Advertisement

Brain Structure and Function

, Volume 221, Issue 1, pp 617–629 | Cite as

Structural changes in the adult rat auditory system induced by brief postnatal noise exposure

  • Ladislav OudaEmail author
  • Jana Burianová
  • Zuzana Balogová
  • Hui Pin Lu
  • Josef Syka
Original Article

Abstract

In previous studies (Grécová et al., Eur J Neurosci 29:1921–1930, 2009; Bures et al., Eur J Neurosci 32:155–164, 2010), we demonstrated that after an early postnatal short noise exposure (8 min 125 dB, day 14) changes in the frequency tuning curves as well as changes in the coding of sound intensity are present in the inferior colliculus (IC) of adult rats. In this study, we analyze on the basis of the Golgi–Cox method the morphology of neurons in the IC, the medial geniculate body (MGB) and the auditory cortex (AC) of 3-month-old Long–Evans rats exposed to identical noise at postnatal day 14 and compare the results to littermate controls. In rats exposed to noise as pups, the mean total length of the neuronal tree was found to be larger in the external cortex and the central nucleus of the IC and in the ventral division of the MGB. In addition, the numerical density of dendritic spines was decreased on the branches of neurons in the ventral division of the MGB in noise-exposed animals. In the AC, the mean total length of the apical dendritic segments of pyramidal neurons was significantly shorter in noise-exposed rats, however, only slight differences with respect to controls were observed in the length of basal dendrites of pyramidal cells as well as in the neuronal trees of AC non-pyramidal neurons. The numerical density of dendritic spines on the branches of pyramidal AC neurons was lower in exposed rats than in controls. These findings demonstrate that early postnatal short noise exposure can induce permanent changes in the development of neurons in the central auditory system, which apparently represent morphological correlates of functional plasticity.

Keywords

Noise exposure Critical period Dendrites Spines Central auditory system Rat 

Notes

Acknowledgments

This study was supported by the Grant Agency of the Czech Republic P303-11-J005, P303/12/1347 and P304/12/G069.

References

  1. Aitkin LM, Moore DR (1975) Inferior colliculus. II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat. J Neurophysiol 38:1208–1216PubMedGoogle Scholar
  2. Bartlett EL, Smith PH (1999) Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J Neurophysiol 81:1999–2016PubMedGoogle Scholar
  3. Blackstad TW, Osen KK, Mugnaini E (1984) Pyramidal neurones of the dorsal cochlear nucleus, a Golgi and computer reconstruction study in cat. Neuroscience 13:827–854CrossRefPubMedGoogle Scholar
  4. Bonham BH, Cheung SW, Godey B, Schreiner CE (2004) Spatial organization of frequency response areas and rate/level functions in the developing AI. J Neurophysiol 91:841–854CrossRefPubMedGoogle Scholar
  5. Bose M, Muñoz-Llancao P, Roychowdhury S, Nichols JA, Jakkamsetti V, Porter B, Byrapureddy R, Salgado H, Kilgard MP, Aboitiz F, Dagnino-Subiabre A, Atzori M (2010) Effect of the environment on the dendritic morphology of the rat auditory cortex. Synapse 64:97–110PubMedCentralCrossRefPubMedGoogle Scholar
  6. Braak H, Braak E (1985) Golgi preparations as a tool in neuropathology with particular reference to investigations of the human telencephalic cortex. Prog Neurobiol 25:93–139CrossRefPubMedGoogle Scholar
  7. Bures Z, Grécová J, Popelár J, Syka J (2010) Noise exposure during early development impairs the processing of sound intensity in adult rats. Eur J Neurosci 32:155–164CrossRefPubMedGoogle Scholar
  8. Chang EF, Merzenich MM (2003) Environmental noise retards auditory cortical development. Science 300:498–502CrossRefPubMedGoogle Scholar
  9. Chang EF, Bao S, Imaizumi K, Schreiner CE, Merzenich MM (2005) Development of spectral and temporal response selectivity in the auditory cortex. Proc Natl Acad Sci USA 102:16460–16465PubMedCentralCrossRefPubMedGoogle Scholar
  10. Claiborne BJ, Amaral DG, Cowan WM (1990) Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302:206–219CrossRefPubMedGoogle Scholar
  11. Dardennes R, Jarreau PH, Meininger V (1984) A quantitative Golgi analysis of the postnatal maturation of dendrites in the central nucleus of the inferior colliculus of the rat. Brain Res 318:159–169CrossRefPubMedGoogle Scholar
  12. De Villers-Sidani E, Chang EF, Bao S, Merzenich MM (2007) Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci 27:180–189CrossRefPubMedGoogle Scholar
  13. Flood DG (1993) Critical issues in the analysis of dendritic extent in aging humans, primates, and rodents. Neurobiol Aging 14:649–654CrossRefPubMedGoogle Scholar
  14. Flores G, Alquicer G, Silva-Gomez AB, Zaldivar G, Stewart J, Quirion R, Srivastava LK (2005) Alterations in dendritic morphology of prefrontal cortical and nucleus accumbens neurons in postpubertal rats after neonatal excitotoxic lesions of the ventral hippocampus. Neuroscience 133:463–470CrossRefPubMedGoogle Scholar
  15. Gabriele ML, Brunso-Bechtold JK, Henkel CK (2000a) Plasticity in the development of afferent patterns in the inferior colliculus of the rat after unilateral cochlear ablation. J Neurosci 20:6939–6949PubMedGoogle Scholar
  16. Gabriele ML, Brunso-Bechtold JK, Henkel CK (2000b) Development of afferent patterns in the inferior colliculus of the rat: projection from the dorsal nucleus of the lateral lemniscus. J Comp Neurol 416:368–382CrossRefPubMedGoogle Scholar
  17. Geal-Dor M, Freeman S, Li G, Sohmer H (1993) Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear Res 69:236–242CrossRefPubMedGoogle Scholar
  18. Gibb R, Kolb B (1998) A method for vibratome sectioning of Golgi–Cox stained whole rat brain. J Neurosci Methods 79:1–4CrossRefPubMedGoogle Scholar
  19. Grécová J, Bures Z, Popelár J, Suta D, Syka J (2009) Brief exposure of juvenile rats to noise impairs the development of the response properties of inferior colliculus neurons. Eur J Neurosci 29:1921–1930CrossRefPubMedGoogle Scholar
  20. Horner CH, Arbuthnott E (1991) Methods of estimation of spine density—are spines evenly distributed throughout the dendritic field? J Anat 177:179–184PubMedCentralPubMedGoogle Scholar
  21. Ison JR, Hammond GR (1971) Modification of the startle reflex in the rat by changes in the auditory and visual environments. J Comp Physiol Psychol 75:435–452CrossRefPubMedGoogle Scholar
  22. Jacobs B, Scheibel AB (2002) Regional dendritic variation in primate cortical pyramidal cells. In: Schuz A, Miller R (eds) Cortical areas: unity and diversity (conceptual advances in brain research series). Taylor & Francis, London, pp 111–131CrossRefGoogle Scholar
  23. Jacobs B, Lubs J, Hannan M, Anderson K, Butti C, Sherwood CC, Hof PR, Manger PR (2011) Neuronal morphology in the African elephant (Loxodonta africana) neocortex. Brain Struct Funct 215:273–298CrossRefPubMedGoogle Scholar
  24. Kandler K (2004) Activity-dependent organization of inhibitory circuits: lessons from the auditory system. Curr Opin Neurobiol 14:96–104CrossRefPubMedGoogle Scholar
  25. Kandler K, Friauf E (1993) Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328:161–184CrossRefPubMedGoogle Scholar
  26. Kasture S, Vinci S, Ibba F, Puddu A, Marongiu M, Murali B, Pisanu A, Lecca D, Zernig G, Acquas E (2009) Withania somnifera prevents morphine withdrawal-induced decrease in spine density in nucleus accumbens shell of rats: a confocal laser scanning microscopy study. Neurotox Res 16:343–355CrossRefPubMedGoogle Scholar
  27. Kolb B, Cioe J, Comeau W (2008) Contrasting effects of motor and visual spatial learning tasks on dendritic arborization and spine density in rats. Neurobiol Learn Mem 90:295–300CrossRefPubMedGoogle Scholar
  28. Koss WA, Belden CE, Hristov AD, Juraska JM (2014) Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse 68:61–72CrossRefPubMedGoogle Scholar
  29. Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L (2005) Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163:78–90CrossRefPubMedGoogle Scholar
  30. Luján R, de Cabo C, Juiz JM (2008) Inhibitory synaptogenesis in the rat anteroventral cochlear nucleus. Neuroscience 154:315–328CrossRefPubMedGoogle Scholar
  31. Malmierca MS, Blackstad TW, Osen KK, Karagülle T, Molowny RL (1993) The central nucleus of the inferior colliculus in rat: a Golgi and computer reconstruction study of neuronal and laminar structure. J. Comp Neurol 333:1–27CrossRefPubMedGoogle Scholar
  32. Malmierca MS, Blackstad TW, Osen KK (2011) Computer-assisted 3-D reconstructions of Golgi-impregnated neurons in the cortical regions of the inferior colliculus of rat. Hear Res 274:13–26CrossRefPubMedGoogle Scholar
  33. McClure MM, Threlkeld SW, Rosen GD, Fitch RH (2005) Auditory processing deficits in unilaterally and bilaterally injured hypoxic–ischemic rats. NeuroReport 16:1309–1312CrossRefPubMedGoogle Scholar
  34. McClure MM, Threlkeld SW, Rosen GD, Fitch RH (2007) Auditory processing and learning/memory following erythropoietin administration in neoratally hypoxic-ischemic injured rats. Brain Res 1132:203–209CrossRefPubMedGoogle Scholar
  35. McMullen NT, Glaser EM (1988) Auditory cortical responses to neonatal deafening: pyramidal neuron spine loss without changes in growth or orientation. Exp Brain Res 72:195–200CrossRefPubMedGoogle Scholar
  36. McMullen NT, Goldberger B, Suter CM, Glaser EM (1988) Neonatal deafening alters nonpyramidal dendrite orientation in auditory cortex: a computer microscope study in the rabbit. J Comp Neurol. 267:92–106CrossRefPubMedGoogle Scholar
  37. Melendez-Ferro M, Perez-Costas E, Roberts RC (2009) A new use for long-term frozen brain tissue: Golgi impregnation. J Neurosci Methods 176:72–77PubMedCentralCrossRefPubMedGoogle Scholar
  38. Nakahara H, Zhang LI, Merzenich MM (2004) Specialization of primary auditory cortex processing by sound exposure in the “critical period”. Proc Natl Acad Sci USA 101:7170–7174PubMedCentralCrossRefPubMedGoogle Scholar
  39. Oliver DL (2005) Neuronal Organization in the Inferior Colliculus. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 69–115CrossRefGoogle Scholar
  40. Paxinos G, Watson C (1998) The rat brain, 4th edn. Academic Press, New YorkGoogle Scholar
  41. Pierson M, Snyder-Keller A (1994) Development of frequency-selective domains in inferior colliculus of normal and neonatally noise-exposed rats. Brain Res 636:55–67CrossRefPubMedGoogle Scholar
  42. Robinson TJ, Kolb B (1997) Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17:8491–8497PubMedGoogle Scholar
  43. Romand R, Ehret G (1990) Development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice. Brain Res Dev Brain Res 54:221–234CrossRefPubMedGoogle Scholar
  44. Romand S, Wang Y, Toledo-Rodriguez M, Markram H (2011) Morphological development of thick-tufted layer v pyramidal cells in the rat somatosensory cortex. Front Neuroanat 5:5PubMedCentralPubMedGoogle Scholar
  45. Rybalko N, Syka J (2001) Susceptibility to noise exposure during postnatal development in rats. Hear Res 155:32–40CrossRefPubMedGoogle Scholar
  46. Rybalko N, Bureš Z, Burianová J, Popelář J, Grécová J, Syka J (2011) Noise exposure during early development influences the acoustic startle reflex in adult rats. Physiol Behav 102:453–458CrossRefPubMedGoogle Scholar
  47. Sanes DH, Constantine-Paton M (1985) The development of stimulus following in the cochlear nerve and inferior colliculus of the mouse. Brain Res 354:255–267CrossRefPubMedGoogle Scholar
  48. Sanes DH, Takács C (1993) Activity-dependent refinement of inhibitory connections. Eur J Neurosci 5:570–574CrossRefPubMedGoogle Scholar
  49. Sanes DH, Markowitz S, Bernstein J, Wardlow J (1992) The influence of inhibitory afferents on the development of postsynaptic dendritic arbors. J Comp Neurol 321:637–644CrossRefPubMedGoogle Scholar
  50. Schachtele SJ, Losh J, Dailey ME, Green SH (2011) Spine formation and maturation in the developing rat auditory cortex. J Comp Neurol 519:3327–3345PubMedCentralCrossRefPubMedGoogle Scholar
  51. Seib LM, Wellman CL (2003) Daily injections alter spine density in rat medial prefrontal cortex. Neurosci Lett 337:29–32CrossRefPubMedGoogle Scholar
  52. Swerdlow NR, Geyer MA, Braff DL (2001) Neural circuit regulation of prepulse inhibition of startle in the rat, current knowledge and future challenges. Psychopharmacology 156:194–215CrossRefPubMedGoogle Scholar
  53. Syka J (2002) Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol Rev 82:601–636CrossRefPubMedGoogle Scholar
  54. Syka J, Rybalko N (2000) Threshold shifts and enhancement of cortical evoked responses after noise exposure in rats. Hear Res 139:59–68CrossRefPubMedGoogle Scholar
  55. Thornton SK, Semple MN, Sanes DH (1999) Conditioned enhancement and suppression in the developing auditory midbrain. Eur J Neurosci 11:1414–1420CrossRefGoogle Scholar
  56. Webster DP, Popper AN, Fay RR (1992) The mammalian auditory pathway: neuroanatomy. Springer, New YorkCrossRefGoogle Scholar
  57. Xu J, Yu L, Cai R, Zhang J, Sun X (2009) Early continuous white noise exposure alters auditory spatial sensitivity and expression of GAD65 and GABAA receptor subunits in rat auditory cortex. Cereb Cortex 20:804–812CrossRefPubMedGoogle Scholar
  58. Zhang LI, Bao S, Merzenich MM (2001) Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 4:1123–1130CrossRefPubMedGoogle Scholar
  59. Zhou X, Merzenich MM (2007) Intensive training in adults refines A1 representations degraded in an early postnatal critical period. Proc Natl Acad Sci USA 104:15935–15940PubMedCentralCrossRefPubMedGoogle Scholar
  60. Zhou X, Nagarajan N, Mossop BJ, Merzenich MM (2008) Influences of un-modulated acoustic inputs on functional maturation and critical-period plasticity of the primary auditory cortex. Neuroscience 154:390–396PubMedCentralCrossRefPubMedGoogle Scholar
  61. Zilles K (1985) The cortex of the rat, a stereotaxic atlas. Springer, BerlinCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Ladislav Ouda
    • 1
    Email author
  • Jana Burianová
    • 1
  • Zuzana Balogová
    • 1
  • Hui Pin Lu
    • 2
  • Josef Syka
    • 1
  1. 1.Department of Auditory Neuroscience, Institute of Experimental MedicineAcademy of Sciences of the Czech RepublicPragueCzech Republic
  2. 2.Medical CollegeNational Cheng Kung UniversityTainanTaiwan

Personalised recommendations