Age-related neurochemical changes in the rhesus macaque inferior colliculus

Frontiers in Aging Neuroscience

Volumn 6, Issue APR, 2014, Pages

  Engle, James R ^a,b,c   Gray, Daniel T ^b   Turner, Heather ^b   Udell, Julia B ^b   Recanzone, Gregg H ^b,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ADULT; AGE RELATED HEARING LOSS; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; AUDITORY THRESHOLD; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; HEARING IMPAIRMENT; IMMUNOREACTIVITY; INFERIOR COLLICULUS; MALE; NONHUMAN; PURE TONE AUDIOMETRY; RHESUS MONKEY; UPREGULATION;

EID: 84901317097     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00073     Document Type: Article

References (69)

1. Abel, S. M., Giguere, C., Consoli, A., Papsin, B. C. (2000a). The effect of aging on horizontal plane sound localization. J. Acoust. Soc. Am. 108, 743-752. doi: 10.1121/1.429607
2. Abel, S. M., Sass-Kortsak, A., and Naugler, J. J. (2000b). The role of high-frequency hearing in age-related speech understanding deficits. Scand. Audiol. 29, 131-138. doi: 10.1080/010503900750042699
3. Allen, A. R., and Starr, A. (1978). Auditory brain stem potentials in monkey (M. mulatta) and man. Electroencephalog. Clin. Neurophysiol. 45, 53-63. doi: 10.1016/0013-4694(78)90341-3
4. Bennett, C. L., Davis, R. T., and Miller, J. M. (1983). Demonstration of presbycusis across repeated measures in a nonhuman primate species. Behav. Neurosci. 97, 602-607. doi: 10.1037/0735-7044.97.4.602
5. Bredt, D. S., Glatt, C. E., Hwang, P. M., Fotuhi, M., Dawson, T. M., and Snyder, S. H. (1991). Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7, 615-624. doi: 10.1016/0896-6273(91)90374-9
6. Caicedo, A., D'Aldin, C., Eybalin, M., and Puel, J. L. (1997). Temporary sensory deprivation changes calcium-binding proteins levels in the auditory brainstem. J. Comp. Neurol. 378, 1-15. doi: 10.1002/(SICI)1096-9861(19970203)378:1%3C1::AID-CNE1%3E3.0.CO;2-8
7. Carder, R. K., Leclerc, S. S., and Hendry, S. H. (1996). Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex. Cereb. Cortex 6, 271-287. doi: 10.1093/cercor/6.2.271
8. Caspary, D. M., Holder, T. M., Hughes, L. F., Milbrandt, J. C., McKernan, R. M., and Naritoku, D. K. (1999). Age-related changes in GABA(A) receptor subunit composition and function in rat auditory system. Neuroscience 93, 307-312. doi: 10.1016/S0306-4522(99)00121-9
9. Caspary, D. M., Hughes, L. F., Schatteman, T. A., and Turner, J. G. (2006). Age-related changes in the response properties of cartwheel cells in rat dorsal cochlear nucleus. Hear. Res. 216-217, 207-215. doi: 10.1016/j.heares.2006.03.005
10. Caspary, D. M., Ling, L., Turner, J. G., and Hughes, L. F. (2008). Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J. Exp. Biol. 211, 1781-1791. doi: 10.1242/jeb.013581
11. Caspary, D. M., Milbrandt, J. C., and Helfert, R. H. (1995). Central auditory aging: GABA changes in the inferior colliculus. Exp. Gerontol. 30, 349-360. doi: 10.1016/0531-5565(94)00052-5
12. Caspary, D. M., Schatteman, T. A., and Hughes, L. F. (2005). Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs. J. Neurosci. 25, 10952-10959. doi: 10.1523/JNEUROSCI.2451-05.2005
13. Cauli, B., Audinat, E., Lambolez, B., Angulo, M. C., Ropert, N., Tsuzuki, K., et al. (1997). Molecular and physiological diversity of cortical nonpyramidal cells. J. Neurosci. 17, 3894-3906.
14. Davis, R. T., and Leathers, C. W. (1985). Behavior and Pathology of Aging in Rhesus Monkeys. New York, NY: A. R Liss.
15. Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M., and Snyder, S. H. (1991a). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. U.S.A. 88, 7797-7801. doi: 10.1073/pnas.88.17.7797
16. Dawson, V. L., Dawson, T. M., London, E. D., Bredt, D. S., and Snyder, S. H. (1991b). Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. U.S.A. 88, 6368-6371. doi: 10.1073/pnas.88.14.6368
17. de la Mothe, L. A., Blumell, S., Kajikawa, Y., and Hackett, T. A. (2006a). Cortical connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J. Comp. Neurol. 496, 27-71. doi: 10.1002/cne.20923
18. de la Mothe, L. A., Blumell, S., Kajikawa, Y., and Hackett, T. A. (2006b). Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J. Comp. Neurol. 496, 72-96. doi: 10.1002/cne.20924
19. de Villiers-Sidani, E., Alzghoul, L., Zhou, X., Simpson, K. L., Lin, R. C., and Merzenich, M. M. (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. doi: 10.1073/pnas.1007885107
20. Engle, J. R., and Recanzone, G. H. (2012). 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. doi: 10.3389/fnagi.2012.00036
21. Engle, J. R., Tinling, S., and Recanzone, G. H. (2013). Age-related hearing loss in rhesus monkeys is correlated with cochlear histopathologies. PLoS ONE 8:e55092. doi: 10.1371/journal.pone.0055092
22. Fowler, C. G., Chiasson, K. B., Leslie, T. H., Thomas, D., Beasley, T. M., Kemnitz, J. W., et al. (2010). Auditory function in rhesus monkeys: effects of aging and caloric restriction in the Wisconsin monkeys five years later. Hear. Res. 261, 75-81. doi: 10.1016/j.heares.2010.01.006
23. Fowler, C. G., Torre, P., Kemnitz, J. W. (2002). Effects of caloric restriction and aging on the auditory function of rhesus monkeys (Macaca mulatta): The University of Wisconsin Study. Hear. Res. 169, 24-35. doi: 10.1016/S0378-5955(02)00335-0
24. Fredich, M., Reisch, A., and Illing, R. B. (2009). Neuronal subtypes in the rat auditory brainstem as defined by molecular profile and axonal projection. Exp. Brain Res. 195, 241-260. doi: 10.1007/s00221-009-1776-7
25. Frisina, D. R., and Frisina, R. D. (1997). Speech recognition in noise and presbycusis: relations to possible neural mechanisms. Hear. Res. 106, 95-104. doi: 10.1016/S0378-5955(97)00006-3
26. Gibson, J. R., Beierlein, M., and Connors, B. W. (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79. doi: 10.1038/47035
27. Gray, D. T., Engle, J. R., and Recanzone, G. H. (2014a). Age-related neurochemical changes in the rhesus macaque superior olivary complex. J. Comp. Neurol. 522, 573-591. doi: 10.1002/cne.23427
28. Gray, D. T., Engle, J. R., and Recanzone, G. H. (2014b). Age-related neurochemical changes in the rhesus macaque cochlear nucleus. J. Comp. Neurol. 522, 1527-1541. doi: 10.1002/cne.23479
29. Gray, D. T., Rudolph, M. L., Engle, J. R., and Recanzone, G. H. (2013). Parvalbumin increases in the medial and lateral geniculate nuclei of aged rhesus macaques. Front. Aging. Res. 5:69. doi: 10.3389/fnagi.2013.00069
30. Groh, J. M., Kelly, K. A., and Underhill, A. M. (2003). A monotonic code for sound azimuth in primate inferior colliculus. J. Cogn. Neurosci. 15, 1217-1231. doi: 10.1162/089892903322598166
31. Hackett, T. A., Preuss, T. M., and Kaas, J. H. (2001). Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J. Comp. Neurol. 441, 197-222. doi: 10.1002/cne.1407
32. Harada, T., Tokuriki, M., and Tanioka, Y. (1999). Age-related changes in the brainstem auditory evoked potentials of the marmoset. Hear. Res. 128, 119-124. doi: 10.1016/S0378-5955(98)00201-9
33. Howard, C. V., and Reed, M. G. (2005). Unbiased Stereology. Abingdon: Garland Science/BIOS Scientific Publishers.
34. Huh, Y., Choon Park, D., Geun, Yeo, S., Cha II, C. (2008). Evidence for increased NADPH-diaphorase-positive neurons in the central auditory system of the aged rat. Acta Otolaryngol. 128, 648-653. doi: 10.1080/00016480701636868
35. Idrizbegovic, E., Bogdanovic, N., Viberg, A., and 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. doi: 10.1016/S0378-5955(03)00076-5
36. Idrizbegovic, E., Bogdanovic, N., Willott, J. F., and 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. doi: 10.1016/j.neurobiolaging.2003.11.004
37. Idrizbegovic, E., Salman, H., Niu, X., and Canlon, B. (2006). Presbyacusis and calcium-binding protein immunoreactivity in the cochlear nucleus of BALB/c mice. Hear. Res. 216-217, 198-206. doi: 10.1016/j.heares.2006.01.009
38. Jones, E. G. (2003). Chemically defined parallel pathways in the monkey auditory system. Ann. N.Y. Acad. Sci. 999, 218-233. doi: 10.1196/annals.1284.033
39. Juarez-Salinas, D. L., Engle, J. R., Navarro, X. O., and Recanzone, G. H. (2010). Hierarchical and serial processing in the spatial auditory cortical pathway is degraded by natural aging. J. Neurosci. 30, 14795-14804. doi: 10.1523/JNEUROSCI.3393-10.2010
40. Kaas, J. H., and Hackett, T. A. (2000). Subdivisions of auditory cortex and processing streams in primates. Proc. Natl. Acad. Sci. U.S.A. 97, 11793-11799. doi: 10.1073/pnas.97.22.11793
41. Kawaguchi, Y., Katsumaru, H., Kosaka, T., Heizmann, C. W., and Hama, K. (1987). Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416, 369-374. doi: 10.1016/0006-8993(87)90921-8
42. Kawaguchi, Y., and Kubota, Y. (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486. doi: 10.1093/cercor/7.6.476
43. Laughlin, N. K., Hartup, B. K., Lasky, R. E., Meier, M. M., and Hecox, K. E. (1999). The development of auditory event related potentials in the rhesus monkey (Macaca mulatta). Dev. Psychobiol. 34, 37-56. doi: 10.1002/(SICI)1098-2302(199901)34:1%3C37::AID-DEV6%3E3.3.CO;2-N
44. Loftus, W. C., Malmierca, M. S., Bishop, D. C., and Oliver, D. L. (2008). The cytoarchitecture of the inferior colliculus revisited: a common organization of the lateral cortex in rat and cat. Neurosci. 154, 196-205. doi: 10.1016/j.neuroscience.2008.01.019
45. Lohmann, C., and 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. doi: 10.1002/(SICI)1096-9861(19960325)367:1%3C90::AID-CNE7%3E3.0.CO;2-E
46. Maier, J. X., and Groh, J. M. (2010). Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates. Front. Integr. Neurosci. 4:121. doi: 10.3389/fnint.2010.00121
47. Mounton, P. R. (2002). Principles and Practices of Unbiased Stereology. Baltmore, MD: The Johns Hopkins University Press.
48. Oliver, D. L. (2005). "Neuronal organization in the inferior colliculus," in The Inferior Colliculus, eds J. A. Winer and C. E. Schreiner (New York, NY: Springer-Verlag). doi: 10.1007/0-387-27083-3_2
49. O'Neill, W. E., Zettel, M. L., Whittemore, K. R., and Frisina, R. D. (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.
50. Ouda, L., Druga, R., and Syka, J. (2008). Changes in parvalbumin immunoreactivity with aging in the central auditory system of the rat. Exp. Gerontol. 43, 782-789. doi: 10.1016/j.exger.2008.04.001
51. Ouda, L., Nwabueze-Ogbo, F. C., Druga, R., and Syka, J. (2003). NADPH-diaphorase-positive neurons in the auditory cortex of young and old rats. Neuroreport 14, 363-366. doi: 10.1097/00001756-200303030-00013
52. Padberg, J., Cerkevich, C., Engle, J., Rajan, A. T., Recanzone, G., Kaas, J., et al. (2009). Thalamocortical connections of parietal somatosensory cortical fields in macaque monkeys are highly divergent and convergent. Cereb. Cortex 19, 2038-2064. doi: 10.1093/cercor/bhn229
53. Parvizi, J., and Damasio, A. R. (2003). Differential distribution of calbindin D28k and parvalbumin among functionally distinctive sets of structures in the macaque brainstem. J. Comp. Neurol. 462, 153-167. doi: 10.1002/cne.10711
54. Petilla Interneuron Nomenclature, G., Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., Benavides-Piccione, R., et al. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568. doi: 10.1038/nrn2402
55. Rauschecker, J. P., and Tian, B. (2000). Mechanisms and streams for processing of "what" and "where" in auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 97, 11800-11806. doi: 10.1073/pnas.97.22.11800
56. Recanzone, G. H., Engle, J. R., and Juarez-Salinas, D. L. (2011). Spatial and temporal processing of single auditory cortical neurons and populations of neurons in the macaque monkey. Hear. Res. 271, 115-122. doi: 10.1016/j.heares.2010.03.084
57. Reuss, S., Schaeffer, D. F., Laages, M. H., and Riemann, R. (2000). Evidence for increased nitric oxide production in the auditory brain stem of the aged dwarf hamster (Phodopus sungorus): an NADPH-diaphorase histochemical study. Mech. Aging Dev. 112, 125-134. doi: 10.1016/S0047-6374(99)00082-2
58. Sanchez-Zuriaga, D., Marti-Gutierrez, N., De La Cruz, M. A., Peris-Sanchis, M. R. (2007). Age-related changes of NADPH-diaphorase-positive neurons in the rat inferior colliculus and auditory cortex. Microsc. Res. Tech. 70, 1051-1059. doi: 10.1002/jemt.20512
59. Scherer-Singler, U., Vincent, S. R., Kimura, H., and McGeer, E. G. (1983). Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Methods 9, 229-234. doi: 10.1016/0165-0270(83)90085-7
60. Schuknecht, H. F. (1964). Further observations on the pathology of presbycusis. Arch. Otolaryngol. 80, 369-382. doi: 10.1001/archotol.1964.00750040381003
61. Schuknecht, H. F., and Gacek, M. R. (1993). Cochlear pathology in presbycusis. Ann. Otol. Rhinol. Laryngol. 102, 1-16.
62. Smiley, J. F., McGinnis, J. P., and Javitt, D. C. (2000). Nitric oxide synthase interneurons in the monkey cerebral cortex are subsets of the somatostatin, neuropeptide Y, and calbindin cells. Brain Res. 863, 205-212. doi: 10.1016/S0006-8993(00)02136-3
63. Snell, K. B. (1997). Age-related changes in temporal gap detection. J. Acoust. Soc. Am. 101, 2214-2220. doi: 10.1121/1.418205
64. Soares-Mota, M., Henze, I., and Mendez-Otero, R. (2001). Nitric oxide synthase-positive neurons in the rat superior colliculus: colocalization of NOS with NMDAR1 glutamate receptor, GABA, and parvalbumin. J. Neurosci. Res. 64, 501-507. doi: 10.1002/jnr.1102
65. Torre, P., Fowler, C. G. (2000). Age-related changes in auditory function of rhesus monkeys (Macaca mulatta). Hear. Res. 142, 131-140. doi: 10.1016/S0378-5955(00)00025-3
66. Torre, P., Mattison, J. A., Fowler, C. G., Lane, M. A., Roth, G. S., Ingram, D. K. (2004). Assessment of auditory function in rhesus monkeys (Macaca mulatta): effects of age and calorie restriction. Neurobiol. Aging 25, 945-954. doi: 10.1016/j.neurobiolaging.2003.09.006
67. Xu, X., and Callaway, E. M. (2009). Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J. Neurosci. 29, 70-85. doi: 10.1523/JNEUROSCI.4104-08.2009
68. Yan, X. X., Jen, L. S., and Garey, L. J. (1996). NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb. Cortex 6, 524-529. doi: 10.1093/cercor/6.3.524
69. Zettel, M. L., Frisina, R. D., Haider, S. E., and O'Neill, W. E. (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.