Multiple topographically organized projections connect the central nucleus of the inferior colliculus to the ventral division of the medial geniculate nucleus in the gerbil, Meriones unguiculatus

Journal of Comparative Neurology

Volumn 503, Issue 3, 2007, Pages 432-453

  Cant, Nell B ^a   Benson, Christina G ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Auditory pathways; Biotinylated dextran amine; Neuroanatomy; Sensory systems

Indexed keywords

DEXTRAN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; COCHLEAR NUCLEUS; CONTROLLED STUDY; FEMALE; GERBIL; INFERIOR COLLICULUS; MEDIAL GENICULATE BODY; MEDIAL LEMNISCUS; NERVE FIBER; NERVE PROJECTION; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL; TOPOGRAPHY; VENTRAL ROOT;

ANIMALS; AUDITORY PATHWAYS; FEMALE; GENICULATE BODIES; GERBILLINAE; INFERIOR COLLICULUS; NERVE FIBERS;

EID: 34250900901     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21391     Document Type: Article

References (98)

1. Adams JC. 1981. Heavy metal intensification of DAB-based reaction product. J. Histochem Cytochem 29:775-779.
2. Andersen RA, Roth GL, Aitkin LM, Merzenich MM. 1980a. The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat. J Comp Neurol 194:649-662.
3. Andersen RA, Knight PL, Merzenich MM. 1980b. The thalamocortical and corticothalamic connections of AI, AII, and the anterior auditory field (AAF) in the cat: evidence for two largely segregated systems of connections. J Comp Neurol 194:663-701.
4. 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.
5. Bajo VM, Nodal FR, Bizley JK, Moore DR, King AJ. 2006. The ferret auditory cortex: descending projections to the inferior colliculus. Cereb Cortex 17:475-491.
6. Bartlett EL, Stark JM, Guillery RW, Smith PH. 2000. Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience 100:811-828.
7. Berman AL, Jones EG. 1982. The thalamus and basal telencephalon of the cat. A cytoarchitectonic atlas with stereotaxic coordinates. Madison, WI: University of Wisconsin Press. p 28-31.
8. Brandner S, Redies H. 1990. The projection from medial geniculate to field AI in cat: organization in the isofrequency dimension. J Neurosci 10:50-61.
9. Brückner S, Rübsamen R. 1995. Binaural response characteristics in isofrequency sheets of the gerbil inferior colliculus. Hearing Res 86:1-14.
10. 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 197:705-722.
11. Budinger E, Heil P, Scheich. 2000. Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur J Neurosci 12:2452-2474.
12. Calford MB. 1983. The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350-2364.
13. Calford MB, Aitkin LM. 1983. Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3:2365-2380.
14. Cant NB, Benson CG. 2005. An atlas of the inferior colliculus of the gerbil in three dimensions. Hearing Res 206:12-27.
15. Cant NB, Benson CG. 2006. Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): differences in distribution of projections from the cochlear nuclei and the superior olivary complex. J Comp Neurol 495:511-528.
16. Cetas JS, Price RO, Velenovsky DS, Sinex DG, McMullen NT. 2001. Frequency organization and cellular lamination in the medial geniculate body of the rabbit. Hearing Res 155:113-123.
17. Cetas JS, Price RO, Velenovsky DS, Crowe JJ, Sinex DG, McMullen NT. 2002. Cell types and response properties of neurons in the ventral division of the medial geniculate body of the rabbit. J Comp Neurol 445:78-96.
18. Chen S, Aston-Jones G. 1998. Axonal collateral-collateral transport of tract tracers in brain neurons: false anterograde labeling and useful tool. Neuroscience 82:1151-1163.
19. Clarey JC, Barone P, Imig TJ. 1992. Physiology of thalamus and cortex. In: Popper AN, Fay RR, editors. The mammalian auditory pathway: neurophysiology. New York: Springer-Verlag. p 232-334.
20. Clerici WJ, Coleman JR. 1990. Anatomy of the rat medial geniculate body: I. Cytoarchitecture, myeloarchitecture, and neocortical connectivity. J Comp Neurol 297:14-31.
21. Coomes DL, Schofield RM, Schofield BR. 2005. Unilateral and bilateral projections from cortical cells to the inferior colliculus in guinea pigs. Brain Res 1042:62-72.
22. Cruikshank SJ, Killackey HP, Metherate R. 2001. Parvalbumin and calbindin are differentially distributed within primary and secondary subregions of the mouse auditory forebrain. Neuroscience 105:553-569.
23. Davis KA. 2002. Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus. J Neurophysiol 87:1824-1835.
24. de Ribaupierre F. 1997. Acoustical information processing in the auditory thalamus and cerebral cortex. In: Ehret E, Romand R, editors. The central auditory system. New York: Oxford University Press. p 317-397.
25. de Venecia RK, Smelser CB, Lossman SD, McMullen NT. 1995. Complementary expression of parvalbumin and calbindin D-28 delineates subdivisions of the rabbit medial geniculate body. J Comp Neurol 359:595-612.
26. Doucet JR, Molavi DL, Ryugo DK. 2003. The source of corticocollicular and corticobulbar projections in area Te1 of the rat. Exp Brain Res 153:461-466.
27. Games KD, Winer JA. 1988. Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hearing Res 34:1-26.
28. González-Hernández TH, Galindo-Mireles D, Castañeyra-Perdomo A, Ferres-Torres R. 1991. Divergent projections of projecting neurons of the inferior colliculus to the medial geniculate body and the contralateral inferior colliculus in the rat. Hearing Res 52:17-21.
29. Graybiel AM. 1973. The thalamo-cortical projection of the so-called posterior nuclear group: a study with anterograde degeneration methods in the cat. Brain Res 49:229-244.
30. He J. 2001. ON and OFF pathways segregated at the auditory thalamus of the guinea pig. J Neurosci 21:8672-8679.
31. Heierli P, de Ribaupierre F, de Ribaupierre Y. 1987. Functional properties and interactions of neuron pairs simultaneously recorded in the medial geniculate body of the cat. Hearing Res 25:209-225.
32. Henkel CK. 1983. Evidence of sub-collicular auditory projections to the medial geniculate nucleus in the cat: an autoradiographic and horseradish peroxidase study. Brain Res 259:21-30.
33. Henkel CK, Spangler KM. 1983. Organization of the efferent projections of the medial superior olivary nucleus in the cat as revealed by HRP and autoradiographic tracing methods. J Comp Neurol 221:416-428.
34. Hu B. 2003. Functional organization of lemniscal and nonlemniscal auditory thalamus. Exp Brain Res 153:543-549.
35. Imig TJ, Morel A. 1984. Topographic and cytoarchitectonic organization of thalamic neurons related to their targets in low-, middle-, and high-frequency representations in cat auditory cortex. J Comp Neurol 227:511-539.
36. Imig TJ, Morel A. 1985. Tonotopic organization in lateral part of posterior group of thalamic nuclei in the cat. J Neurophysiol 53:836-851.
37. Ivarsson C, de Ribaupierre Y, de Ribaupierre F. 1988. Influence of auditory localization cues on neuronal activity in the auditory thalamus of the cat. J Neurophysiol 59:586-606.
38. Jebb AH, Woolsey TA. 1977. A simple stain for myelin in frozen sections: a modification of Mahon's method. Stain Tech 52:315-318.
39. Jin Y-M, Berrebi AS. 2006. Direct projections from the superior olivary complex to the medial geniculate body in rats. ARO Abstracts 29:46.
40. Jones EG. 1985. The thalamus. New York: Plenum Press.
41. Jones EG, Powell TPS. 1971. An analysis of the posterior group of thalamic nuclei on the basis of its afferent connections. J Comp Neurol 143:185-216.
42. Kudo M, Niimi K. 1978. Ascending projections of the inferior colliculus onto the medial geniculate body in the cat studied by anterograde and retrograde tracing techniques. Brain Res 155:113-117.
43. Kudo M, Niimi K. 1980. Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J Comp Neurol 191:545-556.
44. Kuhlenbeck H, Miller RN. 1942. The pretectal region of the rabbit's brain. J Comp Neurol 76:323-365.
45. LeDoux JE, Ruggiero DA, Reis DJ. 1985. Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J Comp Neurol 242:182-213.
46. LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ. 1987. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123-146.
47. Lee CC, Imaizumi K, Schreiner CE, Winer JA. 2004. Concurrent tonotopic processing streams in auditory cortex. Cereb Cortex 14:441-451.
48. Loftus WC, Bishop DC, Saint Marie RL, Oliver DL. 2004. Organization of binaural excitatory and inhibitory inputs to the inferior colliculus from the superior olive. J Comp Neurol 472:330-344.
49. Malmierca MS, Rees A, Le Beau FEN, Bjaalie JG. 1995. Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357:124-144.
50. Malmierca MS, Merchán MA, Henkel CK, Oliver DL. 2002. Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci 22:10891-10897.
51. McMullen NT, Velenovsky DS, Holmes MG. 2005. Auditory thalamic organization: cellular slabs, dendritic arbors and tectothalamic axons underlying the frequency map. Neuroscience 136:927-943.
52. Middlebrooks JC, Zook JM. 1983. Intrinsic organization of the cat's medial geniculate body identified by projections to binaural response-specific bands in the primary auditory cortex. J Neurosci 3:203-224.
53. Molinari M, Dell'Anna ME, Rausell E, Leggio MG, Hashikawa T, Jones EG. 1995. Auditory thalamocortical pathways defined in monkeys by calcium-binding protein immunoreactivity. J Comp Neurol 362:171-194.
54. Moore RY, Goldberg JM. 1963. Ascending projections of the inferior colliculus in the cat. J Comp Neurol 121:109-135.
55. Morel A, Imig TJ. 1987. Thalamic projections to fields A, AI, P, and VP in the cat auditory cortex. J Comp Neurol 265:119-144.
56. Morel A, Rouiller E, de Ribaupierre Y, de Ribaupierre F. 1987. Tonotopic organization in the medial geniculate body (MGB) of lightly anesthetized cats. Exp Brain Res 69:24-42.
57. Morest DK. 1964. The neuronal architecture of the medial geniculate body of the cat. J Anat 98:611-630.
58. Morest DK. 1965a. The lateral tegmental system of the midbrain and the medial geniculate body: study with Golgi and Nauta methods in cat. J Anat 99:611-634.
59. Morest DK. 1965b. The laminar structure of the medial geniculate body of the cat. J Anat 99:143-160.
60. Oliver DL, Hall WC. 1978. The medial geniculate body of the tree shrew, Tupaia glis. I. Cytoarchitecture and midbrain connections. J Comp Neurol 182:423-458.
61. Oliver DL, Beckius GE, Bishop DC, Kuwada S. 1997. Simultaneous anterograde labeling of axonal layers from lateral superior olive and dorsal cochlear nucleus in the inferior colliculus of cat. J Comp Neurol 382:215-229.
62. Olucha-Bordonau FE, Pérez-Villalba A, Teruel-Martí V, Ruiz-Torner A. 2004. Chemical divisions in the medial geniculate body and surrounding paralaminar nuclei of the rat: quantitative comparison of cell density, NADPH diaphorase, acetyl choline esterase and basal expression of c-fos. J Chem Neuroanat 28:147-162.
63. Poggio GF, Mountcastle VB. 1960. A study of the functional contributions of the lemniscal and spinothalamic systems to somatic sensibility: central nervous mechanisms in pain. Bull Johns Hopkins Hosp 106:266-316.
64. Prieto JJ, Winer JA. 1999. Neurons of layer VI in cat primary auditory cortex (AI): Golgi study and sublaminar origins of projection neurons. J Comp Neurol 404:332-358.
65. Radtke-Schuller S. 2004. Cytoarchitecture of the medial geniculate body and thalamic projections to the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi). I. Temporal fields. Anat Embryol 209:59-76.
66. Ramachandran R, May BJ. 2002. Functional segregation of ITD sensitivity in the inferior colliculus of decerebrate cats. J Neurophysiol 88:2251-2261.
67. Redies H, Brandner S, Creutzfeldt OD. 1989. Anatomy of the auditory thalamocortical system of the guinea pig. J Comp Neurol 282:489-511.
68. Rodrigues-Dagaeff C, Simm G, de Ribaupierre Y, Villa A, de Ribaupierre F, Rouiller EM. 1989. Functional organization of the ventral division of the medial geniculate body of the cat: evidence for a rostro-caudal gradient of response properties and cortical projections. Hearing Res 39:103-126.
69. Ross LS, Pollak GD, Zook JM. 1988. Origin of ascending projections to an isofrequency region of the mustache bat's inferior colliculus. J Comp Neurol 270:488-505.
70. Roth GL, Aitkin LM, Andersen RA, Merzenich MM. 1978. Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 182:661-680.
71. Rouiller EM, de Ribaupierre F. 1982. Neurons sensitive to narrow ranges of repetitive acoustic transients in the medial geniculate body of the cat. Exp Brain Res 48:323-326.
72. Rouiller EM, de Ribaupierre F. 1985. Origin of afferents to physiologically defined regions of the medial geniculate body of the cat: ventral and dorsal divisions. Hearing Res 19:97-114.
73. Rouiller EM, Rodrigues-Dagaeff C, Simm G, de Ribaupierre Y, Villa A, de Ribaupierre F. 1989. Functional organization of the medial division of the medial geniculate body of the cat: tonotopic organization, spatial distribution of response properties and cortical connections. Hearing Res 39:127-142.
74. Ryan AF. 1976. Hearing sensitivity of the Mongolian gerbil, Meriones unguiculatus. J Acoust Soc Am 59:1222-1226.
75. Ryan AF, Woolf NK, Sharp FR. 1982. Tonotopic organization in the central auditory pathway of the Mongolian gerbil: a 2-deoxyglucose study. J Comp Neurol 207:369-380.
76. Samson FK, Barone P, Irons WA, Clarey JC, Poirier P, Imig TJ. 2000. Directionality derived from differential sensitivity to monaural and binaural cues in the cat's medial geniculate body. J Neurophysiol 84:1330-1345.
77. Sanes DH, Merickel M, Rubel EW. 1989. Evidence for an alteration of the tonotopic map in the gerbil cochlea during development. J Comp Neurol 279:436-444.
78. Semple MN, Aitkin LM. 1979. Representation of sound frequency and laterality by units in central nucleus of cat inferior colliculus. J Neurophysiol 42:1626-1639.
79. 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 266:519-534.
80. Velenovsky DS, Cetas JS, Price RO, Sinex DG, McMullen NT. 2003. Functional subregions in primary auditory cortex defined by thalamocortical terminal arbors: an electrophysiological and anterograde labeling study. J Neurosci 23:308-316.
81. Warr WB, de Olmos JS, Heimer L. 1981. Horseradish peroxidase. The basic procedure. In: Heimer L, Robards MJ, editors. Neuroanatomical tract-tracing methods. New York: Plenum Press. p 207-262.
82. Wenstrup JJ. 2005. The tectothalamic system. In: Winer JA, Schreiner CE, editors. The inferior colliculus. New York: Springer. p 200-230.
83. Wenstrup JJ, Grose CD. 1995. Inputs to combination-sensitive neurons in the medial geniculate body of the mustached bat: the missing fundamental. J Neurosci 15:4693-4711.
84. Wenstrup JJ, Ross LS, Pollak GD. 1986. Binaural response organization within a frequency-band representation of the inferior colliculus: implications for sound localization. J Neurosci 6:962-973.
85. Wenstrup JJ, Larue DT, Winer JA. 1994. Projections of physiologically defined subdivisions of the inferior colliculus in the mustached bat: targets in the medial geniculate body and extrathalamic nuclei. J Comp Neurol 346:207-236.
86. Willard FH, Ryugo DK. 1983. Anatomy of the central auditory system. In: Willott JF, editor. The auditory psychobiology of the mouse. Springfield, IL: Charles C Thomas. p 201-304.
87. Winer JA. 1984. The human medial geniculate body. Hearing Res 15:225-247.
88. Winer JA. 1985. The medial geniculate body of the cat. Adv Anat Embryol Cell Biol 86:1-97.
89. Winer JA. 1992. The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper AN, Fay RR, editors. The mammalian auditory pathway: neuroanatomy. Springer handbook of auditory research, vol. 1. New York: Springer. p 222-409.
90. Winer JA. 2006. Decoding the auditory corticofugal systems. Hearing Res 212:1-8.
91. 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.
92. Winer JA, Wenstrup JJ. 1994. Cytoarchitecture of the medial geniculate body in the mustached bat (Pteronotus parnelli). J Comp Neurol 346:161-182.
93. Winer JA, Morest DK, Diamond IT. 1988. A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys virginiana, with a comment on the posterior intralaminar nuclei of the thalamus. J Comp Neurol 274:422-448.
94. Winer JA, Larue DT, Diehl JJ, Hefti BJ. 1998. Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400:147-174.
95. Winer JA, Kelly JB, Larue DT. 1999. Neural architecture of the rat medial geniculate body. Hearing Res 130:19-41.
96. Winer JA, Diehl JJ, Larue DT. 2001. Projections of auditory cortex to the medial geniculate body of the cat. J Comp Neurol 430:27-55.
97. Wong D, Kelly JP. 1981. Differentially projecting cells in individual layers of the auditory cortex: a double-labeling study. Brain Res 230:362-366.
98. Wong-Riley MTT. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11-28.