAY ABOVE IC; DIFFUSION TENSOR IMAGING; DTI; ELDERLY SUBJECTS WITH EXPRESSED PRESBYCUSIS; ELDERLY SUBJECTS WITH MILD PRESBYCUSIS; EP; FA; FRACTIONAL ANISOTROPY; GFS; GM; GRAY MATTER; GYRUS FRONTALIS SUPERIOR; HESCHL'S GYRUS; HG; IC; INFERIOR COLLICULUS; MD; MEAN DIFFUSIVITY; MP; MR MORPHOMETRY; PLANUM TEMPORALE; PRESBYCUSIS; PT; REGION OF INTEREST; ROI; SENSORINEURAL HEARING LOSS; SNHL; V1; VISUAL CORTEX; WHITE MATTER; WHITE MATTER UNDER HESCHL'S GYRUS; WM; WM_HG; YC; YOUNG SUBJECTS WITH PHYSIOLOGIC HEARING/YOUNG CONTROLS;

ADULT; AGED; AGING; AUDITORY CORTEX; AUDITORY DISEASES, CENTRAL; AUDITORY PATHWAYS; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE FIBERS, MYELINATED; PRESBYCUSIS; YOUNG ADULT;

EID: 84891921508     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.12.010     Document Type: Article

References (87)

1. Aboitiz F., Rodriguez E., Olivares R., Zaidel E. Age-related changes in fibre composition of the human corpus callosum: sex differences. Neuroreport 1996, 7:1761-1764.
2. Alexander D.C., Pierpaoli C., Basser P.J., Gee J.C. Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans Med Imaging 2001, 20:1131-1139.
3. Anderson S., Parbery-Clark A., Yi H.G., Kraus N. A neural basis of speech-in-noise perception in older adults. Ear Hear 2011, 32:750-757.
4. Ashburner J., Friston K.J. Voxel-based morphometry - the methods. Neuroimage 2000, 11:805-821.
5. Balogová Z, Tintěra J, Profant O, Ibrahim I, Jílek M, Syka J (2013) Central presbycusis examined by fMRI. In: 11th EFAS congress (Kiss JG and Stephan K, eds), p 56. Budapest, Hungary.
6. Basser P.J., Jones D.K. Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review. NMR Biomed 2002, 15:456-467.
7. Basser P.J., Pajevic S., Pierpaoli C., Aldroubi A. Fiber tract following in the human brain using DT-MRI data. IEICE Trans Inf Syst 2002, E85D:15-21.
8. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 2002, 15:435-455.
9. Behrens T.E.J., Berg H.J., Jbabdi S., Rushworth M.F.S., Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. Neuroimage 2007, 34:144-155.
10. Bonner M.F., Grossman M. Gray matter density of auditory association cortex relates to knowledge of sound concepts in primary progressive aphasia. J Neurosci 2012, 32:7986-7991.
11. Bouma A., Gootjes L. Effects of attention on dichotic listening in elderly and patients with dementia of the Alzheimer type. Brain Cogn 2011, 76:286-293.
12. Boyen K., Langers D.R.M., de Kleine E., van Dijk P. Gray matter in the brain: differences associated with tinnitus and hearing loss. Hear Res 2013, 295:67-78.
13. Burianova J., Ouda L., Profant O., Syka J. Age-related changes in GAD levels in the central auditory system of the rat. Exp Gerontol 2009, 44:161-169.
14. Caspary D.M., Ling L., Turner J.G., Hughes L.F. Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 2008, 211:1781-1791.
15. Caspary D.M., Raza A., Armour B.A.L., Pippin J., Arneric S.P. Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus - implications for neural presbycusis. J Neurosci 1990, 10:2363-2372.
16. Chang Y.M., Lee S.H., Lee Y.J., Hwang M.J., Bae S.J., Kim M.N., Lee J.M., Woo S.K., Lee H.J., Kang D.S. Auditory neural pathway evaluation on sensorineural hearing loss using diffusion tensor imaging. Neuroreport 2004, 15:1699-1703.
17. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis - I. Segmentation and surface reconstruction. Neuroimage 1999, 9:179-194.
18. Dale A.M., Sereno M.I. Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction - a linear-approach. J Cogn Neurosci 1993, 5:162-176.
19. Desikan R.S., Segonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., Buckner R.L., Dale A.M., Maguire R.P., Hyman B.T., Albert M.S., Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006, 31:968-980.
20. Destrieux C., Fischl B., Dale A., Halgren E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 2010, 53:1-15.
21. du Boisgueheneuc F., Levy R., Volle E., Seassau M., Duffau H., Kinkingnehun S., Samson Y., Zhang S., Dubois B. Functions of the left superior frontal gyrus in humans: a lesion study. Brain 2006, 129:3315-3328.
22. Eggermont J.J. Differential-effects of age on click-rate and amplitude modulation-frequency coding in primary auditory-cortex of the cat. Hear Res 1993, 65:175-192.
23. Emmorey K., Allen J.S., Bruss J., Schenker N., Damasio H. A morphornetric analysis of auditory brain regions in congenitally deaf adults. Proc Natl Acad Sci U S A 2003, 100:10049-10054.
24. Firszt J.B., Ulmer J.L., Gaggl W. Differential representation of speech sounds in the human cerebral hemispheres. Anat Rec A Discov Mol Cell Evol Biol 2006, 288A:345-357.
25. Fischl B. FreeSurfer. Neuroimage 2012, 62:774-781.
26. Fischl B., Dale A.M. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 2000, 97:11050-11055.
27. Fischl B., Liu A., Dale A.M. Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. Ieee Transactions on Medical Imaging 2001, 20:70-80.
28. Fitch R.H., Miller S., Tallal P. Neurobiology of speech perception. Annu Rev Neurosci 1997, 20:331-353.
29. Gates G.A., Feeney M.P., Mills D. Cross-sectional age-changes of hearing in the elderly. Ear Hear 2008, 29:865-874.
30. Goldberg E., Roediger D., Kucukboyaci N.E., Carlson C., Devinsky O., Kuzniecky R., Halgren E., Thesen T. Hemispheric asymmetries of cortical volume in the human brain. Cortex 2013, 49:200-210.
31. Greve D.N., Fischl B. Accurate and robust brain image alignment using boundary-based registration. Neuroimage 2009, 48:63-72.
32. Groschel M., Gotze R., Ernst A., Basta D. Differential impact of temporary and permanent noise-induced hearing loss on neuronal cell density in the mouse central auditory pathway. J Neurotrauma 2010, 27:1499-1507.
33. Guo X.X., Skoog I., Idrizbegovic E., Pantoni L., Simoni M., Rosenhall U. Hearing loss and cortical atrophy in a population-based study on non-demented women. Age Ageing 2008, 37:333-336.
34. Heiervang E., Hugdahl K., Steinmetz H., Inge Smievoll A., Stevenson J., Lund A., Ersland L., Lundervold A. Planum temporale, planum parietale and dichotic listening in dyslexia. Neuropsychologia 2000, 38:1704-1713.
35. Helfert R.H., Sommer T.J., Meeks J., Hofstetter P., Hughes L.F. Age-related synaptic changes in the central nucleus of the inferior colliculus of Fischer-344 rats. J Comp Neurol 1999, 406:285-298.
36. Hickok G., Poeppel D. Opinion - the cortical organization of speech processing. Nat Rev Neurosci 2007, 8:393-402.
37. Humes L.E., Dubno J.R., Gordon-Salant S., Lister J.J., Cacace A.T., Cruickshanks K.J., Gates G.A., Wilson R.H., Wingfield A. Central presbycusis: a review and evaluation of the evidence. J Am Acad Audiol 2012, 23:635-666.
38. Husain F.T., Medina R.E., Davis C.W., Szymko-Bennett Y., Simonyan K., Pajor N.M., Horwitz B. Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res 2011, 1369:74-88.
39. Hwang J.H., Li C.W., Wu C.W., Chen J.H., Liu T.C. Aging effects on the activation of the auditory cortex during binaural speech listening in white noise: an fMRI study. Audiol NeuroOtol 2007, 12:285-294.
40. Jenkinson M., Beckmann C.F., Behrens T.E., Woolrich M.W., Smith S.M. FSL. Neuroimage 2012, 62:782-790.
41. Jezzard P., Balaban R.S. Correction for geometric distortion in echo-planar images from B-0 field variations. Magn Reson Med 1995, 34:65-73.
42. Lin Y., Wang J., Wu C., Wai Y., Yu J., Ng S. Diffusion tensor imaging of the auditory pathway in sensorineural hearing loss: changes in radial diffusivity and diffusion anisotropy. J Magn Reson Imaging 2008, 28:598-603.
43. Ling L.L., Hughes L.F., Caspary D.M. Age-related loss of the GABA synthetic enzyme glutamic acid decarboxylase in rat primary auditory cortex. Neuroscience 2005, 132:1103-1113.
44. Lunner T., Rudner M., Ronnberg J. Cognition and hearing aids. Scand J Psychol 2009, 50:395-403.
45. Lutz J., Hemminger F., Stahl R., Dietrich O., Hempel M., Reiser M., Jager L. Evidence of subcortical and cortical aging of the acoustic pathway: a diffusion tensor imaging (DTI) study. Acad Radiol 2007, 14:692-700.
46. Madden D.J., Bennett I.J., Burzynska A., Potter G.G., Chen N.K., Song A.W. Diffusion tensor imaging of cerebral white matter integrity in cognitive aging. Biochim Biophys Acta Mol Basis Dis 2012, 1822:386-400.
47. Madden D.J., Bennett I.J., Song A.W. Cerebral white matter integrity and cognitive aging: contributions from diffusion tensor imaging. Neuropsychol Rev 2009, 19:415-435.
48. Mazelová J., Popelar J., Syka J. Auditory function in presbycusis: peripheral vs. central changes. Exp Gerontol 2003, 38:87-94.
49. Mendelson J.R., Ricketts C. Age-related temporal processing speed deterioration in auditory cortex. Hear Res 2001, 158:84-94.
50. Miao W., Li J., Tang M., Xian J., Li W., Liu Z., Liu S., Sabel B.A., Wang Z., He H. Altered white matter integrity in adolescents with prelingual deafness: a high-resolution tract-based spatial statistics imaging study. AJNR Am J Neuroradiol 2013, 34(6):1264-1270.
51. Morris J.S., Friston K.J., Dolan R.J. Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proc Biol Sci 1998, 265:649-657.
52. Newman S.D., Twieg D. Differences in auditory processing of words and pseudowords: an fMRI study. Hum Brain Mapp 2001, 14:39-47.
53. Ouda L., Burianova J., Syka J. Age-related changes in calbindin and calretinin immunoreactivity in the central auditory system of the rat. Exp Gerontol 2012, 47:497-506.
54. Ouda L., Druga R., Syka J. Changes in parvalburnin immunoreactivity with aging in the central auditory system of the rat. Exp Gerontol 2008, 43:782-789.
55. Ouda L., Syka J. Immunocytochemical profiles of inferior colliculus neurons in the rat and their changes with aging. Frontiers in Neural Circuits 2012, 6(68):1-14.
56. Park D.C., Reuter-Lorenz P. The adaptive brain: aging and neurocognitive scaffolding. Annu Rev Psychol 2009, 60:173-196.
57. Penhune V.B., Cismaru R., Dorsaint-Pierre R., Petitto L.A., Zatorre R.J. The morphometry of auditory cortex in the congenitally deaf measured using MRI. Neuroimage 2003, 20:1215-1225.
58. Petitto L.A., Zatorre R.J., Gauna K., Nikelski E.J., Dostie D., Evans A.C. Speech-like cerebral activity in profoundly deaf people processing signed languages: implications for the neural basis of human language. Proc Natl Acad Sci U S A 2000, 97:13961-13966.
59. Pfefferbaum A., Sullivan E.V., Hedehus M., Lim K.O., Adalsteinsson E., Moseley M. Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn Reson Med 2000, 44:259-268.
60. Pichora-Fuller M.K., Souza P.E. Effects of aging on auditory processing of speech. Int J Audiol 2003, 42:S11-S16.
61. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RDC (2010) nlme: linear and nonlinear mixed effects models. In: R package, 3.1-97 Edition.
62. Profant O., Balogová Z., Dezortová M., Wagnerová D., Hájek M., Syka J. Metabolic changes in the auditory cortex in presbycusis demonstrated by MR spectroscopy. Exp Gerontol 2013, 48(8):795-800.
63. Radvansky G.A., Dijkstra K. Aging and situation model processing. Psychon Bull Rev 2007, 14:1027-1042.
64. Recanzone G.H., Engle J.R., Juarez-Salinas D.L. Spatial and temporal processing of single auditory cortical neurons and populations of neurons in the macaque monkey. Hear Res 2011, 271:115-122.
65. Rybalko N., Suta D., Nwabueze-Ogbo F., Syka J. Effect of auditory cortex lesions on the discrimination of frequency-modulated tones in rats. Eur J Neurosci 2006, 23:1614-1622.
66. Rybalko N., Suta D., Popelar J., Syka J. Inactivation of the left auditory cortex impairs temporal discrimination in the rat. Behav Brain Res 2010, 209:123-130.
67. Schirmer A., Fox P.M., Grandjean D. On the spatial organization of sound processing in the human temporal lobe: a meta-analysis. Neuroimage 2012, 63:137-147.
68. Schuknecht H.F., Gacek M.R. Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol 1993, 102:1-16.
69. Seeman M. Czech speech audiometry 1960, Státní zdravotnické nakladatelství, Prague.
70. Segonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., Fischl B. A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004, 22:1060-1075.
71. Segonne F., Pacheco J., Fischl B. Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 2007, 26:518-529.
72. Shafto M., Randall B., Stamatakis E.A., Wright P., Tyler L.K. Age-related neural reorganization during spoken word recognition: the interaction of form and meaning. J Cogn Neurosci 2012, 24:1434-1446.
73. Sharp D.J., Scott S.K., Mehra M.A., Wise R.J.S. The neural correlates of declining performance with age: evidence for age-related changes in cognitive control. Cereb Cortex 2006, 16:1739-1749.
74. Shibata D.K. Differences in brain structure in deaf persons on MR imaging studied with voxel-based morphometry. Am J Neuroradiol 2007, 28:243-249.
75. Sled J.G., Zijdenbos A.P., Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. Ieee Transactions on Medical Imaging 1998, 17:87-97.
76. Stebbins G.T., Murphy C.M. Diffusion tensor imaging in Alzheimer's disease and mild cognitive impairment. Behav Neurol 2009, 21:39-49.
77. Stenfelt S., Ronnberg J. The signal-cognition interface: interactions between degraded auditory signals and cognitive processes. Scand J Psychol 2009, 50:385-393.
78. Suta D., Rybalko N., Pelanova J., Popelar J., Syka J. Age-related changes in auditory temporal processing in the rat. Exp Gerontol 2011, 46:739-746.
79. Syka J. The Fischer 344 rat as a model of presbycusis. Hear Res 2010, 264:70-78.
80. Team R.D.C. R: a language and environment for statistical computing 2010, R Foundation for Statistical Computing, Vienna.
81. Toga A.W., Thompson P.M. Temporal dynamics of brain anatomy. Annu Rev Biomed Eng 2003, 5:119-145.
82. Tramo M.J., Cariani P.A., Koh C.K., Makris N., Braida L.D. Neurophysiology and neuroanatomy of pitch perception: auditory cortex. Neurosci Music II Percept Perform 2005, 1060:148-174.
83. Tulving E. Episodic memory: from mind to brain. Annu Rev Psychol 2002, 53:1-25.
84. Tyler L.K., Shafto M.A., Randall B., Wright P., Marslen-Wilson W.D., Stamatakis E.A. Preserving syntactic processing across the adult life span: the modulation of the frontotemporal language system in the context of age-related atrophy. Cereb Cortex 2010, 20:352-364.
85. Vermeij A., van Beek A., Rikkert M., Claassen J., Kessels R.P.C. Effects of aging on cerebral oxygenation during working-memory performance: a functional near-infrared spectroscopy study. PLoS One 2012, 7.
86. Walton J.P., Frisina R.D., O'Neill W.E. Age-related alteration in processing of temporal sound features in the auditory midbrain of the CBA mouse. J Neurosci 1998, 18:2764-2776.
87. Wong P.C.M., Ettlinger M., Sheppard J.P., Gunasekera G.M., Dhar S. Neuroanatomical characteristics and speech perception in noise in older adults. Ear Hear 2010, 31:471-479.