Systematic mapping of the monkey inferior colliculus reveals enhanced low frequency sound representation

Journal of Neurophysiology

Volumn 105, Issue 4, 2011, Pages 1785-1797

  Bulkin, David A ^a   Groh, Jennifer M ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Auditory midbrain implant; Prosthetic; Tonotopy; Topography

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY RESPONSE; BRAIN MAPPING; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; INFERIOR COLLICULUS; INFORMATION PROCESSING; LOW FREQUENCY NOISE; MACACA; MALE; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; PROSTHESIS; RECORDING; RHESUS MONKEY; SOUND DETECTION; TONOTOPY;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; AUDITORY THRESHOLD; BRAIN MAPPING; ELECTRODES; FEMALE; INFERIOR COLLICULI; MACACA MULATTA; MALE; MODELS, ANIMAL; SENSORY RECEPTOR CELLS; SOUND;

EID: 79955158029     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00857.2010     Document Type: Article

References (83)

1. Aitkin L, Tran L, Syka J. The responses of neurons in subdivisions of the inferior colliculus of cats to tonal, noise and vocal stimuli. Exp Brain Res 98: 53-64, 1994.
2. Aitkin LM, Dickhaus H, Schult W, Zimmermann M. External nucleus of inferior colliculus: auditory and spinal somatosensory afferents and their interactions. J Neurophysiol 41: 837-847, 1978.
3. Aitkin LM, Kenyon CE, Philpott P. The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. J Comp Neurol 196: 25-40, 1981.
4. Aitkin LM, Phillips SC. Is the inferior colliculus and obligatory relay in the cat auditory system? Neurosci Lett 44: 259-264, 1984.
5. Aitkin LM, Webster WR, Veale JL, Crosby DC. Inferior colliculus. I. Comparison of response properties of neurons in central, pericentral, and external nuclei of adult cat. J Neurophysiol 38: 1196-1207, 1975.
6. Andersen RA, Snyder RL, Merzenich MM. The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical fields of the cat. J Comp Neurol 191: 479-494, 1980.
7. Astl J, Popelar J, Kvasnak E, Syka J. Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. Audiology 35: 335-345, 1996.
8. Calford MB, Aitkin LM. Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3: 2365-2380, 1983.
9. Cant NB. Projections from the cochlear nuclear complex to the inferior colliculus. In: The Inferior Colliculus, edited by Winer JA, Schreiner CE. New York, NY: Springer, 2005, p. 115-131.
10. Casseday JH, Covey E. Frequency tuning properties of neurons in the inferior colliculus of an FM bat. J Comp Neurol 319: 34-50, 1992.
11. Clopton BM, Winfield JA. Tonotopic organization in the inferior colliculus of the rat. Brain Res 56: 355-358, 1973.
12. Coleman JR, Clerici WJ. Sources of projections to subdivisions of the inferior colliculus in the rat. J Comp Neurol 262: 215-226, 1987.
13. Coleman M. What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. Int J Primatol 30: 55-91, 2009.
14. Colletti V, Shannon R, Carner M, Sacchetto L, Turazzi S, Masotto B, Colletti L. The first successful case of hearing produced by electrical stimulation of the human midbrain. Otol Neurotol 28: 39-43, 2007.
15. Colletti V, Shannon RV, Carner M, Veronese S, Colletti L. Progress in restoration of hearing with the auditory brainstem implant. Prog Brain Res 175: 333-345, 2009.
16. Cooper MH, Young PA. Cortical projections to the inferior colliculus of the cat. Exp Neurol 51: 488-502, 1976.
17. Dezso A, Schwarz DW, Schwarz IE. A survey of the auditory midbrain, thalamus and forebrain in the chicken (Gallus domesticus) with cytochrome oxidase histochemistry. J Otolaryngol 22: 391-396, 1993.
18. Diamond IT, Jones EG, Powell TP. The projection of the auditory cortex upon the diencephalon and brain stem in the cat. Brain Res 15: 305-340, 1969.
19. Druga R, Syka J. Ascending and descending projections to the inferior colliculus in the rat. Physiol Bohemoslov 33: 31-42, 1984a.
20. Druga R, Syka J. Neocortical projections to the inferior colliculus in the rat. (An experimental study using anterograde degeneration techniques). Physiol Bohemoslov 33: 251-253, 1984b.
21. Druga R, Syka J, Rajkowska G. Projections of auditory cortex onto the inferior colliculus in the rat. Physiol Res 46: 215-222, 1997.
22. Ehret G, Schreiner CE. Spectral and intensity coding in the auditory midbrain. In: The Inferior Colliculus, edited by Winer JA, Schreiner CE. New York, NY: Springer, 2005, p. 312-345.
23. FitzPatrick KA. Cellular architecture and topographic organization of the inferior colliculus of the squirrel monkey. J Comp Neurol 164: 185-207, 1975.
24. Gonzalez-Hernandez T, Mantolan-Sarmiento B, Gonzalez-Gonzalez B, Perez-Gonzalez H. Sources of GABAergic input to the inferior colliculus of the rat. J Comp Neurol 372: 309-326, 1996.
25. Groh JM, Kelly KA, Underhill AM. A monotonic code for sound azimuth in primate inferior colliculus. J Cogn Neurosci 15: 1217-1231, 2003.
26. Groh JM, Trause AS, Underhill AM, Clark KR, Inati S. Eye position influences auditory responses in primate inferior colliculus. Neuron 29: 509-518, 2001.
27. Harting JK, Van Lieshout DP. Projections from the rostral pole of the inferior colliculus to the cat superior colliculus. Brain Res 881: 244-247, 2000.
28. Hutson KA, Glendenning KK, Masterton RB. Acoustic chiasm. IV: Eight midbrain decussations of the auditory system in the cat. J Comp Neurol 312: 105-131, 1991.
29. Jay MF, Sparks DL. Auditory receptive fields in primate superior colliculus shift with changes in eye position. Nature 309: 345-347, 1984.
30. Jay MF, Sparks DL. Sensorimotor integration in the primate superior colliculus. I. Motor convergence. J Neurophysiol 57: 22-34, 1987a.
31. Jay MF, Sparks DL. Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals. J Neurophysiol 57: 35-55, 1987b.
32. Judge SJ, Richmond BJ, Chu FC. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20: 535-538, 1980.
33. Kalwani RM, Bloy L, Elliott MA, Gold JI. A method for localizing microelectrode trajectories in the macaque brain using MRI. J Neurosci Methods 176: 104-111, 2009.
34. Kelly JB, Glenn SL, Beaver CJ. Sound frequency and binaural response properties of single neurons in rat inferior colliculus. Hear Res 56: 273-280, 1991.
35. Knudsen EI, Konishi M. Space and frequency are represented separately in auditory midbrain of the owl. J Neurophysiol 41: 870-884, 1978.
36. Köppl C, Gleich O, Manley G. An auditory fovea in the barn owl cochlea. J Comp Physiol A 171: 695-704, 1993.
37. Kossl M, Vater M. The cochlear frequency map of the mustache bat, Pteronotus parnellii. J Comp Physiol A 157: 687-697, 1985.
38. Kudo M, Niimi K. Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J Comp Neurol 191: 545-556, 1980.
39. Kuwada S, Batra R, Stanford TR. Monaural and binaural response properties of neurons in the inferior colliculus of the rabbit: effects of sodium pentobarbital. J Neurophysiol 61: 269-282, 1989.
40. Lee CC, Sherman SM. Drivers and modulators in the central auditory pathways. Front Neurosci 4: 79, 2010.
41. Lim HH, Anderson DJ. Auditory cortical responses to electrical stimulation of the inferior colliculus: implications for an auditory midbrain implant. J Neurophysiol 96: 975-988, 2006.
42. Lim HH, Anderson DJ. Spatially distinct functional output regions within the central nucleus of the inferior colliculus: implications for an auditory midbrain implant. J Neurosci 27: 8733-8743, 2007.
43. Lim HH, Lenarz M, Lenarz T. Auditory midbrain implant: a review. Trends Amplif 13: 149-180, 2009.
44. Lim HH, Lenarz T, Anderson DJ, Lenarz M. The auditory midbrain implant: effects of electrode location. Hear Res 242: 74-85, 2008.
45. Lopez DE, Saldaña E, Nodal FR, Merchan MA, Warr WB. Projections of cochlear root neurons, sentinels of the rat auditory pathway. J Comp Neurol 415: 160-174, 1999.
46. Malmierca MS, Rees A, Le Beau FE, Bjaalie JG. Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357: 124-144, 1995.
47. Merzenich MM, Reid MD. Representation of the cochlea within the inferior colliculus of the cat. Brain Res 77: 397-415, 1974.
48. Miller KE, Casseday JH, Covey E. Relation between intrinsic connections and isofrequency contours in the inferior colliculus of the big brown bat, Eptesicus fuscus. Neuroscience 136: 895-905, 2005.
49. Moore BCJ. An Introduction to the Psychology of Hearing. Bingley, UK: Emerald, vol. XIIII, 2008.
50. Moore DR, Semple MN, Addison PD. Some acoustic properties of neurones in the ferret inferior colliculus. Brain Res 269: 69-82, 1983.
51. Morest DK. Laminar structure of inferior colliculus of cat (Abstract). In American Association of Anatomists 77th Session; 1964 Mar 31-Apr 3; Denver, CO.
52. Morest DK, Oliver DL. The neuronal architecture of the inferior colliculus in the cat: defining the functional anatomy of the auditory midbrain. J Comp Neurol 222: 209-236, 1984.
53. Muller M, Laube B, Burda H, Bruns V. Structure and function of the cochlea in the African mole rat (Cryptomys hottentotus): evidence for a low frequency acoustic fovea. J Comp Physiol A 171: 469-476, 1992.
54. Osen KK. Projection of the cochlear nuclei on the inferior colliculus in the cat. J Comp Neurol 144: 355-372, 1972.
55. Paxinos G, Huang XF, Toga AW. The Rhesus Monkey Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 2000, p. 163.
56. Pfingst BE, Hienz R, Miller J. Reaction-time procedure for measurement of hearing. II. Threshold functions. J Acoust Soc Am 57: 431-436, 1975.
57. Pfingst BE, Laycock J, Flammino F, Lonsbury-Martin B, Martin G. Pure tone thresholds for the rhesus monkey. Hear Res 1: 43-47, 1978.
58. Poon PW, Sun X, Kamada T, Jen PH. Frequency and space representation in the inferior colliculus of the FM bat, Eptesicus fuscus. Exp Brain Res 79: 83-91, 1990.
59. Populin LC, Tollin DJ, Yin TC. Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat. J Neurophysiol 92: 2151-2167, 2004.
60. Porter KK, Metzger RR, Groh JM. Representation of eye position in primate inferior colliculus. J Neurophysiol 95: 1826-1842, 2006.
61. Porter KK, Metzger RR, Groh JM. Visual- and saccade-related signals in the primate inferior colliculus. Proc Natl Acad Sci USA 104: 17855-17860, 2007.
62. Ramón Y, Cajal S. Histologie du Système Nerveux de l'Homme et des Vertébrés, Paris: A. Maloine, vol. 1, 1911, p. 997.
63. Robards MJ. 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: 547-565, 1979.
64. RoBards MJ, Watkins DW III, Masterton RB. An anatomical study of some somesthetic afferents to the intercollicular terminal zone of the midbrain of the opossum. J Comp Neurol 170: 499-524, 1976.
65. Robinson DA. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10: 137-145, 1963.
66. Rockel AJ, Jones EG. The neuronal organization of the inferior colliculus of the adult cat. I. The central nucleus. J Comp Neurol 147: 11-60, 1973a.
67. Rockel AJ, Jones EG. The neuronal organization of the inferior colliculus of the adult cat. II. The pericentral nucleus. J Comp Neurol 149: 301-334, 1973b.
68. Rockel AJ, Jones EG. Observations on the fine structure of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 147: 61-92, 1973c.
69. Rose JE, Greenwood DD, Goldberg JM, Hind JE. Some discharge characteristics of single neurons in the inferior colliculus of the cat. I. Tonotopical organization, relation of spike-counts to tone intensity, and firing patterns of single elements. J Neurophysiol 26: 294-320, 1963.
70. Ross DA, Groh JM. Performance of monkeys on a frequency discrimination task involving pitch direction (higher vs. lower) judgments. In: Society for Neuroscience Annual Meeting. Chicago, IL: 2009.
71. Ryan A, Miller J. Single unit responses in the inferior colliculus of the awake and performing rhesus monkey. Exp Brain Res 32: 389-407, 1978.
72. Saldaña E, Feliciano M, Mugnaini E. Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 371: 15-40, 1996.
73. Saldaña E, Merchan MA. Intrinsic and commissural connections of the rat inferior colliculus. J Comp Neurol 319: 417-437, 1992.
74. Schofield BR. Projections to the inferior colliculus from layer VI cells of auditory cortex. Neuroscience 159: 246-258, 2009.
75. Schofield BR. Superior olivary complex and lateral lemniscal connections of the auditory midbrain. In: The Inferior Colliculus, edited by Winer JA, Schreiner CE. New York, NY: Springer, 2005, p. 132-154.
76. Stebbins WC, Green S, Miller FL. Auditory sensitivity of the monkey. Science 153: 1646-1647, 1966.
77. Stiebler I, Ehret G. Inferior colliculus of the house mouse. I. A quantitative study of tonotopic organization, frequency representation, and tone-threshold distribution. J Comp Neurol 238: 65-76, 1985.
78. Syka J, Popelar J, Kvasnak E, Astl J. Response properties of neurons in the central nucleus and external and dorsal cortices of the inferior colliculus in guinea pig. Exp Brain Res 133: 254-266, 2000.
79. Wessberg J, Stambaugh CR, Kralik JD, Beck PD, Laubach M, Chapin JK, Kim J, Biggs SJ, Srinivasan MA, Nicolelis MAL. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408: 361-365, 2000.
80. Willott JF, Urban GP. Response properties of neurons in nuclei of the mouse inferior colliculus. J Comp Physiol A 127: 175-184, 1978.
81. Winer JA, Chernock ML, Larue DT, Cheung SW. Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey. Hear Res 168: 181-195, 2002.
82. Zook JM, Winer JA, Pollak GD, Bodenhamer RD. Topology of the central nucleus of the mustache bat's inferior colliculus: correlation of single unit properties and neuronal architecture. J Comp Neurol 231: 530-46, 1985.
83. Zwiers MP, Versnel H, Van Opstal AJ. Involvement of monkey inferior colliculus in spatial hearing. J Neurosci 24: 4145-4156, 2004.