Advertisement

Brain Structure and Function

, Volume 217, Issue 2, pp 303–321 | Cite as

Expression of medium and heavy chain neurofilaments in the developing human auditory cortex

  • Arvind Singh Pundir
  • L. Shahul Hameed
  • P. C. Dikshit
  • Praveen Kumar
  • Surender Mohan
  • Bishan Radotra
  • S. K. Shankar
  • Anita Mahadevan
  • Soumya IyengarEmail author
Original Article

Abstract

Neurofilament medium (NF-M) and heavy (NF-H) chain proteins have been used as markers for maturity in the developing brain since their accumulation in axons leads to an increase in conduction velocity. Earlier studies have demonstrated immunoreactivity of neurofilaments in Layer I of the human auditory cortex at 22 gestation weeks (GW), whereas that in other layers developed between 1 and 12 postnatal years, suggesting a gradual increase in the processing of sounds. However, third trimester fetuses and infants are fairly sophisticated in their ability to discern different aspects of complex sounds. Given these contradictory findings, we decided to study the expression of neurofilaments in human auditory cortex between 15 GW and adulthood. We found that mRNA and protein for both NF-M and NF-H were present in the presumptive human auditory cortex in the second trimester and during the postnatal period (1 year—adulthood). Axons in all layers of the auditory cortex were immunoreactive for neurofilaments by 25 GW and the density of the neurofilament-rich plexus in the cortical wall became adult-like during the first postnatal year in humans (9 postnatal months). Our results suggest that in terms of neurofilament expression, axons within the preterm human auditory cortex may be more mature than previously thought.

Keywords

Auditory cortex Fetal human brain Heavy chain neurofilament protein Heschl’s gyrus Immunohistochemistry for SMI-312 and SMI-31 Medium chain neurofilament protein 

Notes

Acknowledgments

This work was supported by intramural funds from the National Brain Research Centre, Manesar. The authors gratefully acknowledge the support provided by Prof. V Ravindranath (IISc, Bangalore, former Director, NBRC), Dr. TS Rao (Director, DBT), and Dr. OP Sharma for setting up the collection of postmortem tissue at NBRC, Ram Mehar (NBRC, Manesar) for technical support and Nikhil Ahuja and Neha Sehgal (NBRC, Manesar) for help with the methods.

Supplementary material

429_2011_352_MOESM1_ESM.tif (5.3 mb)
Supplementary Figure 1 Negative controls for immunohistochemistry using SMI-312 and SMI-31 demonstrate the absence of staining in coronal sections of the Heschl’s gyrus at 15GW, 25GW, 32GW, 40GW, 9 postnatal months and an adult (36 yr). Scale bar = 20 μm. (TIFF 5,475 kb)

References

  1. Antonini A, Stryker MP (1993) Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J Neurosci 13:3549–3573PubMedGoogle Scholar
  2. Bayer SA, Altman J (2005a) The Human Brain during the Second Trimester, Atlas of Human Central Nervous System Development, vol. 3, CRC Press (Taylor and Francis group), FloridaGoogle Scholar
  3. Bayer SA, Altman J (2005b) The Human Brain during the Third Trimester, Atlas of Human Central Nervous System Development, vol. 2, CRC Press (Taylor and Francis group), Florida USAGoogle Scholar
  4. Boulder Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257–261CrossRefGoogle Scholar
  5. Bourne JA, Rosa MG (2006) Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT). Cereb Cortex 16(3):405–414PubMedCrossRefGoogle Scholar
  6. Bourne JA, Warner CE, Rosa MG (2005) Topographic and laminar maturation of striate cortex in early postnatal marmoset monkeys, as revealed by neurofilament immunohistochemistry. Cereb Cortex 15(6):740–748PubMedCrossRefGoogle Scholar
  7. Burkhalter A, Bernardo KL, Charles V (1993) Development of local circuits in human visual cortex. J Neurosci 13:1916–1931PubMedGoogle Scholar
  8. Cheour M, Alho K, Ceponiene R, Reinikainen K, Sainio K, Pohjavuori M, Aaltonen ONäätänen R (1998) Maturation of the mismatch negativity in infants. Int J Psychophysiol 29:217–226PubMedCrossRefGoogle Scholar
  9. Cheour-Luhtanen M, Alho K, Kujala T, Sainio K, Reinikainen K, Renlund M, Aaltonen O, Eerola O, Naatanen R (1995) Mismatch negativity indicates vowel discrimination in newborns. Hear Res 82:53–58PubMedCrossRefGoogle Scholar
  10. Cheour-Luhtanen M, Alho K, Sainio K, Rinne T, Reinikainen K, Pohjavuori M, Renlund M, Aaltonen O, Eerola O, Näätänen R (1996) The ontogenetically earliest discriminative response of the human brain. Psychophysiology 33(4):478–481PubMedCrossRefGoogle Scholar
  11. Cheour-Luhtanen M, Alho K, Sainio K, Reinikainen K, Renlund M, Aaltonen O, Eerola O, Näätänen R (1997) The mismatch negativity to speech sounds at the age of three months. Dev Neuropsychol 13:167–174CrossRefGoogle Scholar
  12. Chiry O, Tardif E, Magistretti PJ, Clarke S (2003) Patterns of calcium-binding proteins support parallel and hierarchical organization of human auditory areas. Eur J Neurosci 17:397–410PubMedCrossRefGoogle Scholar
  13. Dehaene-Lambertz G, Dehaene S, Hertz-Pannier L (2002) Functional neuroimaging of speech perception in infants. Science 298:201–205CrossRefGoogle Scholar
  14. Draganova R, Eswaran H, Murphy P, Huotilainen M, Lowery C, Preissl H (2005) Sound frequency change detection in fetuses and newborns, a magnetoencephalographic study. Neuroimage 28:354–361PubMedCrossRefGoogle Scholar
  15. Draganova R, Eswaran H, Murphy P, Lowery C, Preissl H (2007) Serial magnetoencephalographic study of fetal and newborn auditory discriminative evoked responses. Early Hum Dev 83:199–207PubMedCrossRefGoogle Scholar
  16. Dubois J, Hertz-Pannier L, Dehaene-Lambertz G, Cointepas Y, Le Bihan D (2006) Assessment of the early organization and maturation of infants’ cerebral white matter fiber bundles: a feasibility study using quantitative diffusion tensor imaging and tractography. NeuroImage 30:1121–1132PubMedCrossRefGoogle Scholar
  17. Escurat M, Djabali K, Gumpel M, Gros F, Portier MM (1990) Differential expression of two neuronal intermediate-filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat. J Neurosci 10:764–784PubMedGoogle Scholar
  18. Garcia ML, Lobsiger CS, Shah SB, Deerinck TJ, Crum J, Young D, Ward CM, Crawford TO, Gotow T, Uchiyama Y, Ellisman MH, Calcutt NA, Cleveland DW (2003) NF-M is an essential target for the myelin-directed “outside-in” signaling cascade that mediates radial axonal growth. J Cell Biol 163:1011–1020PubMedCrossRefGoogle Scholar
  19. Garcia ML, Rao MV, Fujimoto J, Garcia VB, Shah SB, Crum J, Gotow T, Uchiyama Y, Ellisman M, Calcutt NA, Cleveland DW (2009) Phosphorylation of highly conserved neurofilament medium KSP repeats is not required for myelin-dependent radial axonal growth. J Neurosci 29:1277–1284PubMedCrossRefGoogle Scholar
  20. Groome LJ, Mooney DM, Holland SB, Smith LA, Atterbury JL, Dykman RA (1999) Behavioral state affects heart rate response to low-intensity sound in human fetuses. Early Hum Dev 54:39–54PubMedCrossRefGoogle Scholar
  21. Hashikawa T, Molinari M, Rausell E, Jones EG (1995) Patchy and laminar termination of medial geniculate axons in monkey auditory cortex. J Comp Neurol 362:195–208PubMedCrossRefGoogle Scholar
  22. Haynes RL, Borenstein NS, Desilva TM, Folkerth RD, Liu LG, Volpe JJ, Kinney HC (2005) Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol 484:156–167PubMedCrossRefGoogle Scholar
  23. Hevner RF (2000) Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J Neuropathol Exp Neurol 59:385–392PubMedGoogle Scholar
  24. Hilbig H, Bidmon HJ, Oppermann OT, Remmerbach T (2004) Influence of post-mortem delay and storage temperature on the immunohistochemical detection of antigens in the CNS of mice. Exp Toxicol Pathol 56:159–171PubMedCrossRefGoogle Scholar
  25. Hirokawa N, Glicksman MA, Willard MB (1984) Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J Cell Biol 98:1523–1536PubMedCrossRefGoogle Scholar
  26. Hoffman PN, Lasek RJ (1975) The slow component of axonal transport. Identification of major structural polypeptides of the axon and their generality among mammalian neurons. J Cell Biol 66:351–366PubMedCrossRefGoogle Scholar
  27. Holst M, Eswaran H, Lowery C, Murphy P, Norton J, Preissl H (2005) Development of auditory evoked fields in human fetuses and newborns: a longitudinal MEG study. Clin Neurophysiol 116:1949–1955PubMedCrossRefGoogle Scholar
  28. Iyengar S, Bottjer SW (2002) Development of individual axon arbors in a thalamocortical circuit necessary for song learning in zebra finches. J Neurosci 22:901–911PubMedGoogle Scholar
  29. Jacoby RA, Marshak DW (2000) Synaptic connections of DB3 diffuse bipolar cell axons in macaque retina. J Comp Neurol 416:19–29PubMedCrossRefGoogle Scholar
  30. Jardri R, Pins D, Thomas P (2008) A case of fMRI-guided rTMS treatment of coenesthetic hallucinations. Am J Psychiatry 165:1490–1491PubMedCrossRefGoogle Scholar
  31. Judas M, Rados M, Jovanov-Milosevic N, Hrabac P, Stern-Padovan R, Kostovic I (2005) Structural, immunocytochemical, and mr imaging properties of periventricular crossroads of growing cortical pathways in preterm infants. AJNR Am J Neuroradiol 26:2671–2684PubMedGoogle Scholar
  32. Kisilevsky BS, Muir DW, Low JA (1992) Maturation of human fetal responses to vibroacoustic stimulation. Child Dev 63:1497–1508PubMedCrossRefGoogle Scholar
  33. Kisilevsky BS, Hains SM, Lee K, Xie X, Huang H, Ye HH, Zhang K, Wang Z (2003) Effects of experience on fetal voice recognition. Psychol Sci 14:220–224PubMedCrossRefGoogle Scholar
  34. Kostovic I, Jovanov-Milosevic N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fetal Neonatal Med 11:415–422PubMedCrossRefGoogle Scholar
  35. Kostovic I, Judas M (2010) The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 99:1119–1127PubMedCrossRefGoogle Scholar
  36. Kostovic I, Judas M, Rados M, Hrabac P (2002) Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 12:536–544PubMedCrossRefGoogle Scholar
  37. Kriz J, Zhu Q, Julien JP, Padjen AL (2000) Electrophysiological properties of axons in mice lacking neurofilament subunit genes: disparity between conduction velocity and axon diameter in absence of NF-H. Brain Res 885:32–44PubMedCrossRefGoogle Scholar
  38. Krmpotic-Nemanic J, Kostovic I, Kelovic Z, Nemanic D (1980) Development of acetylcholinesterase (AChE) staining in human fetal auditory cortex. Acta Otolaryngol 89:388–392PubMedCrossRefGoogle Scholar
  39. 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) 116:69–73CrossRefGoogle Scholar
  40. Kuhl PK (2004) Early language acquisition: cracking the speech code. Nat Rev Neurosci 5:831–843PubMedCrossRefGoogle Scholar
  41. Kushnerenko E, Ceponiene R, Balan P, Fellman V, Huotilainen M, Naatanen R (2002) Maturation of the auditory event-related potentials during the 1st year of life. Neuroreport 13:47–51PubMedCrossRefGoogle Scholar
  42. Lee MK, Cleveland DW (1996) Neuronal intermediate filaments. Annu Rev Neurosci 19:187–217PubMedCrossRefGoogle Scholar
  43. Marin-Padilla M (1990) Three-dimensional structural organization of layer I of the human cerebral cortex: a Golgi study. J Comp Neurol 299:89–105PubMedCrossRefGoogle Scholar
  44. Marin-Padilla M (1992) Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J Comp Neurol 321:223–240PubMedCrossRefGoogle Scholar
  45. Martin R, Door R, Ziegler A, Warchol W, Hahn J, Breitig D (1999) Neurofilament phosphorylation and axon diameter in the squid giant fibre system. Neuroscience 88:327–336PubMedCrossRefGoogle Scholar
  46. Mehler J, Jusczyk P, Lambertz G, Halsted N, Bertoncini J, Amiel-Tison C (1988) A precursor of language acquisition in young infants. Cognition 29:143–178PubMedCrossRefGoogle Scholar
  47. Moore JK (2002) Maturation of human auditory cortex: implications for speech perception. Ann Otol Rhinol Laryngol Suppl 189:7–10PubMedGoogle Scholar
  48. Moore JK, Guan YL (2001) Cytoarchitectural and axonal maturation in human auditory cortex. J Assoc Res Otolaryngol 2:297–311PubMedCrossRefGoogle Scholar
  49. Moore JK, Linthicum FH Jr (2007) The human auditory system: a timeline of development. Int J Audiol 46(9):460–478PubMedCrossRefGoogle Scholar
  50. Moore JK, Perazzo LM, Braun A (1995) Time course of axonal myelination in the human brainstem auditory pathway. Hear Res 87:21–31PubMedCrossRefGoogle Scholar
  51. Moore JK, Guan YL, Shi SR (1997) Axogenesis in the human fetal auditory system, demonstrated by neurofilament immunohistochemistry. Anat Embryol (Berl) 195:15–30CrossRefGoogle Scholar
  52. Morlet T, Lapillonne A, Ferber C, Duclaux R, Sann L, Putet G, Salle B, Collet L (1995) Spontaneous Otoacoustic emissions in preterm neonates: prevalence and gender effects. Hear Res 90(1–2):44–54PubMedCrossRefGoogle Scholar
  53. Ohara O, Gahara Y, Miyake T, Teraoka H, Kitamura T (1993) Neurofilament deficiency in quail caused by nonsense mutation in neurofilament-L gene. J Cell Biol 121:387–395PubMedCrossRefGoogle Scholar
  54. Pasman JW, Rotteveel JJ, de Graaf R, Maassen B, Notermans SLH (1991) Detectability of auditory evoked response components in preterm infants. Early Hum Dev 26:129–141PubMedCrossRefGoogle Scholar
  55. Pasman JW, Rotteveel JJ, de Graaf R, Stegeman DF, Visco YM (1992) The effect of preterm birth on brainstem, middle latency and cortical auditory evoked responses (BMC AERs). Early Hum Dev 31:113–129PubMedCrossRefGoogle Scholar
  56. Paulussen M, Jacobs S, Van der Gucht E, Hof PR, Arckens L (2011) Cytoarchitecture of the mouse neocortex revealed by the low-molecular-weight neurofilament protein subunit. Brain Struct Funct. doi: 10.1007/s00429-011-0311-3
  57. Plioplys AV, Gravel C, Hawkes R (1986) Selective suppression of neurofilament antigen expression in the hypothyroid rat cerebral cortex. J Neurol Sci 75:53–68PubMedCrossRefGoogle Scholar
  58. Ponton CW, Moore JK, Eggermont JJ (1996) Auditory brain stem response generation by parallel pathways: differential maturation of axonal conduction time and synaptic transmission. Ear Hear 17:402–410PubMedCrossRefGoogle Scholar
  59. Pujol J, Soriano-Mas C, Ortiz H, Sebastia′n-Galle′s N, Losilla JM, Deus J (2006) Myelination of language-related areas in the developing brain. Neurology 66:339–343PubMedCrossRefGoogle Scholar
  60. Querleu D, Renard X, Boutteville C, Crepin G (1989) Hearing by the human fetus? Semin Perinatol 13:409–420PubMedGoogle Scholar
  61. Radnikow G, Feldmeyer D, Lubke J (2002) Axonal projection, input and output synapses, and synaptic physiology of Cajal-Retzius cells in the developing rat neocortex. J Neurosci 22:6908–6919PubMedGoogle Scholar
  62. Ramus F, Hauser MD, Miller C, Morris D, Mehler J (2000) Language discrimination by human newborns and by cotton-top tamarin monkeys. Science 288:349–351PubMedCrossRefGoogle Scholar
  63. Rao MV, Garcia ML, Miyazaki Y, Gotow T, Yuan A, Mattina S, Ward CM, Calcutt NA, Uchiyama Y, Nixon RA, Cleveland DW (2002) Gene replacement in mice reveals that the heavily phosphorylated tail of neurofilament heavy subunit does not affect axonal caliber or the transit of cargoes in slow axonal transport. J Cell Biol 158(4):681–693PubMedCrossRefGoogle Scholar
  64. Rivier F, Clarke S (1997) Cytochrome oxidase, acetylcholinesterase, and NADPH-diaphorase staining in human supratemporal and insular cortex: evidence for multiple auditory areas. Neuroimage 6:288–304PubMedCrossRefGoogle Scholar
  65. Sailaja K, Ahuja RK, Gopinath G (1996) Biparietal diameter: a useful measure for determining gestational age of human abortuses. Natl Med J India 9:165–167PubMedGoogle Scholar
  66. Sakaguchi T, Okada M, Kitamura T, Kawasaki K (1993) Reduced diameter and conduction velocity of myelinated fibers in the sciatic nerve of a neurofilament-deficient mutant quail. Neurosci Lett 153:65–68PubMedCrossRefGoogle Scholar
  67. Sarnat HB, Flores-Sarnat L (2002a) Cajal-Retzius and subplate neurons: their role in cortical development. Eur J Paediatr Neurol 6:91–97PubMedCrossRefGoogle Scholar
  68. Sarnat HB, Flores-Sarnat L (2002b) Role of Cajal-Retzius and subplate neurons in cerebral cortical development. Semin Pediatr Neurol 9:302–308PubMedCrossRefGoogle Scholar
  69. Sarnat HB, Flores-Sarnat L, Trevenen CL (2010) Synaptophysin immunoreactivity in the human hippocampus and neocortex from 6 to 41 weeks of gestation. J Neuropathol Exp Neurol 69:234–245PubMedCrossRefGoogle Scholar
  70. Schlaepfer WW, Bruce J (1991) Simultaneous up-regulation of neurofilament proteins during the postnatal development of the rat nervous system. J Neurosci Res 25:39–49CrossRefGoogle Scholar
  71. Seki T, Arai Y (1999) Different polysialic acid-neural cell adhesion molecule expression patterns in distinct types of mossy fiber boutons in the adult hippocampus. J Comp Neurol 410:115–125PubMedCrossRefGoogle Scholar
  72. Sheridan CJ, Matuz T, Draganova R, Eswaran H, Preissl H (2010) Fetal magnetoencephalography—achievements and challenges in the study of prenatal and early postnatal brain responses: a review. Infant Child Dev 19:80–93PubMedCrossRefGoogle Scholar
  73. Tapscott SJ, Bennett GS, Holtzer H (1981) Neuronal precursor cells in the chick neural tube express neurofilament proteins. Nature 292:836–838PubMedCrossRefGoogle Scholar
  74. Tardif E, Clarke S (2001) Intrinsic connectivity of human auditory areas: a tracing study with DiI. Eur J Neurosci 13:1045–1050PubMedCrossRefGoogle Scholar
  75. Ulfig N, Chan WY (2002) Axonal patterns in the prosencephalon of the human developing brain. Neuroembryology 1:4–16CrossRefGoogle Scholar
  76. Ulfig N, Nickel J, Bohl J (1998) Monoclonal antibodies SMI 311 and SMI 312 as tools to investigate the maturation of nerve cells and axonal patterns in human fetal brain. Cell Tissue Res 291:433–443PubMedCrossRefGoogle Scholar
  77. Verney C, Derer P (1995) Cajal-Retzius neurons in human cerebral cortex at midgestation show immunoreactivity for neurofilament and calcium-binding proteins. J Comp Neurol 359:144–153PubMedCrossRefGoogle Scholar
  78. von Economo C, Koskinas GN (1925) Die Cytoarchitectonik der Hirnrinde des erwachsenen Menschen. Julius Springer, BerlinGoogle Scholar
  79. Vouloumanos A, Werker JF (2007) Listening to language at birth: evidence for a bias for speech in neonates. Dev Sci. 10:159–164PubMedCrossRefGoogle Scholar
  80. Zecevic N, Milosevic A, Rakic S, Marin-Padilla M (1999) Early development and composition of the human primordial plexiform layer: an immunohistochemical study. J Comp Neurol 412:241–254PubMedCrossRefGoogle Scholar
  81. Zhu Q, Couillard-Despres S, Julien JP (1997) Delayed maturation of regenerating myelinated axons in mice lacking neurofilaments. Exp Neurol 148:299–316PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Arvind Singh Pundir
    • 1
  • L. Shahul Hameed
    • 1
  • P. C. Dikshit
    • 2
  • Praveen Kumar
    • 3
  • Surender Mohan
    • 3
  • Bishan Radotra
    • 4
  • S. K. Shankar
    • 5
  • Anita Mahadevan
    • 5
  • Soumya Iyengar
    • 1
    Email author
  1. 1.Division of Systems NeuroscienceNational Brain Research Centre (Deemed University)GurgaonIndia
  2. 2.Department of Forensic MedicineMaulana Azad Medical CollegeNew DelhiIndia
  3. 3.Department of Obstetrics and GynecologyBase HospitalDelhiIndia
  4. 4.Department of HistopathologyPost Graduate Institute of Medical Education and ResearchChandigarhIndia
  5. 5.Department of NeuropathologyNational Institute of Mental Health and Allied SciencesBangaloreIndia

Personalised recommendations