Advertisement

Brain Structure and Function

, Volume 222, Issue 4, pp 1829–1846 | Cite as

NADPH-diaphorase-positive neurons in the human inferior colliculus: morphology, distribution and clinical implications

  • D. Hinova-Palova
  • B. Landzhov
  • E. Dzhambazova
  • L. Edelstein
  • M. Minkov
  • K. Fakih
  • R. Minkov
  • A. Paloff
  • W. Ovtscharoff
Original Article

Abstract

Using the nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) reaction with nitroblue tetrazolium, we provided a detailed investigation of the distribution, dimensional characteristics and morphology of NADPH-d-positive neurons in the three main subdivisions of the human inferior colliculus (IC): central nucleus, pericentral nucleus, and external nucleus. In accordance with their perikaryal diameter, dendritic and axonal morphology, these neurons were categorized as large (averaging up to 45 μm in diameter), medium (20–30 µm), small (13–16 µm) and very small (7–10 µm). Their morphological differences could contribute to varying functionality and processing capacity. Our results support the hypothesis that large and medium NADPH-d-positive cells represent projection neurons, while the small cells correspond to interneurons. Heretofore, the very small NADPH-d-positive neurons have not been described in any species. Their functions—and if they are, indeed, the smallest neurons in the IC of humans—remain to be clarified. Owing to their location, we posit that they are interneurons that connect the large NADPH-d-positive neurons and thereby serve as an anatomical substrate for information exchange and processing before feeding forward to higher brain centers. Our results also suggest that the broad distribution of nitric oxide (NO) synthesis in the human IC is closely tied to the neuromodulatory action of NO on collicular neurotransmitters such as GABA and glutamate, and to calcium-binding proteins such as parvalbumin. A deeper understanding of the relationship between NADPH-d-positive fibers in all IC connections and their co-localization with other neurotransmitters and calcium-binding proteins will assist in better defining the function of NO in the context of its interplay with the cerebral cortex, the sequelae of the aging process and neurodegenerative disorders.

Keywords

Human Inferior colliculus NADPH-diaphorase Nitric oxide Presbycusis 

Abbreviations

AQ

Cerebral aqueduct

CN

Central nucleus

CNS

Central nervous system

dmCN

Dorsomedial central nucleus

EN

External nucleus

GABA

Gamma-aminobutyric acid

IC

Inferior colliculus

ICZ

Intercollicular zone

mPN

Medial pericentral nucleus

NADPH-d

Nicotinamide adenine dinucleotide phosphate-diaphorase

NO

Nitric oxide

NOS

Nitric oxide synthase

PN

Pericentral nucleus

References

  1. Aitkin LM, Phillips SC (1984) The interconnections of the inferior colliculi through their commissure. J Comp Neurol 228:210–216PubMedCrossRefGoogle Scholar
  2. Ayala YA, Malmierca MS (2013) Stimulus-specific adaptation and deviance detection in the inferior colliculus. Front Neural Circ 6:89. doi: 10.3389/fncir.2012.00089 Google Scholar
  3. Ayala YA, Perez-Gonzalez D, Duque D, Nelken I, Malmierca MS (2013) Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus. Front Neural Circ 6:119. doi: 10.3389/fncir.2012.00119 Google Scholar
  4. Bakhos D, Villeuneuve A, Kim S, Hammoudi K, Hommet C (2015) Hearing loss and Alzheimer’s disease. Geriatr Psychol Neuropsychiatr Vieil 3:195–204. doi: 10.1684/pnv.2015.0539 Google Scholar
  5. Berkley KJ, Budell RJ, Blomqvist A, Bull M (1986) Output systems of the dorsal column nuclei in the cat. Brain Res 396(3):199–225PubMedCrossRefGoogle Scholar
  6. Bledsoe SC, Shore SE, Guitton MJ (2003) Spatial representation of corticofugal input in the inferior colliculus: a multicontact silicon probe approach. Exp Brain Res 153:530–542PubMedCrossRefGoogle Scholar
  7. Brown MC (2003) Audition. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ (eds) Fundamental neuroscience. Academic Press, San Diego, pp 699–726Google Scholar
  8. Bruhwyler J, Chleide E, Liégeois JF, Carreer F (1993) Nitric oxide: a new messenger in the brain. Neurosci Biobehav Rev 17:373–384PubMedCrossRefGoogle Scholar
  9. Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197(4):705–722PubMedCrossRefGoogle Scholar
  10. Budinger E, Heil P, Scheich H (2000) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur J Neurosci 12:2452–2474PubMedCrossRefGoogle Scholar
  11. Cacciaglia R, Escera C, Slabu L, Grimm S, Sanjuán A, Ventura-Campos N, Ávila C (2015) Involvement of the human midbrain and thalamus in auditory deviance detection. Neuropsychologia 68:51–58. doi: 10.1016/j.neuropsychologia.2015.01.001 PubMedCrossRefGoogle Scholar
  12. Casseday JH, Fremouw T, Covey E (2002) The inferior colliculus: a hub for the central auditory system. In: Oertel D, Fay RR, Popper AN (eds) Springer handbook of auditory research, vol 15., Integrative functions in the mammalian auditory pathwaySpringer-Verlag, New York, pp 238–318Google Scholar
  13. Chernock ML, Larue DT, Winer JA (2004) A periodic network of neurochemical modules in the inferior colliculus. Hear Res 188(1–2):12–20PubMedCrossRefGoogle Scholar
  14. Coote EJ, Rees A (2008) The distribution of nitric oxide synthase in the inferior colliculus of guinea pig. Neuroscience 154(1):218–225PubMedCrossRefGoogle Scholar
  15. Covey E, Casseday JH (1986) Connectional basis for frequency representation in the nuclei of the lateral lemniscus of the bat Eptesicus fuscus. J Neurosci 6(10):2926–2940PubMedGoogle Scholar
  16. De Felipe J (1993) A study of NADPH-diaphorase-positive axonal plexuses in the human temporal cortex. Brain Res 615:342–346CrossRefGoogle Scholar
  17. Dimova R, Vuillet J, Seite R (1980) Study of the rat neostriatum using a combined Golgi-electron microscope technique and serial sections. Neuroscience 5:1581–1596PubMedCrossRefGoogle Scholar
  18. Druga R, Syka J (1993) NADPH-diaphorase activity in the central auditory structures of the rat. NeuroReport 4:999–1002PubMedCrossRefGoogle Scholar
  19. Druga R, Syka J (2001) Effect of auditory cortex lesions on NADPH-diaphorase staining in the inferior colliculus of rat. NeuroReport 12:1555–1559PubMedCrossRefGoogle Scholar
  20. Druga R, Syka J, Rajkowska G (1997) Projections of auditory cortex onto the inferior colliculus in the rat. Physiol Res 46:215–222PubMedGoogle Scholar
  21. Dudzinski DM, Igarashi J, Greif D, Michel T (2006) The regulation and pharmacology of endothelial nitric oxide synthase. Annu Rev Pharmacol Toxicol 46:235–276PubMedCrossRefGoogle Scholar
  22. Duque D, Ayala YA, Malmierca MS (2015) Deviance detection in auditory subcortical structures: what can we learn from neurochemistry and neural connectivity? Cell Tissue Res 361(1):215–232. doi: 10.1007/s00441-015-2134-7 PubMedCrossRefGoogle Scholar
  23. Dzambazova E, Bocheva A, Landzhov B, Bozhilova-Pastirova A (2008) Effects of kyotorphin on NADPH-d reactive neurons in rats after cold stress. Compt Rend Acad Bulg Sci 61(5):661–666Google Scholar
  24. Dzambazova E, Landzhov B, Bocheva A, Bozhilova-Pastirova A (2011a) Effects of kyotorphin on NADPH-d reactive neurons in rat’s cerebral cortex after acute immobilization stress. Compt Rend Bulg Acad Sci 64(11):1779–1784Google Scholar
  25. Dzambazova E, Landzhov B, Bocheva A, Bozhilova-Pastirova A (2011b) Effects of d-kyotorphin on nociception and NADPH-d neurons in rat’s periaqueductal gray after immobilization stress. Amino Acids 41(4):937–944PubMedCrossRefGoogle Scholar
  26. Edelstein L, Hinova-Palova D, Denaro FJ, Landzhov B, Malinova L, Minkov M, Paloff A, Ovtscharoff W (2012a) NADPH-diaphorase-positive neurons in the human claustrum. In: Society for Neuroscience, 42nd Annual Meeting, Abstract #895.20Google Scholar
  27. Edelstein L, Hinova-Palova D, Landzhov B, Malinova L, Minkov M, Paloff A, Ovtscharoff W (2012b) Neuronal nitric oxide synthase immunoreactivity in the human claustrum: light- and electron microscopic investigation. In: Society for Neuroscience, 42nd Annual Meeting, Abstract #895.21Google Scholar
  28. Egberongbe YI, Gentleman SM, Falkai P, Bogerts B, Polak JM, Roberts GW (1994) The distribution of nitric oxide synthase immunoreactivity in the human brain. Neuroscience 59(3):561–578PubMedCrossRefGoogle Scholar
  29. Engle JR, Gray DT, Turner H, Udell JB, Recanzone GH (2014) Age-related neurochemical changes in the rhesus macaque inferior colliculus. Front Aging Neurosci 6:73. doi: 10.3389/fnagi.2014.00073 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Esplugues JV (2002) NO as a signaling molecule in the nervous system. Br J Pharmacol 135:1079–1095PubMedPubMedCentralCrossRefGoogle Scholar
  31. Faye-Lund H, Osen KK (1985) Anatomy of the inferior colliculus in rat. Anat Embryol 171:1–20PubMedCrossRefGoogle Scholar
  32. Foster NL, Mellott JG, Schofield BR (2014) Perineuronal nets and GABAergic cells in the inferior colliculus of guinea pigs. Front Neuroanat 7:53. doi: 10.3389/fnana.2013.00053 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Fredrich M, Reisch A, Illing RB (2009) Neuronal subtype identity in the rat auditory brainstem as defined by molecular profile and axonal projection. Exp Brain Res 195(2):241–260. doi: 10.1007/s00221-009-1776-7 PubMedCrossRefGoogle Scholar
  34. Friauf E (2000) Development of chondroitin sulfate proteoglycans in the central auditory system of rats correlates with acquisition of mature properties. Audiol Neurootol 5(5):251–262PubMedCrossRefGoogle Scholar
  35. Gao PP, Zhang JW, Cheng JS, Zhou IY, Wu EX (2014) The inferior colliculus is involved in deviant sound detection as revealed by BOLD fMRI. Neuroimage 91:220–227PubMedCrossRefGoogle Scholar
  36. Geniec P, Morest DK (1971) The neuronal architecture of the human posterior colliculus. Acta Otolaryngol (Suppl) 295:1–33Google Scholar
  37. Glendenning KK, Masterton RB (1983) Acoustic chiasm: efferent projections of the lateral superior olive. J Neurosci 3(8):1521–1537PubMedGoogle Scholar
  38. Glendenning KK, Baker BN, Hutson KA, Masterton RB (1992) Acoustic chiasm V: inhibition and excitation in the ipsilateral and contralateral projections of LSD. J Comp Neurol 319:100–122PubMedCrossRefGoogle Scholar
  39. Gonzalez-Hernandez T, Mantolan-Sarmiento B, Gonzalez-Gonzalez B, Perez-Gonzalez H (1996) Sources of GABAergic input to the inferior colliculus of the rat. J Comp Neurol 372:309–326PubMedCrossRefGoogle Scholar
  40. Guardiani E, Zalewski C, Brewer C, Merideth M, Introne W, Smith AC, Gordon L, Gahl W, Kim HJ (2011) Otologic and audiologic manifestations of Hutchinson-Gilford progeria syndrome. Laryngoscope 121:2250–2255. doi: 10.1002/lary.22151 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Guix FX, Uribesalgo I, Coma M, Munoz FJ (2005) The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76:126–152PubMedCrossRefGoogle Scholar
  42. Gulati K, Joshi JC, Ray A (2015) Recent advances in stress research: focus on nitric oxide. Eur J Pharmacol 765:406–414. doi: 10.1016/j.ejphar.2015.08.055 PubMedCrossRefGoogle Scholar
  43. Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304:103–122PubMedCrossRefGoogle Scholar
  44. Hilbig H, Nowack S, Boeckler K, Bidmon H-J, Zilles K (2007) Characterization of neuronal subsets surrounded by perineuronal nets in the rhesus auditory brainstem. J Anat 210(5):507–517PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hinova-Palova DV, Dimova RN, Ivanov DP (1989) Identification of small neurons (“dwarf cells”) in the claustrum of the cat. Light and electron microscopic observations. Verb Anat Ges 82 (Anat Anz Suppl 164):883–884Google Scholar
  46. Hinova-Palova DV, Paloff AM, Christova T, Ovtscharoff W (1997) Topographical distribution of NADPH-diaphorase positive neurons in the cat’s claustrum. Eur J Morphol 35:105–116PubMedCrossRefGoogle Scholar
  47. Hinova-Palova DV, Edelstein L, Landzhov B, Minkov M, Malinova L, Hristov S, Denaro FJ, Alexandrov A, Kiriakova T, Brainova I, Paloff A, Ovtscharoff W (2014) Topographical distribution and morphology of NADPH-diaphorase-stained neurons in the human claustrum. Front Syst Neurosci 8:96. doi: 10.3389/fnsys.2014.00096 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Holstein GR, Friedrich VL, Martinelli GP (2001) Monoclonal l-citrulline immunostaining reveals nitric oxide-producing vestibular neurons. Ann NY Acad Sci 942:65–78. doi: 10.1111/j.1749-6632.2001.tb03736.x PubMedCrossRefGoogle Scholar
  49. Hudspeth AJ (2000) Hearing. In: Kandel ER, Schwartz JH, Jessel TM (eds) Principles of neural science. Mac-Graw Hill Companies, New York, pp 590–613Google Scholar
  50. Huffman RF, Henson OW (1990) The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Brain Res Rev 15:295–323PubMedCrossRefGoogle Scholar
  51. Hutson KA, Glendenning KK, Masterton RB (1991) Acoustic chiasm. IV: eight midbrain decussations of the auditory system in the cat. J Comp Neurol 312:105–131PubMedCrossRefGoogle Scholar
  52. Iacopucci AP, Mello RO, Barbosa-Silva R, Melo-Thomas L (2012) L-NOARG-induced catalepsy can be influenced by glutamatergic neurotransmission mediated by NMDA receptors in the inferior colliculus. Behav Brain Res 234(2):149–154. doi: 10.1016/j.bbr.2012.06.022 PubMedCrossRefGoogle Scholar
  53. Ito T, Bishop DC, Oliver DL (2009) Two classes of GABAergic neurons in the inferior colliculus. J Neurosci 29(44):13860–13869. doi: 10.1523/JNEUROSCI.3454-09.2009 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Ito T, Bishop DC, Oliver DL (2016) Functional organization of the local circuit in the inferior colliculus. Anat Sci Int 91(1):22–34CrossRefGoogle Scholar
  55. Joshi JC, Ray A, Gulati K (2015) Effects of morphine on stress induced anxiety in rats: role of nitric oxide and Hsp70. Physiol Behav 139:393–396PubMedCrossRefGoogle Scholar
  56. Jung J, Na C, Huh Y (2012) Alterations in nitric oxide synthase in the aged CNS. Oxid Med Cell Longev 2012:718976. doi: 10.1155/2012/718976 (Epub 2012) PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kemp JM, Powell TPS (1971) The structure of the caudate nucleus of the cat. Light and electron micros-copy. Phil Trans Roy Soc Lond Ser B 262:383–401CrossRefGoogle Scholar
  58. Kruse M, Novarro D, Desjardins P, Butterworth RF (2004) Increased brain endothelial nitric oxide synthase expression in thiamine deficiency: relationship to selective vulnerability. Neurochem Int 45:49–56PubMedCrossRefGoogle Scholar
  59. Kulesza RJ, Viñuela A, Saldaña E, Berrebi AS (2002) Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat. Hear Res 168(1–2):12–24PubMedCrossRefGoogle Scholar
  60. Landzhov B, Dzhambazova E (2012) Alteration in nitric oxide activity in the ventrolateral periaqueductal gray after immobilization stress in rats. Acta Morphol Anthropol 19:127–130Google Scholar
  61. Landzhov B, Bocheva A, Dzambazova E (2011a) Expression of nitric oxide in neurons of rat’s caudate putamen caused by d-kyotorphin. A histochemical study. Collect Czech Chem C Symp Ser 13:77–79Google Scholar
  62. Landzhov B, Dzambazova E, Bocheva (2011b) A effect of Tyr-Arg on NADPH-d-reactivity neurons in rat’s striatum. Collect Czech Chem C Symp Ser 13:31–33Google Scholar
  63. Lim HH, Anderson DJ (2006) Auditory cortical responses to electrical stimulation of inferior colliculus: implications for an auditory midbrain implant. J Neurophysiol 97:1413–1427PubMedCrossRefGoogle Scholar
  64. Loftus WC, Malmierca MS, Bishop DC, Oliver DL (2008) The cytoarchitecture of the inferior colliculus revisited: a common organization of the lateral cortex in rat and cat. Neuroscience 154:196–205PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lysakowski A, Singer M (2000) Nitric oxide synthase localized in a subpopulation of vestibular efferents with NADPH diaphorase histochemistry and nitric oxide synthase immunohistochemistry. J Comp Neurol 427(4):508–521PubMedCrossRefGoogle Scholar
  66. Malmierca MS, Rees A, Le Beau FE, Bjaalie JG (1995) Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357:124–144PubMedCrossRefGoogle Scholar
  67. Malmierca MS, Cristaudo S, Perez-Gonzalez D, Covey E (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29:5483–5493PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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 274:13–26PubMedCrossRefGoogle Scholar
  69. Martinelli G, Fridrich V, Holstein G (2002) l-citrulline immunostaining identifies nitric oxide production sites within neurons. Neuroscience 114:111–122. doi: 10.1016/S0306-4522(02)00238-5 PubMedCrossRefGoogle Scholar
  70. Meininger V, Pol D, Derer P (1986) The inferior colliculus of the mouse. A Nissl and Golgi study. Neuroscience 17(4):1159–1179PubMedCrossRefGoogle Scholar
  71. Mizukawa K (1990) Reduced nicotinamide adenine dinucleotide phosphate-diaphorase histochemistry: light and electron microscopic investigations. Meth Neurosci 3:457–472CrossRefGoogle Scholar
  72. Mizukawa K, Vincent ST, McGeer PL, McGeer EG (1989) Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibres in the cat central nervous system. J Comp Neurol 279:281–311PubMedCrossRefGoogle Scholar
  73. Moore DR (1988) Auditory brainstem of the ferret: sources of projections to the inferior colliculus. J Comp Neurol 269(3):342–354PubMedCrossRefGoogle Scholar
  74. Moore DR, Kotak VC, Sanes DH (1998) Commissural and lemniscal synaptic input to the gerbil inferior colliculus. J Neurophysiol 80:2229–2236PubMedGoogle Scholar
  75. Morawski M, Bruckner G, Jager C, Seeger G, Kunzle H, Arendt T (2010) Aggrecan-based extracellular matrix shows unique cortical features and conserved subcortical principles of mammalian brain organization in the Madagascan lesser hedgehog tenrec (Echinops telfairi Martin, 1838). Neuroscience 165(3):831–849. doi: 10.1016/j.neuroscience.2009.08.018 PubMedCrossRefGoogle Scholar
  76. Moreno-Lopez B, Estrada C, Escuero M (1998) Mechanisms of action and targets of nitric oxide in the oculomotor system. J Neurosci 18:10672–10679PubMedGoogle Scholar
  77. Morest DK, Oliver DL (1984) The neuronal architecture of the inferior colliculus in the cat: defining the functional ana-tomy of the auditory midbrain. J Comp Neurol 222:209–236PubMedCrossRefGoogle Scholar
  78. Moriizumi T, Hattori T (1991) Pallidotectal projection to the inferior colliculus of the rat. Exp Brain Res 87:223–226PubMedCrossRefGoogle Scholar
  79. Moriizumi T, Leduc-Cross B, Wu JY, Hattori T (1992) Separate neuronal populations of the rat substantia nigra pars lateralis with distinct projection sites and transmitter phenotypes. Neuroscience 46(3):711–720PubMedCrossRefGoogle Scholar
  80. Nakamoto KT, Mellott JG, Killius J, Storey-Workley ME, Sowick CS, Schofield BR (2013) Analysis of excitatory synapses in the guinea pig inferior colliculus: a study using electron microscopy and GABA immunocytochemistry. Neuroscience 237:170–183. doi: 10.1016/j.neuroscience.2013.01.061 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Nwabueze-Ogbo FC, Popelar J, Syka J (2002) Changes in the acoustically evoked activity in the inferior colliculus of the rat after functional ablation of the auditory cortex. Physiol Res 51:S95–S104PubMedGoogle Scholar
  82. Ohm TG, Braak H (1989) Auditory brainstem nuclei in Alzheimer’s disease. Neurosci Lett 96:60–63PubMedCrossRefGoogle Scholar
  83. Olazabal UE, Moore JK (1989) Nigrotectal projection to the inferior colliculus: horseradish peroxidase transport and tyrosine hydroxylase immunohistochemical studies in rats, cats, and bats. J Comp Neurol 282:98–118PubMedCrossRefGoogle Scholar
  84. Oliver DL (1987) Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction. J Comp Neurol 264(1):24–46PubMedCrossRefGoogle Scholar
  85. Oliver DL, Morest DK (1984) The central nucleus of the inferior colliculus in the cat. J Comp Neurol 222:237–264PubMedCrossRefGoogle Scholar
  86. Oliver DL, Winer JA, Beckius GE, Saint Marie RL (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J Comp Neurol 340(1):27-42PubMedCrossRefGoogle Scholar
  87. Ouda L, Syka J (2012) Immunocytochemical profiles of inferior colliculus neurons in the rat and their changes with aging. Front Neural Circuits 6:68. doi: 10.3389/fncir.2012.00068 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Paloff AM, Hinova-Palova D (1998) Topographical distribution of NADPH-diaphorase-positive neurons in the cat’s inferior colliculus. J Brain Res 39:231–243Google Scholar
  89. Paloff AM, Usunoff KG (1992) Projections to the inferior colliculus from the dorsal column nuclei. An experimental electron microscopic study in the cat. J Hirnforsch 33:597–610PubMedGoogle Scholar
  90. Paloff AM, Usunoff KG, Hinova-Palova DV (1992) Ultrastructure of golgi-impregnated and gold-toned neurons in the central nucleus of the inferior colliculus in the cat. J Hirnforsch 33:361–407PubMedGoogle Scholar
  91. Paloff AM, Christova T, Hinova-Palova DV, Ovtscharoff W (1994) Topographical distribution of NOS. Investigation with NADPH-diaphorase reaction in the cat’s brain. National Conference of Anatomy. Histology and Embryology, Stara Zagora (Bulgaria), AbstractsGoogle Scholar
  92. Papantchev V, Paloff A, Christova T, Hinova-Palova D, Ovtscharoff W (2005) Light microscopical study of nitric oxide synthase I-positive neurons, including fibres in the vestibular nuclear complex of the cat. Acta Histochem 107(2):113–120PubMedCrossRefGoogle Scholar
  93. Papantchev V, Paloff A, Hinova-Palova D, Hristov S, Todorova D, Ovtscharoff W (2006) Neuronal nitric oxide synthase immunopositive neurons in cat vestibular complex: a light and electron microscopic study. J Mol Histol 37(8–9):343–352PubMedCrossRefGoogle Scholar
  94. Pasik P, Pasik T, Di Figlia M (1976) Quantitative aspects of neuronal organization in the neostriatum of the Macaque Monkey. In: Yahr MD (ed) Basal Ganglia. Raven press, New York, pp 57–89Google Scholar
  95. Perez-Gonzalez D, Malmierca MS, Covey E (2005) Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22:2879–2885PubMedCrossRefGoogle Scholar
  96. Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64(1):51–68PubMedCrossRefGoogle Scholar
  97. Ramon y Cajal S (1891) Sur la structure de l’ecorce cerebrale de quelques mamiferes. La Cellule 7:125–176Google Scholar
  98. Ramon y Cajal S (1911) Histologie du Systeme Nerveux de l’Homme et des vertebres, vol 2. Maloine, ParisGoogle Scholar
  99. RoBards MJ (1979) Somatic neurons in the brainstem and neocortex projecting to the external nucleus of the inferior colliculus: an anatomical study in the opossum. J Comp Neurol 184(3):547–565PubMedCrossRefGoogle Scholar
  100. Rodrigo J, Springall DR, Utenthal O, Bentura ML, Abadia-Molina F, Riveros-Moreno V, Martinez-Murillo R, Polak JM, Moncada S (1994) Localization of nitric oxide synthase in the adult rat brain. Philos Trans R Soc London B 345:175–221CrossRefGoogle Scholar
  101. Sala C, Segal M (2014) Dendritic spines: the locus of structural and functional plasticity. Physiol Rev 94(1):141–188PubMedCrossRefGoogle Scholar
  102. Saldana E, Merchan MA (1992) Intrinsic and commissural connections of the rat inferior colliculus. J Comp Neurol 319:417–437PubMedCrossRefGoogle Scholar
  103. Saldana E, Feliciano M, Mugnaini E (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 371:15–40PubMedCrossRefGoogle Scholar
  104. Sanchez-Zuriaga D, Martн-Gutiйrrez N, De La Cruz MA, Peris-Sanchis MR (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 PubMedCrossRefGoogle Scholar
  105. Saxon DW, Beitz AJ (2000) Neuropeptides associated with the vestibular nuclei. In: Beitz AJ and Anderson JH (eds) Neurichemistry of the Vestibular System, Boca Raton, FL:CRC Press, 183–196Google Scholar
  106. Schuller G, Covey E, Casseday JH (1991) Auditory pontine grey: connections and response properties in the horseshoe bat. Europ J Neurosci 3:648–662CrossRefGoogle Scholar
  107. Sharma V, Nag TC, Wadhwa S, Roy TS (2009) Stereological investigation and expression of calcium-binding proteins in developing human inferior colliculus. J Chem Neuroanat 37(2):78–86PubMedCrossRefGoogle Scholar
  108. Shneiderman A, Henkel CK (1987) Banding of lateral superior olivary nucleus afferents in the inferior colliculus: a possible substrate for sensory integration. J Comp Neurol 266(4):519–534PubMedCrossRefGoogle Scholar
  109. Shneiderman A, Oliver DL, Henkel CK (1988) Connections of the dorsal nucleus of the lateral lemniscus: an inhibitory parallel pathway in the ascending auditory system? J Comp Neurol 276(2):188–208PubMedCrossRefGoogle Scholar
  110. Sinha UK, Hollen KM, Rodriguez R, Miller CA (1993) Auditory system degeneration in Alzheimer’s disease. Neurology 43(4):779–785PubMedCrossRefGoogle Scholar
  111. Smith PH (1992) Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique. J Neurosci 12:3700–3715PubMedGoogle Scholar
  112. Suga N, Ma XF (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4:783–794PubMedCrossRefGoogle Scholar
  113. Suga N, Gao EQ, Zhang YF, Ma XF, Olsen JF (2000) The corticofugal system for hearing: recent progress. Proc Natl Acad Sci USA 97:11807–11814PubMedPubMedCentralCrossRefGoogle Scholar
  114. Tanaka K, Otani K, Tokunaga A, Sugita S (1985) The organization of neurons in the nucleus of the lateral lemniscus projecting to the superior and inferior colliculi in the rat. Brain Res 341(2):252–260PubMedCrossRefGoogle Scholar
  115. Thomas E, Pears AGE (1961) The line localization of dehydrogenases in the nervous system. Histochemie 2:266–282PubMedCrossRefGoogle Scholar
  116. Thomas E, Pearse AGE (1964) The solitary active cells: histochemical demonstration of damage-resistant nerve cells with a TPN-diaphorase reaction. Acta Neuropathol (Berl) 3:238–249CrossRefGoogle Scholar
  117. Vincent SR, Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755–784PubMedCrossRefGoogle Scholar
  118. Vitale C, Marcelli V, Allocca R, Santangelo G, Riccardi P, Erro R, Amboni M, Pellecchia MT, Cozzolino A, Longo K, Picillo M, Moccia M, Agosti V, Sorrentino G, Cavaliere M, Marciano E, Barone P (2012) Hearing impairment in Parkinson’s disease: expanding the nonmotor phenotype. Mov Disord 27(12):1530–1535. doi: 10.1002/mds.25149 PubMedCrossRefGoogle Scholar
  119. Wenstrup JJ, Larue DT, Winer JA (1994) Projections of physiologically defined subdi-visions of the inferior colliculus in the mustached bat: targets in the medial geniculated body and extrathalamic nuclei. J Comp Neurol 346:207–236PubMedCrossRefGoogle Scholar
  120. Whitley JM, Henkel CK (1984) Topographical organization of the inferior collicular projection and other connections of the ventral nucleus of the lateral lemniscus in the cat. J Comp Neurol 229(2):257–270PubMedCrossRefGoogle Scholar
  121. Willard FH, Martin GF (1983) The auditory brainstem nuclei and some of their projections to the inferior colliculus in the North American opossum. Neuroscience 10:1203–1232PubMedCrossRefGoogle Scholar
  122. Winer JA (2005) Three systems of descending projections to the inferior colliculus. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, NewYork, pp 231–247CrossRefGoogle Scholar
  123. Winer JA, Larue DT, Diehl JJ, Hefti BJ (1998) Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400:147–174PubMedCrossRefGoogle Scholar
  124. Wu MD, Kimura M, Hiromichi I, Helfert RH (2008) A classification of NOergic neurons in the inferior colliculus of rat according to co-existence with classical amino acid transmitters. Okajimas Folia Anat Jpn 85(1):17–27PubMedCrossRefGoogle Scholar
  125. Yan J, Ehret G (2002) Corticofugal modulation of midbrain sound processing in the house mouse. Eur J Neurosci 16:119–128PubMedCrossRefGoogle Scholar
  126. Zhang DX, Li L, Kelly JB, Wu SH (1998) GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat. Hear Res 117:1–12PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Anatomy, Histology and Embryology, Faculty of MedicineMedical University of SofiaSofiaBulgaria
  2. 2.Department of Chemistry, Biochemistry, Physiology and PathophysiologySofia University “St. Kliment Ohridski”SofiaBulgaria
  3. 3.Del MarUSA
  4. 4.Department of Anatomy, Histology and EmbryologyMedical University of VarnaVarnaBulgaria
  5. 5.Department of Oral and Maxillofacial SurgeryMedical University of SofiaSofiaBulgaria

Personalised recommendations