Long-term regulation in calretinin staining in the rat inferior colliculus after unilateral auditory cortical ablation

Journal of Comparative Neurology

Volumn 518, Issue 20, 2010, Pages 4261-4276

  Clarkson, Cheryl ^a   Juíz, Jośe M ^b   Merch́an, Miguel Á ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

Author keywords

Auditory descending pathways; Calcium binding proteins; Calcium homeostasis; Corticofugal projection; Neuronal excitability; Stereology; Western blot

Indexed keywords

CALRETININ;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; BRAIN NERVE CELL; CONTROLLED STUDY; INFERIOR COLLICULUS; INNERVATION; MALE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; WESTERN BLOTTING;

ANIMALS; AUDITORY CORTEX; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULI; MALE; RANDOM ALLOCATION; RATS; RATS, WISTAR;

EID: 77957909912     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22453     Document Type: Article

References (86)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Alvarado JC, Fuentes-Santamaría V, Henkel CK, Brunso-Bechtold JK. 2004. Alterations in calretinin immunostaining in the ferret superior olivary complex after cochlear ablation. J Comp Neurol 470:63-79.
3. Alvarado JC, Fuentes-Santamaria V, Franklin SR, Brunso-Bechtold JK, Henkel CK. 2005. Unilateral cochlear ablation in adult ferrets results in upregulation in calretinin immuno-staining in the central nucleus of the inferior colliculus. Neuroscience 136:957-969.
4. Andersen RA, Roth GL, Aitkin LM, Merzenich MM. 1980. The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat. J Comp Neurol 194:649-662.
5. Arai R, Winsky L, Arai M, Jacobowitz DM. 1991. Immunohisto-chemical localization of calretinin in the rat hindbrain. J Comp Neurol 310:21-44.
6. Bajo VM, Moore DR. 2005. Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus. J Comp Neurol 486:101-116.
7. Bajo VM, Nodal FR, Bizley JK, Moore DR, King AJ. 2007. The ferret auditory cortex: descending projections to the inferior colliculus. Cereb Cortex 17:475-491.
8. Bearzatto B, Servais L, Roussel C, Gall D, Baba-Aissa F, Schurmans S, de Kerchove d'Exaerde A, Cheron G, Schiffmann SN. 2006. Targeted calretinin expression in granule cells of calretinin-null mice restores normal cerebellar functions. FASEB J 20:380-382.
9. Becker M, Nothwang HG, Friauf E. 2008. Different protein profiles in inferior colliculus and cerebellum: a comparative proteomic study. Neuroscience 154:233-244.
10. Beyerl BD. 1978. Afferent projections to the central nucleus of the inferior colliculus in the rat. Brain Res 145: 209-223.
11. 2+-buffering provided by calretinin. Biochim Biophys Acta 1449: 169-177.
12. Bowen GP, Lin D, Taylor MK, Ison JR. 2003. Auditory cortex lesions in the rat impair both temporal acuity and noise increment thresholds, revealing a common neural substrate. Cereb Cortex 13:815-822.
13. Buckingham SD, Kwak S, Jones AK, Blackshaw SE, Sattelle DB. 2008. Edited GluR2, a gatekeeper for motor neurone survival?. Bioessays 30:1185-1192.
14. Caicedo A, d'Aldin C, Eybalin M, Puel JL. 1997. Temporary sensory deprivation changes calcium-binding proteins levels in the auditory brainstem. J Comp Neurol 378:1-15.
15. Camp AJ, Wijesinghe R. 2009. Calretinin: modulator of neuronal excitability. Int J Biochem Cell Biol 41:2118-2121.
16. Clarkson C, Lopez DE, Merch́an MA. 2009. Long-term functional recovery in the rat auditory system after unilateral auditory cortex ablation. Acta Otolaryngol 13:1-7.
17. Coleman JR, Clerici WJ. 1987. Sources of projections to subdivisions of the inferior colliculus in the rat. J Comp Neurol 262:215-226.
18. Cooke JE, Zhang H, Kelly JB. 2007. Detection of sinusoidal amplitude modulated sounds: deficits after bilateral lesions of auditory cortex in the rat. Hear Res 231:90-99.
19. D'Orlando C, Fellay B, Schwaller B, Salicio V, Bloc A, Gotzos V, Celio MR. 2001. Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells. Brain Res 909:145-158.
20. D'Orlando C, Celio MR, Schwaller B. 2002. Calretinin and cal-bindin D-28k, but not parvalbumin protect against glutamate-induced delayed excitotoxicity in transfected N18-RE 105 neuroblastoma-retina hybrid cells. Brain Res 945: 181-190.
21. Diamond IT, Jones EG, Powell TP. 1969. The projection of the auditory cortex upon the diencephalon and brain stem in the cat. Brain Res 15:305-340.
22. Doucet JR, Molavi DL, Ryugo DK. 2003. The source of cortico-collicular and corticobulbar projections in area Te1 of the rat. Exp Brain Res 153:461-466.
23. Druga R, Syka J. 1984a. Ascending and descending projections to the inferior colliculus in the rat. Physiol Bohemoslov 33:31-42.
24. Druga R, Syka J. 1984b. Neocortical projections to the inferior colliculus in the rat. (An experimental study using antero-grade degeneration techniques). Physiol Bohemoslov 33: 251-253.
25. Druga R, Syka J. 2001. Effect of auditory cortex lesions on NADPH-diaphorase staining in the inferior colliculus of rat. Neuroreport 12:1555-1559.
26. Edmonds B, Reyes R, Schwaller B, Roberts WM. 2000. Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3:786-790.
27. Faye-Lund H, Osen KK. 1985. Anatomy of the inferior colliculus in rat. Anat Embryol 171:1-20.
28. FitzPatrick KA, Imig TJ. 1978. Projections of auditory cortex upon the thalamus and midbrain in the owl monkey. J Comp Neurol 177:573-555.
29. Forster CR, Illing RB. 2000. Plasticity of the auditory brain-stem: cochleotomy-induced changes of calbindin-D28k expression in the rat. J Comp Neurol 416:173-187.
30. 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 195:241-260.
31. Fuentealba P, Klausberger T, Karayannis T, Suen WY, Huck J, Tomioka R, Rockland K, Capogna M, Studer M, Morales M, Somogyi P. 2010. Expression of COUP-TFII nuclear receptor in restricted GABAergic neuronal populations in the adult rat hippocampus. J Neurosci 30:1595-1609.
32. Fuentes-Santamaria V, Alvarado JC, Brunso-Bechtold JK, Henkel CK. 2003. Upregulation of calretinin immunostaining in the ferret inferior colliculus after cochlear ablation. J Comp Neurol 460:585-596.
33. Gall D, Roussel C, Susa I, D'Angelo E, Rossi P, Bearzatto B, Galas MC, Blum D, Schurmans S, Schiffmann SN. 2003. Altered neuronal excitability in cerebellar granule cells of mice lacking calretinin. J Neurosci 23:9320-9327.
34. Gall D, Roussel C, Nieus T, Cheron G, Servais L, D'Angelo E, Schiffmann SN. 2005. Role of calcium binding proteins in the control of cerebellar granule cell neuronal excitability: experimental and modeling studies. Prog Brain Res 148: 321-328.
35. Games KD, Winer JA. 1988. Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hear Res 34:1-25.
36. Goldstein ME, Sternberger LA, Sternberger NH. 1987. Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H). J Neuroimmunol 14:135-148.
37. Guillery RW, Herrup K. 1997. Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2-7.
38. Gundersen HJ, Jensen EB, Kiêu K, Nielsen J. 1999. The efficiency of systematic sampling reconsidered. J Microsc 193:199-211.
39. Gurden H, Schiffmann SN, Lemaire M, Bohme GA, Parmentier M, Schurmans S. 1998. Calretinin expression as a critical component in the control of dentate gyrus long-term potentiation induction in mice. Eur J Neurosci 10: 3029-3033.
40. Henny P, Jones BE. 2008. Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glu-tamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci 27:654-670.
41. Herbert H, Aschoff A, Ostwald J. 1991. Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304:103-122.
42. Idrizbegovic E, Bogdanovic N, Canlon B. 1999. Sound stimulation increases calcium-binding protein immunoreactivity in the inferior colliculus in mice. Neurosci Lett 259:49-52.
43. Isaacs KR, Wolpoe ME, Jacobowitz DM. 2000. Vulnerability to calcium-induced neurotoxicity in cultured neurons expressing calretinin. Exp Neurol 163:311-323.
44. 2+-overload or trophic factor deprivation. Biochim Biophys Acta 1313:194-200.
45. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
46. Langley OK, Sternberger NH, Sternberger LA. 1988. Expression of neurofilament proteins by Purkinje cells: ultrastructural immunolocalization with monoclonal antibodies. Brain Res 457:12-20.
47. Lohmann C, Friauf E. 1996. Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brain-stem of adult and developing rats. J Comp Neurol 367: 90-109.
48. Lukas W, Jones KA. 1994. Cortical neurons containing calretinin are selectively resistant to calcium overload and excitotoxicity in vitro. Neuroscience 61:307-316.
49. Melo LL, Brandao ML, Graeff FG, Sandner G. 1997. Bilateral ablation of the auditory cortex in the rat alters conditioned emotional suppression to a sound as appraised through a latent inhibition study. Behav Brain Res 88:59-65.
50. Mockel V, Fischer G. 1994. Vulnerability to excitotoxic stimuli of cultured rat hippocampal neurons containing the calcium-binding proteins calretinin and calbindin D28K. Brain Res 648:109-120.
51. Molnar Z, Cheung AF. 2006. Towards the classification of sub-populations of layer V pyramidal projection neurons. Neurosci Res 55:105-115.
52. Nakamoto KT, Jones SJ, Palmer AR. 2008. Descending projections from auditory cortex modulate sensitivity in the mid-brain to cues for spatial position. J Neurophysiol 99: 2347-2356.
53. 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(Suppl 1):S95-S104.
54. Paxinos G, Watson C. 2005. The rat brain in stereotaxic coordinates, 5th ed. San Diego: Elsevier Academic Press.
55. Paxinos G, Carrive P, Wang H, Wang PY. 1999. Chemoarchitectonic atlas of the rat brainstem. San Diego: Elsevier Academic Press.
56. Popelar J, Nwabueze-Ogbo FC, Syka J. 2003. Changes in neuronal activity of the inferior colliculus in rat after temporal inactivation of the auditory cortex. Physiol Res 52: 615-628.
57. Prieto JJ, Winer JA. 1999. Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons. J Comp Neurol 404:332-358.
58. Rogers JH, Resibois A. 1992. Calretinin and calbindin-D28k in rat brain: patterns of partial co-localization. Neuroscience 51:843-865.
59. Rostkowski AB, Teppen TL, Peterson DA, Urban JH. 2009. Cell-specific expression of neuropeptide Y Y1 receptor immunoreactivity in the rat basolateral amygdala. J Comp Neurol 517:166-176.
60. Roussel C, Erneux T, Schiffmann SN, Gall D. 2006. Modulation of neuronal excitability by intracellular calcium buffering: from spiking to bursting. Cell Calcium 39:455-466.
61. Rybalko N, Suta D, Nwabueze-Ogbo F, Syka J. 2006. Effect of auditory cortex lesions on the discrimination of frequency-modulated tones in rats. Eur J Neurosci 23:1614-1522.
62. Saldãna E, Merch́an MA. 1992. Intrinsic and commissural connections of the rat inferior colliculus. J Comp Neurol 319: 417-437.
63. Saldãna 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 371:15-40.
64. Sans N, Moniot B, Raymond J. 1995. Distribution of calretinin mRNA in the vestibular nuclei of rat and guinea pig and the effects of unilateral labyrinthectomy: a non-radioactive in situ hybridization study. Brain Res Mol Brain Res 28: 1-11.
65. Schiffmann SN, Cheron G, Lohof A, d'Alcantara P, Meyer M, Parmentier M, Schurmans S. 1999. Impaired motor coordination and Purkinje cell excitability in mice lacking calretinin. Proc Natl Acad Sci USA 96:5257-5262.
66. Schofield BR. 2009. Projections to the inferior colliculus from layer VI cells of auditory cortex. Neuroscience 159: 246-258.
67. Schurmans S, Schiffmann SN, Gurden H, Lemaire M, Lipp HP, Schwam V, Pochet R, Imperato A, Bohme GA, Parmentier M. 1997. Impaired long-term potentiation induction in dentate gyrus of calretinin-deficient mice. Proc Natl Acad Sci USA 94:10415-10420.
68. 2+ buffers. Cell Mol Life Sci 66:275-300.
69. Schwaller B, Buchwald P, Blumcke I, Celio MR, Hunziker W. 1993. Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell calcium 14:639-648.
70. Schwaller B, Bruckner G, Celio MR, Hartig W. 1999. A polyclonal goat antiserum against the calcium-binding protein calretinin is a versatile tool for various immunochemical techniques. J Neurosci Methods 92:137-144.
71. Sia Y, Bourne JA. 2008. The rat temporal association cortical area 2 (Te2) comprises two subdivisions that are visually responsive and develop independently. Neuroscience 156: 118-128.
72. Stack KE, Code RA. 2000. Calretinin expression in the chick cochlear nucleus after deafferentation. Brain Res 873: 135-139.
73. Sternberger LA. 1986. Immunocytochemistry, 3rd edn. New York: John Wiley.
74. Sternberger LA, Sternberger NH. 1983. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 80: 6126-6130.
75. Syka J, Rybalko N, Mazelova J, Druga R. 2002. Gap detection threshold in the rat before and after auditory cortex ablation. Hear Res 172:151-159.
76. Talwar SK, Musial PG, Gerstein GL. 2001. Role of mammalian auditory cortex in the perception of elementary sound properties. J Neurophysiol 85:2350-2358.
77. Threlkeld SW, Penley SC, Rosen GD, Fitch RH. 2008. Detection of silent gaps in white noise following cortical deactivation in rats. Neuroreport 19:893-898.
78. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354.
79. Van De Werd HJ, Uylings HB. 2008. The rat orbital and agranular insular prefrontal cortical areas: a cytoarchitectonic and chemoarchitectonic study. Brain Struct Funct 212: 387-401.
80. Voelker CC, Garin N, Taylor JS, Gahwiler BH, Hornung JP, Molnar Z. 2004. Selective neurofilament (SMI-32, FNP-7 and N200) expression in subpopulations of layer V pyramidal neurons in vivo and in vitro. Cereb Cortex 14:1276-1286.
81. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
82. Winer JA, Prieto JJ. 2001. Layer V in cat primary auditory cortex (AI): cellular architecture and identification of projection neurons. J Comp Neurol 434:379-412.
83. Winer JA, Larue DT, Diehl JJ, Hefti BJ. 1998. Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400:147-174.
84. Winsky L, Jacobowitz DM. 1995. Effects of unilateral cochlea ablation on the distribution of calretinin mRNA and immunoreactivity in the guinea pig ventral cochlear nucleus. J Comp Neurol 354:564-582.
85. Wu G, Lu ZH, Obukhov AG, Nowycky MC, Ledeen RW. 2007. Induction of calcium influx through TRPC5 channels by cross-linking of GM1 ganglioside associated with alpha5-beta1 integrin initiates neurite outgrowth. J Neurosci 27: 7447-7458.
86. Zettel ML, O'Neill WE, Trang TT, Frisina RD. 2001. Early bilateral deafening prevents calretinin up-regulation in the dorsal cortex of the inferior colliculus of aged CBA/CaJ mice. Hear Res 158:131-138.