Development of myelination and cholinergic innervation in the central auditory system of a prosimian primate (Otolemur garnetti)

Journal of Comparative Neurology

Volumn 521, Issue 16, 2013, Pages 3804-3816

  Miller, Daniel J ^a   Lackey, Elizabeth P ^a   Hackett, Troy A ^a   Kaas, Jon H ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Acetylcholine; Comparative anatomy; Myelin; Neocortex; Ontogeny

Indexed keywords

ACETYLCHOLINESTERASE;

ADULTHOOD; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; BIRTH; INFERIOR COLLICULUS; MEDIAL GENICULATE BODY; MYELINATED NERVE; MYELINATION; NEOCORTEX; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OTOLEMUR GARNETTI; PARASYMPATHETIC INNERVATION; POSTNATAL DEVELOPMENT; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECIES DIFFERENCE;

ACETYLCHOLINE; COMPARATIVE ANATOMY; MYELIN; NEOCORTEX; ONTOGENY;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; AUDITORY CORTEX; AUDITORY PATHWAYS; BRAIN MAPPING; CELL COUNT; GENICULATE BODIES; INFERIOR COLLICULI; MYELIN SHEATH; STEREOTAXIC TECHNIQUES; STREPSIRHINI;

EID: 84892835466     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23379     Document Type: Article

References (81)

1. Abraham H, Vincze A, Jewgenow I, Veszpremi B, Kravjak A, Gomori E, Seress L. 2010. Myelination in the human hippocampal formation from midgestation to adulthood. Int J Dev Neurosci 28:401-410.
2. Aubert I, Cecyre D, Gauthier S, Quirion R. 1996. Comparative ontogenic profile of cholinergic markers, including nicotinic and muscarinic receptors, in the rat brain. J Comp Neurol 369:31-55.
3. Bartus RT, Dean RL 3rd, Beer B, Lippa AS. 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-414.
4. Benes FM. 1989. Myelination of cortical-hippocampal relays during late adolescence. Schizophr Bull 15:585-593.
5. Bock NA, Hashim E, Kocharyan A, Silva AC. 2011. Visualizing myeloarchitecture with magnetic resonance imaging in primates. Ann N Y Acad Sci 1225-1228.
6. Bogin B. 1999. Evolutionary perspective on human growth. Annu Rev Anthropol 28:109-153.
7. Brody BA, Kinney HC, Kloman AS, Gilles FH. 1987. Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol 46:283-301.
8. Coyle JT, Yamamura HI. 1976. Neurochemical aspects of the ontogenesis of cholinergic neurons in the rat brain. Brain Res 118:429-440.
9. Davies P, Maloney AJ. 1976. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2:1403.
10. Davison AN, Dobbing J. 1966. Myelination as a vulnerable period in brain development. Br Med Bull 22:40-44.
11. Deacon TW. 1997. What makes the human brain different. Annu Rev Anthropol 26:337-357.
12. Deoni SC, Mercure E, Blasi A, Gasston D, Thomson A, Johnson M, Williams SC, Murphy DG. 2011. Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 31:784-791.
13. Descarries L, Aznavour N, Hamel E. 2005. The acetylcholine innervation of cerebral cortex: new data on its normal development and its fate in the hAPP(SW, IND) mouse model of Alzheimer's disease. J Neural Transm 112:149-162.
14. Ehrlich A. 1974. Infant development in two prosimian species: greater galago and slow loris. Dev Psychobiol 7:439-454.
15. Fields RD. 2010. Neuroscience. Change in the brain's white matter. Science 330:768-769.
16. Flechsig P. 1901. Developmental (myelogenetic) localization of the cerebral cortex in the human subject. Lancet 2: 1027-1029.
17. Foehring RC, Lorenzon NM. 1999. Neuromodulation, development and synaptic plasticity. Can J Exp Psychol 53:45-61.
18. Gallyas F. 1971. A principle for silver staining of tissue elements by physical development. Acta Morphol Acad Sci Hung 19:57-71.
19. Geneser-Jensen FA, Blackstad TW. 1971. Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, parasubiculum, and presubiculum. Z Zellforsch Mikrosk Anat 114:460-481.
20. Gibson KR. 1970. Sequence of myelinization in the brain of Macaca mulatta. University of California, Berkeley. Gilles FH. 1976. Myelination in the neonatal brain. Hum Pathol 7:244-248.
21. Gilles FH. 1976. Myelination in the neonatal brain. Hum Pathol 7:244-248.
22. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF 3rd, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM. 2004. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101: 8174-8179.
23. Gorry JD. 1963. Studies on the comparative anatomy of the ganglion basale of Meynert. Acta Anat (Basel) 55:51-104.
24. Hackett TA, Stepniewska I, Kaas JH. 1998. Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol 392:475-495.
25. Hackett TA, Preuss TM, Kaas JH. 2001. Architectonic identification of the core region in auditory cortex of macaques, chimpanzees and humans. J Comp Neurol 441:197-222.
26. Hamano K, Iwasaki N, Takeya T, Takita H. 1996. A quantitative analysis of rat central nervous system myelination using the immunohistochemical method for MBP. Brain Res Dev Brain Res 93:18-22.
27. Hamano K, Takeya T, Iwasaki N, Nakayama J, Ohto T, Okada Y. 1998. A quantitative study of the progress of myelination in the rat central nervous system, using the immunohistochemical method for proteolipid protein. Brain Res Dev Brain Res 108:287-293.
28. Heckers S, Geula C, Mesulam MM. 1992. Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J Comp Neurol 325:68-82.
29. Hohmann CF, Ebner FF. 1985. Development of cholinergic markers in mouse forebrain. I. Choline acetyltransferase enzyme activity and acetylcholinesterase histochemistry. Brain Res 355:225-241.
30. Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD. 2006. Astrocytes promote myelination in response to electrical impulses. Neuron 49:823-832.
31. Kaas JH. 2012. The evolution of neocortex in primates. Prog Brain Res 195:91-102.
32. Kennedy GE. 2005. From the ape's dilemma to the weanling's dilemma: early weaning and its evolutionary context. J Hum Evol 48:123-145.
33. Kinney HC, Brody BA, Kloman AS, Gilles FH. 1988. Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants. J Neuropathol Exp Neurol 47:217-234.
34. Knickmeyer RC, Gouttard S, Kang C, Evans D, Wilber K, Smith JK, Hamer RM, Lin W, Gerig G, Gilmore JH. 2008. A structural MRI study of human brain development from birth to 2 years. J Neurosci 28:12176-12182.
35. Knickmeyer RC, Styner M, Short SJ, Lubach GR, Kang C, Hamer R, Coe CL, Gilmore JH. 2010. Maturational trajectories of cortical brain development through the pubertal transition: unique species and sex differences in the monkey revealed through structural magnetic resonance imaging. Cereb Cortex 20:1053-1063.
36. Kostovic I, Goldman-Rakic PS. 1983. Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 219:431-447.
37. Krmpotic-Nemanic J, Kostovic I, Kelovic Z, Nemanic D, Mrzljak L. 1983. Development of the human fetal auditory cortex: growth of afferent fibres. Acta Anat (Basel) 116:69-73.
38. Krubitzer LA, Kaas JH. 1990. Cortical connections of MT in four species of primates: areal, modular, and retinotopic patterns. Vis Neurosci 5:165-204.
39. Langworthy OR. 1933. Development of behavior patterns and myelination of the nervous system in the human fetus and infant. In: Contributions to embryology, vol. XXVI. Washington, DC: Carnegie Institute of Washington. p 1-57.
40. Leigh SR. 2004. Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 62:139-164.
41. Leigh SR, Park PB. 1998. Evolution of human growth prolongation. Am J Phys Anthropol 107:331-350.
42. Levitt P. 2003. Structural and functional maturation of the developing primate brain. J Pediatr 143(4 Suppl):S35-45.
43. Li SC. 2012. Neuromodulation of behavioral and cognitive development across the life span. Dev Psychol 48:810-814.
44. Looney GA, Elberger AJ. 1986. Myelination of the corpus callosum in the cat: time course, topography, and functional implications. J Comp Neurol 248:336-347.
45. Lucas-Meunier E, Fossier P, Baux G, Amar M. 2003. Cholinergic modulation of the cortical neuronal network. Pflugers Arch 446:17-29.
46. Makinodan M, Rosen KM, Ito S, Corfas G. 2012. A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337:1357-1360.
47. Matsuoka T, Sumiyoshi T, Tsunoda M, Takasaki I, Tabuchi Y, Uehara T, Itoh H, Suzuki M, Kurachi M. 2010. Change in the expression of myelination/oligodendrocyte-related genes during puberty in the rat brain. J Neural Transm 117:1265-1268.
48. Metherate R, Hsieh CY. 2003. Regulation of glutamate synapses by nicotinic acetylcholine receptors in auditory cortex. Neurobiol Learn Mem 80:285-290.
49. Miller DJ, Duka T, Stimpson CD, Schapiro SJ, Baze WB, McArthur MJ, Fobbs AJ, Sousa AM, Sestan N, Wildman DE, Lipovich L, Kuzawa CW, Hof PR, Sherwood CC. 2012. Prolonged myelination in human neocortical evolution. Proc Natl Acad Sci U S A 109:16480-16485.
50. Moore DR. 1985. Postnatal development of the mammalian central auditory system and the neural consequences of auditory deprivation. Acta Otolaryngol Suppl 421:19-30.
51. Moore JK, Guan YL. 2001. Cytoarchitectural and axonal maturation in human auditory cortex. J Assoc Res Otolaryngol 2:297-311.
52. Moore JK, Linthicum FH Jr. 2007. The human auditory system: a timeline of development. Int J Audiol 46:460-478.
53. Moore JK, Perazzo LM, Braun A. 1995. Time course of axonal myelination in the human brainstem auditory pathway. Hear Res 87:21-31.
54. Moore JK, Ponton CW, Eggermont JJ, Wu BJ, Huang JQ. 1996. Perinatal maturation of the auditory brain stem response: changes in path length and conduction velocity. Ear Hear 17:411-418.
55. Moore JK, Guan YL, Shi SR. 1997. Axogenesis in the human fetal auditory system, demonstrated by neurofilament immunohistochemistry. Anat Embryol (Berl) 195:15-30.
56. Morel A, Kaas JH. 1992. Subdivisions and connections of auditory cortex in owl monkeys. J Comp Neurol 318:27-63.
57. Morel A, Garraghty PE, Kaas JH. 1993. Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys. J Comp Neurol 335:437-459.
58. Mouton PR, Gokhale AM, Ward NL, West MJ. 2002. Stereological length estimation using spherical probes. J Microsc 206(Pt 1):54-64.
59. Nadler JV, Cotman CW, Lynch GS. 1973. Altered distribution of choline acetyltransferase and acetylcholinesterase activities in the developing rat dentate gyrus following entorhinal lesion. Brain Res 63:215-220.
60. Preuss TM, Goldman-Rakic PS. 1991. Myelo-and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. J Comp Neurol 310:429-474.
61. Raghanti MA, Simic G, Watson S, Stimpson CD, Hof PR, Sherwood CC. 2011. Comparative analysis of the nucleus basalis of Meynert among primates. J Neurosci 16:1-15.
62. Robertson RT, Mostamand F, Kageyama GH, Gallardo KA, Yu J. 1991. Primary auditory cortex in the rat: transient expression of acetylcholinesterase activity in developing geniculocortical projections. Brain Res Dev Brain Res 58: 81-95.
63. Ruediger T, Bolz J. 2007. Neurotransmitters and the development of neuronal circuits. Adv Exp Med Biol 621:104-105.
64. Sakai T, Hirata S, Fuwa K, Sugama K, Kusunoki K, Makishima H, Eguchi T, Yamada S, Ogihara N, Takeshita H. 2012. Fetal brain development in chimpanzees versus humans. Curr Biol 22:R791-791.
65. Sano M, Kaga K, Kuan CC, Ino K, Mima K. 2007. Early myelination patterns in the brainstem auditory nuclei and pathway: MRI evaluation study. Int J Pediatr Otorhinolaryngol 71:1105-1115.
66. Sano M, Kuan CC, Kaga K, Itoh K, Ino K, Mima K. 2008. Early myelination patterns in the central auditory pathway of the higher brain: MRI evaluation study. Int J Pediatr Otorhinolaryngol 72:1479-1486.
67. Semba K. 2004. Phylogenetic and ontogenetic aspects of the basal forebrain cholinergic neurons and their innervation of the cerebral cortex. Prog Brain Res 145:3-43.
68. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, Greenstein D, Clasen L, Evans A, Rapoport JL, Giedd JN, Wise SP. 2008. Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28:3586-3594.
69. Sherwood CC, Gordon AD, Allen JS, Phillips KA, Erwin JM, Hof PR, Hopkins WD. 2011. Aging of the cerebral cortex differs between humans and chimpanzees. Proc Natl Acad Sci U S A 108:13029-13034.
70. Shi Y, Short SJ, Knickmeyer RC, Wang J, Coe CL, Niethammer M, Gilmore JH, Zhu H, Styner MA. 2013. Diffusion tensor imaging-based characterization of brain neurodevelopment in primates. Cereb Cortex 23:36-48.
71. Shideler KK, Yan J. 2010. M1 muscarinic receptor for the development of auditory cortical function. Mol Brain 3:29.
72. Simons M, Trajkovic K. 2006. Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis. J Cell Sci 119(Pt 21):4381-4389.
73. Simons M, Trotter J. 2007. Wrapping it up: the cell biology of myelination. Curr Opin Neurobiol 17:533-540.
74. Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW. 2003. Mapping cortical change across the human life span. Nat Neurosci 6:309-315.
75. Stevens B, Porta S, Haak LL, Gallo V, Fields RD. 2002. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36: 855-868.
76. Takahashi E, Dai G, Rosen GD, Wang R, Ohki K, Folkerth RD, Galaburda AM, Wedeen VJ, Ellen Grant P. 2011. Developing neocortex organization and connectivity in cats revealed by direct correlation of diffusion tractography and histology. Cereb Cortex 21:200-211.
77. Wake H, Lee PR, Fields RD. 2011. Control of local protein synthesis and initial events in myelination by action potentials. Science 333:1647-1651.
78. Watson RE, Desesso JM, Hurtt ME, Cappon GD. 2006. Postnatal growth and morphological development of the brain: a species comparison. Birth Defects Res B Dev Reprod Toxicol 77:471-484.
79. Waxman SG. 1977. Conduction in myelinated, unmyelinated, and demyelinated fibers. Arch Neurol 34:585-589.
80. Yakovlev PL, Lecours AR. 1967. The myelogenetic cycles of regional maturation of the brain. In: Minkowski A, editor. Regional development of the brain in early life. Oxford, UK: Blackwell Publishers. p 3-70.
81. Zhang ZW. 2006. Canadian Association of Neurosciences review: postnatal development of the mammalian neocortex: role of activity revisited. Can J Neurol Sci 33:158-169.