The non-lemniscal auditory cortex in ferrets: Convergence of corticotectal inputs in the superior colliculus

Frontiers in Neuroanatomy

Volumn , Issue MAY, 2010, Pages

  Bajo, Victoria M ^a   Nodal, Fernando R ^a   Bizley, Jennifer K ^a   King, Andrew J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Auditory cortical fields; Corticofugal input; Multisensory integration; Neural tracers; Orientation behavior; Sound localization

Indexed keywords

ANIMAL TISSUE; ANTERIOR ECTOSYLVIAN GYRUS; ARTICLE; AUDITORY CORTEX; BRAIN CORTEX; CORTICOTECTAL PROJECTION; ECTOSYLVIAN GYRUS; FEMALE; FERRET; MALE; NERVE CELL NETWORK; NERVE PROJECTION; NONHUMAN; NONLEMNISCAL AUDITORY CORTEX; POSTERIOR ECTOSYLVIAN GYRUS; PYRAMIDAL NERVE CELL; SUPERIOR COLLICULUS;

EID: 84863102986     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. Adams, J. C. (1981). Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 29, 775
2. Allman, B. L., Keniston, L. P., and Meredith, M. A. (2009). Adult deafness induces somatosensory conversion of ferret auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 106, 5925-5930.
3. Alvarado, J. C., Stanford, T. R., Rowland, B. A., Vaughan, J. W., and Stein, B. E. (2009). Multisensory integration in the superior colliculus requires synergy among corticocollicular inputs. J. Neurosci. 29, 6580-6592
4. Alvarado, J. C., Stanford, T. R., Vaughan, J. W., and Stein, B. E. (2007). Cortex mediates multisensory but not unisensory integration in superior colliculus. J. Neurosci. 27, 12775-12786
5. Bajo, V. M., Nodal, F. R., Bizley, J. K., Moore, D. R., and King, A. J. (2007). The ferret auditory cortex: descending projections to the inferior colliculus. Cereb. Cortex 17, 475-491
6. Bajo, V. M., Nodal, F. R., Moore, D. R., and King, A. J. (2010). The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nat. Neurosci. 13, 253-260
7. Behan, M. (1985). An EM-autoradiographic and EM-HRP study of the commissural projection of the superior colliculus in the cat. J. Comp. Neurol. 234, 105-116
8. Beitel, R. E., and Kaas, J. H. (1993). Effects of bilateral and unilateral ablation of auditory cortex in cats on the unconditioned head orienting response to acoustic stimuli. J. Neurophysiol. 70, 351-369
9. Binns, K. E., Grant, S., Withington, D. J., and Keating, M. J. (1992). A topographic representation of auditory space in the external nucleus of the inferior colliculus of the guinea-pig. Brain Res. 589, 231-242
10. Bizley, J. K., and King, A. J. (2009). Visual infl uences on ferret auditory cortex. Hear. Res. 258, 55-63.
11. Bizley, J. K., Nodal, F. R., Bajo, V. M., Nelken, I., and King, A. J. (2007). Physiological and anatomical evidence for multisensory interactions in auditory cortex. Cereb. Cortex 17, 2172-2189
12. Bizley, J. K., Nodal, F. R., Nelken, I., and King, A. J. (2005). Functional organization of ferret auditory cortex. Cereb. Cortex 15, 1637-1653
13. Bowman, E. M., and Olson, C. R. (1988a). Visual and auditory association areas of the cat's posterior ectosylvian gyrus: thalamic afferents. J. Comp. Neurol. 272, 15-29
14. Bowman, E. M., and Olson, C. R. (1988b). Visual and auditory association areas of the cat's posterior ectosylvian gyrus: cortical afferents. J. Comp. Neurol. 272, 30-42
15. Burnett, L. R., Stein, B. E., Chaponis, D., and Wallace, M. T. (2004). Superior colliculus lesions preferentially disrupt multisensory orientation. Neuroscience 124, 535-547
16. Cantone, G., Xiao, J., and Levitt, J. B. (2006). Retinotopic organization of ferret suprasylvian cortex. Vis. Neurosci. 23, 61-77
17. Chevalier, G., and Mana, S. (2000). Honeycomb-like structure of the intermediate layers of the rat superior colliculus, with additional observations in several other mammals: AChE patterning. J. Comp. Neurol. 419,137-153
18. Clarey, J. C., and Irvine, D. R. (1986). Auditory response properties of neurons in the anterior ectosylvian sulcus of the cat. Brain Res. 386, 12-19
19. Clemo, H. R., and Stein, B. E. (1982). Somatosensory cortex: a 'new' somatotopic representation. Brain Res. 235, 162-168
20. Clemo, H. R., and Stein, B. E. (1983). Organization of a fourth somatosensory area of cortex in cat. J. Neurophysiol. 50, 910-925
21. Clemo, H. R., and Stein, B. E. (1986). Effects of cooling somatosensory cortex on response properties of tactile cells in the superior colliculus. J. Neurophysiol. 55, 1342-1368
22. Diamond, I. T., Jones, E. G., and Powell, T. P. (1969). The projection of the auditory cortex upon the diencephalons and brain stem in the cat. Brain Res. 15, 305-340
23. Fritz, J., Shamma, S., Elhilali, M., and Klein, D. (2003). Rapid task-related plasticity of spectrotemporal receptive fi elds in primary auditory cortex. Nat. Neurosci. 6, 1216-1223
24. Fuentes-Santamaria, V., Alvarado, J. C., McHaffi e, J. G., and Stein, B. E. (2009). Axon morphologies and convergence patterns of projections from different sensory-specifi c cortices of the anterior ectosylvian sulcus onto multisensory neurons in the cat superior colliculus. Cereb. Cortex 19, 2902-2915
25. Fuentes-Santamaria, V., Alvarado, J. C., Stein, B. E., and McHaffi e, J. G. (2008). Cortex contacts both output neurons and nitrergic interneurons in the superior colliculus: direct and indirect routes for multisensory integration. Cereb. Cortex 18, 1640-1652
26. Gundersen, H. J. (1988). The nucleator. J. Microsc. 151, 3-21
27. Harting, J. K., Updyke, B. V., and van Lieshout, D. P. (1992). Corticotectal projections in the cat: anterograde transport studies of twenty-five cortical areas. J. Comp. Neurol. 324, 379-414
28. Heffner, H. E., and Heffner, R. S. (1990). Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques. J. Neurophysiol. 64, 915-931
29. Jenkins, W. M., and Merzenich, M. M. (1984). Role of cat primary auditory cortex for sound-localization behavior. J. Neurophysiol. 52, 819-847
30. Jiang, W., Jiang, H., and Stein, B. E. (2002). Two cortical areas facilitate multisensory orientation behavior. J. Cogn. Neurosci. 14, 1240-1255
31. Jiang, W., Wallace, M. T., Jiang, H., Vaughan, J. W., and Stein, B. E. (2001). Two cortical areas mediate multisensory integration in superior colliculus neurons. J. Neurophysiol. 85, 506-522
32. Jiang, Z. D., Moore, D. R., and King, A. J. (1997). Sources of subcortical projections to the superior colliculus in the ferret. Brain Res. 755, 279-292
33. Kacelnik, O., Nodal, F. R., Parsons, C. H., and King, A. J. (2006). Traininginduced plasticity of auditory localization in adult mammals. PLoS Biol. 4, e71. doi:10.1371/journal.pbio.0040071
34. Kanaseki, T., and Sprague, J. M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. J. Comp. Neurol. 158, 319-337.
35. Kavanagh, G. L., and Kelly, J. B. (1987). Contribution of auditory cortex to sound localization by the ferret (Mustela putorius). J. Neurophysiol. 57, 1746-1766
36. Kelly, J. B., Judge, P. W., and Phillips, D. P. (1986). Representation of the cochlea in primary auditory cortex of the ferret (Mustela putorius). Hear. Res. 24, 111-115
37. King, A. J. (1993). The Wellcome Prize Lecture. A map of auditory space in the mammalian brain: neural computation and development. Exp. Physiol. 78, 559-590
38. King, A. J. (2004). The superior colliculus. Curr. Biol. 14, R335-R338
39. King, A. J., and Hutchings, M. E. (1987). Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: a map of auditory space. J. Neurophysiol. 57, 596-624
40. King, A. J., Jiang, Z. D., and Moore, D. R. (1998). Auditory brainstem projections to the ferret superior colliculus: anatomical contribution to the neural coding of sound azimuth. J. Comp. Neurol. 390, 342-365
41. Kowalski, N., Versnel, H., and Shamma, S. A. (1995). Comparison of responses in the anterior and primary auditory fields of the ferret cortex. J. Neurophysiol. 73, 1513-1523
42. Lomber, S. G., and Malhotra, S. (2008). Double dissociation of 'what' and 'where' processing in auditory cortex. Nat. Neurosci. 11, 609-616
43. Lomber, S. G., Malhotra, S., and Hall, A. J. (2007a). Functional specialization in non-primary auditory cortex of the cat: areal and laminar contributions to sound localization. Hear. Res. 229, 31-45
44. Lomber, S. G., Malhotra, S., and Sprague, J. M. (2007b). Restoration of acoustic orienting into a cortically deaf hemifi eld by reversible deactivation of the contralesional superior colliculus: the acoustic "Sprague Effect." J. Neurophysiol. 97, 979-993
45. Lomber, S. G., Payne, B. R., and Cornwell, P. (2001). Role of the superior colliculus in analyses of space: superficial and intermediate layer contributions to visual orienting, auditory orienting, and visuospatial discriminations during unilateral and bilateral deactivations. J. Comp. Neurol. 441, 44-57
46. Lovejoy, L. P., and Krauzlis, R. J. (2010). Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nat. Neurosci. 13, 261-266
47. Malhotra, S., Hall, A. J., and Lomber, S. G. (2004). Cortical control of sound localization in the cat: unilateral cooling deactivation of 19 cerebral areas. J. Neurophysiol. 92, 1625-1643
48. Malhotra, S., and Lomber, S. G. (2007). Sound localization during homotopic and heterotopic bilateral cooling deactivation of primary and nonprimary auditory cortical areas in the cat. J. Neurophysiol. 97, 26-43
49. Mana, S., and Chevalier, G. (2001). Honeycomb-like structure of the intermediate layers of the rat superior colliculus: afferent and efferent connections. Neuroscience 103, 673-693
50. Manger, P. R., Engler, G., Moll, C. K., and Engel, A. K. (2005). The anterior ectosylvian visual area of the ferret: a homologue for an enigmatic visual cortical area of the cat? Eur. J. Neurosci. 22, 706-714
51. Manger, P. R., Engler, G., Moll, C. K., and Engel, A. K. (2008). Location, architecture, and retinotopy of the anteromedial lateral suprasylvian visual area (AMLS) of the ferret (Mustela putorius). Vis. Neurosci. 25, 27-37
52. Manger, P. R., Nakamura, H., Valentiniene, S., and Innocenti, G. M. (2004). Visual areas in the lateral temporal cortex of the ferret (Mustela putorius). Cereb. Cortex 14, 676-689
53. Meredith, M. A., and Clemo, H. R. (1989). Auditory cortical projection from the anterior ectosylvian sulcus (Field AES) to the superior colliculus in the cat: an anatomical and electrophysiological study. J. Comp. Neurol. 289, 687-707
54. Meredith, M. A., Miller, L. K., Ramoa, A. S., Clemo, H. R., and Behan, M. (2001). Organization of the neurons of origin of the descending pathways from the ferret superior colliculus. Neurosci. Res. 40, 301-313
55. Middlebrooks, J. C., and Knudsen, E. I. (1984). A neural code for auditory space in the cat's superior colliculus. J. Neurosci. 4, 2621-2634
56. Mucke, L., Norita, M., Benedek, G., and Creutzfeldt, O. (1982). Physiologic and anatomic investigation of a visual cortical area situated in the ventral bank of the anterior ectosylvian sulcus of the cat. Exp. Brain Res. 46, 1-11
57. Nelken, I., Bizley, J. K., Nodal, F. R., Ahmed, B., Schnupp, J. W., and King, A. J. (2004). Large-scale organization of ferret auditory cortex revealed using continuous acquisition of intrinsic optical signals. J. Neurophysiol. 92, 2574-2588
58. Nodal, F. R., Doubell, T. P., Jiang, Z. D., Thompson, I. D., and King, A. J. (2005). Development of the projection from the nucleus of the brachium of the inferior colliculus to the superiorcolliculus in the ferret. J. Comp. Neurol. 485, 202-217
59. Nodal, F. R., Kacelnik, O., Bajo, V. M., Bizley, J. K., Moore, D. R., and King, A. J. (2010). Lesions of the auditory cortex impair azimuthal sound localization and its recalibration in ferrets. J. Neurophysiol. 103, 1209-1225
60. Olson, C. R., and Graybiel, A. M. (1987). Ectosylvian visual area of the cat: location, retinotopic organization, and connections. J. Comp. Neurol. 261, 277-294
61. Pallas, S. L., and Sur, M. (1993). Visual projections induced into the auditory pathway of ferrets: II. Corticocortical connections of primary auditory cortex. J. Comp. Neurol. 337, 317-333
62. Palmer, A. R., and King, A. J. (1982). The representation of auditory space in the mammalian superior colliculus. Nature 299, 248-249
63. Philipp, R., Distler, C., and Hoffmann, K. P. (2006). A motion-sensitive area in ferret extrastriate visual cortex: an analysis in pigmented and albino animals. Cereb. Cortex 16, 779-790
64. Ramsay, A. M., and Meredith, M. A. (2004). Multiple sensory afferents to ferret pseudosylviansulcal cortex. Neuroreport 15, 461-465
65. Scannell, J. W., Sengpiel, F., Tovée, M. J., Benson, P. J., Blakemore, C., and Young, M. P. (1996). Visual motion processing in the anterior ectosylviansulcus of the cat. J. Neurophysiol. 76, 895-907
66. Schnupp, J. W. H., and King, A. J. (1997). Coding for auditory space in the nucleus of the brachium of the inferior colliculus in the ferret. J. Neurophysiol. 78, 2717-2731
67. Serizawa, M., McHaffi e, J. G., Hoshino, K., and Norita, M. (1994). Corticostriatal and corticotectal projections from visual cortical areas 17, 18 and 18a in the pigmented rat. Arch. Histol. Cytol. 57, 493-507
68. Sprague, J. M., and Meikle, Th. Jr. (1965). The role of the superior colliculus in visually guided behavior. Exp. Neurol. 11, 115-146
69. Stecker, G. C., Harrington, I. A., Macpherson, E. A., and Middlebrooks, J. C. (2005). Spatial sensitivity in the dorsal zone (area DZ) of cat auditory cortex. J. Neurophysiol. 94, 1267-1280
70. Stein, B. E. (1978). Nonequivalent visual, auditory, and somatic corticotectal infl uences in cat. J. Neurophysiol. 41, 55-64
71. Stein, B. E. (1998). Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Exp. Brain Res. 123, 124-135
72. Stein, B. E., and Meredith, M. A. (1991). "Functional organization of the superior colliculus," in The Neural Basis of Visual Function, ed. A. G. Leventhal (Hampshire: Macmillan), 85-110
73. Swadlow, H. A., and Weyand, T. G. (1981). Efferent systems of the rabbit visual cortex: laminar distribution of the cells of origin, axonal conduction velocities, and identifi cation of axonal branches. J. Comp. Neurol. 203, 799-822
74. Thompson, G. C., and Masterton, R. B. (1978). Brain stem auditory pathways involved in reflexive head orientation to sound. J. Neurophysiol. 41, 1183-1202
75. Tigges, J., and Tigges, M. (1981). Distribution of retinofugal and corticofugal axon terminals in the superior colliculus of squirrel monkey. Invest. Ophthalmol. Vis. Sci. 20, 149-158
76. Tunkl, J. E. (1980). Location of auditory and visual stimuli in cats with superior colliculus ablations. Exp. Neurol. 68, 395-402
77. Wallace, M. N., Roeda, D., and Harper, M. S. (1997). Deoxyglucose uptake in the ferret auditory cortex. Exp. Brain Res. 117, 488-500
78. Wallace, M. T., Meredith, M. A., and Stein, B. E. (1993). Converging infl uences from visual, auditory, and somatosensory cortices onto output neurons of the superior colliculus. J. Neurophysiol. 69, 1797-1809
79. Wallace, S. F., Rosenquist, A. C., and Sprague, J. M. (1990). Ibotenic acid lesions of the lateral substantia nigra restore visual orientation behavior in the hemianopic cat. J. Comp. Neurol. 296, 222-252
80. Winer, J. A., Larue, D. T., Diehl, J. J., and Hefti, B. J. (1998). Auditory cortical projections to the cat inferior colliculus. J. Comp. Neurol. 400, 147-174
81. Yu, L., Stein, B. E., and Rowland, B. A. (2009). Adult plasticity in multisensory neurons: short-term experience-dependent changes in the superior colliculus. J. Neurosci. 29, 15910-15922.