Abstract
The head-related transfer function (HRTF) of the cat adds directionally dependent energy minima to the amplitude spectrum of complex sounds. These spectral notches are a principal cue for the localization of sound source elevation. Physiological evidence suggests that the dorsal cochlear nucleus (DCN) plays a critical role in the brainstem processing of this directional feature. Type O units in the central nucleus of the inferior colliculus (ICC) are a primary target of ascending DCN projections and, therefore, may represent midbrain specializations for the auditory processing of spectral cues for sound localization. Behavioral studies confirm a loss of sound orientation accuracy when DCN projections to the inferior colliculus are surgically lesioned. This study used simple analogs of HRTF notches to characterize single-unit response patterns in the ICC of decerebrate cats that may contribute to the directional sensitivity of the brain's spectral processing pathways. Manipulations of notch frequency and bandwidth demonstrated frequency-specific excitatory responses that have the capacity to encode HRTF-based cues for sound source location. These response patterns were limited to type O units in the ICC and have not been observed for the projection neurons of the DCN. The unique spectral integration properties of type O units suggest that DCN influences are transformed into a more selective representation of sound source location by a local convergence of wideband excitatory and frequency-tuned inhibitory inputs.
Keywords: sound localization, head-related transfer function, dorsal cochlear nucleus, central nucleus, spectral integration
Full Text
The Full Text of this article is available as a PDF (524.1 KB).
Acknowledgements
E. Young contributed archival data from his previous studies of the dorsal cochlear nucleus. This work was supported by National Institute of Deafness and Other Communication Disorders grant 5R01DC00954. Pharmacological manipulations were performed in conjunction with NIDCD grant 1R03DC03758.
References
- 1.Aitkin LM, Martin RL. The representation of stimulus azimuth by high best-frequency azimuth-selective neurons in the central nucleus of the inferior colliculus of the cat. J. Neurophysiol. 1987;57:1185–1200. doi: 10.1152/jn.1987.57.4.1185. [DOI] [PubMed] [Google Scholar]
- 2.Aitkin LM, Martin RL. Neurons in the inferior colliculus of cats sensitive to sound-source elevation. Hear. Res. 1990;50:97–105. doi: 10.1016/0378-5955(90)90036-O. [DOI] [PubMed] [Google Scholar]
- 3.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. 1975;38:1195–1207. doi: 10.1152/jn.1975.38.5.1196. [DOI] [PubMed] [Google Scholar]
- 4.Batra R, Kuwada S, Fitzpatrick DC. Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. J. Neurophysiol. 1997;78:1222–1236. doi: 10.1152/jn.1997.78.3.1222. [DOI] [PubMed] [Google Scholar]
- 5.Cant NB, Casseday JH. Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J. Comp. Neurol. 1986;247:457–476. doi: 10.1002/cne.902470406. [DOI] [PubMed] [Google Scholar]
- 6.Casseday JH, Neff WD. Localization of pure tones. J. Acoust. Soc. Am. 1973;54:365–372. doi: 10.1121/1.1913586. [DOI] [PubMed] [Google Scholar]
- 7.Clements M, Kelly JB. Auditory spatial responses of young guinea pigs (Cavia porcellus) during and after ear plugging. J. Comp. Physiol. Psychol. 1978;92:34–44. doi: 10.1037/h0077424. [DOI] [PubMed] [Google Scholar]
- 8.Davis KA. Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus. J. Neurophysiol. 2002;87:1824–1835. doi: 10.1152/jn.00769.2001. [DOI] [PubMed] [Google Scholar]
- 9.Davis KA, Ding J, Benson TE, Voigt HF. Response properties of units in the dorsal cochlear nucleus of unanesthetized decerberate gerbil. J. Neurophysiol. 1996;75:1411–1431. doi: 10.1152/jn.1996.75.4.1411. [DOI] [PubMed] [Google Scholar]
- 10.Davis KA, Ramachandran R, May BJ. Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. J. Neurophysiol. 1999;82:164–175. doi: 10.1152/jn.1999.82.1.164. [DOI] [PubMed] [Google Scholar]
- 11.Delgutte B, Joris PX, Litovsky RY, Yin TC. Receptive fields and binaural interactions for virtual-space stimuli in the cat inferior colliculus. J. Neurophysiol. 1999;81:2833–2851. doi: 10.1152/jn.1999.81.6.2833. [DOI] [PubMed] [Google Scholar]
- 12.Havey DC, Caspary DM. A simple technique for constructing ‘piggy-back' multibarrel microelectrodes. Electroenceph. Clin. Neurophysiol. 1980;48:249–251. doi: 10.1016/0013-4694(80)90313-2. [DOI] [PubMed] [Google Scholar]
- 13.Heffner RS, Heffner HE. Localization of noise, use of binaural cues, and a description of the superior olivary complex in the smallest carnivore, the least weasel (Mustel nivalis). Behav. Neurosci. 1987;101:701–708. doi: 10.1037//0735-7044.101.5.701. [DOI] [PubMed] [Google Scholar]
- 14.Heffner RS, Heffner HE. Sound localization and use of binaural cues by the gerbil (Mustel nivalis). Behav. Neurosci. 1988a;102:422–428. doi: 10.1037//0735-7044.102.3.422. [DOI] [PubMed] [Google Scholar]
- 15.Heffner RS, Heffner HE. Sound localization in a predatory rodent, the northern grasshopper mouse (Onychomys leucogaster). J. Comp. Psychol. 1988b;102:66–71. doi: 10.1037/0735-7036.102.1.66. [DOI] [PubMed] [Google Scholar]
- 16.Huang AY, May BJ. Sound orientation behavior in cats. II. Mid-frequency spectral cues for sound localization. J. Acoust. Soc. Am. 1996a;100:1070–1080. doi: 10.1121/1.416293. [DOI] [PubMed] [Google Scholar]
- 17.Huang AY, May BJ. Spectral cues for sound localization in cats. Effects of frequency domain on minimum audible angles in the median and horizontal planes. J. Acoust. Soc. Am. 1996b;100:2341–2348. doi: 10.1121/1.417943. [DOI] [PubMed] [Google Scholar]
- 18.Imig TJ, Bibikov NG, Poirier P, Samson FK. Directionality derived from pinna-cue spectral notches in cat dorsal cochlear nucleus. J. Neurophysiol. 2000;83:907–925. doi: 10.1152/jn.2000.83.2.907. [DOI] [PubMed] [Google Scholar]
- 19.Imig TJ, Poirier P, Irons WA, Samson FK. Monaural spectral contrast mechanism for neural sensitivity to sound direction in the medial geniculate body of the cat. J. Neurophysiol. 1997;78:2754–2771. doi: 10.1152/jn.1997.78.5.2754. [DOI] [PubMed] [Google Scholar]
- 20.Irvine DRF. The Auditory Brainstem. In: Autrum H, Ottoson D, Perl ER, Schmidt RF, Shimazu H, Willis D, editors. Progress in Sensory Physiology, Vol. 7. Berlin: Springer–Verlag; 1986. pp. 128–211. [Google Scholar]
- 21.Kelly JB, Potash M. Directional responses to sounds in young gerbils (Meriones unguiculatus). J. Comp. Psychol. 1986;100:37–45. doi: 10.1037//0735-7036.100.1.37. [DOI] [PubMed] [Google Scholar]
- 22.LeBeau FE, Malmierca MS, Rees A. Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J. Neurosci. 2001;21:7303–7312. doi: 10.1523/JNEUROSCI.21-18-07303.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.May BJ. Role of the dorsal cochlear nucleus in the sound localization behavior of cats. Hear. Res. 2000;148:74–87. doi: 10.1016/S0378-5955(00)00142-8. [DOI] [PubMed] [Google Scholar]
- 24.May BJ, Huang AY. Sound orientation behavior in cats: I. Localization of broadband noise. J. Acoust. Soc. Am. 1996;100:1059–1069. doi: 10.1121/1.416292. [DOI] [PubMed] [Google Scholar]
- 25.May BJ, Huang AY. Spectral cues for sound localization in cats: A model for discharge rate representations in the auditory nerve. J. Acoust. Soc. Am. 1997;101:2705–2719. doi: 10.1121/1.418559. [DOI] [PubMed] [Google Scholar]
- 26.Masterton RB. Neurobehavioral studies of the central auditory system. Ann. Otol. Rhinol. Laryngol. 1997;Suppl 168:31–34. [PubMed] [Google Scholar]
- 27.Merzenich MM, Reid MD. Representation of the cochlea within the inferior colliculus of the cat. Brain. Res. 1974;77:397–415. doi: 10.1016/0006-8993(74)90630-1. [DOI] [PubMed] [Google Scholar]
- 28.Musicant AD, Chan JC, Hind JE. Direction-dependent spectral properties of cat external ear: new data and cross-species comparisons. J. Acoust. Soc. Am. 1990;87:757–781. doi: 10.1121/1.399545. [DOI] [PubMed] [Google Scholar]
- 29.Nelken I, Young ED. Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus. I. Regions of linear interaction. J. Neurophysiol. 1997;78:800–811. doi: 10.1152/jn.1997.78.2.790. [DOI] [PubMed] [Google Scholar]
- 30.Nelken I, Young ED. Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV neurons to narrowband and wideband stimuli. J. Neurophysiol. 1994;71:2446–2462. doi: 10.1152/jn.1994.71.6.2446. [DOI] [PubMed] [Google Scholar]
- 31.Oliver DL, Beckius G. Fine structure of GABA-labeled axonal endings in the inferior colliculus of the cat. Immunocytochemistry on deplasticized ultrathin sections. Neuroscience. 1992;46:455–463. doi: 10.1016/0306-4522(92)90065-a. [DOI] [PubMed] [Google Scholar]
- 32.Oliver DL, Beckius GE, Bishop DC, Kuwada S. Simultaneous anterograde labeling of axonal layers from lateral superior olive and dorsal cochlear nucleus in the inferior colliculus of cat. J. Comp. Neurol. 1997;382:215–229. doi: 10.1002/(SICI)1096-9861(19970602)382:2<215::AID-CNE6>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
- 33.Pollak GD, Park TJ. The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus. Hear. Res. 1993;65:99–117. doi: 10.1016/0378-5955(93)90205-F. [DOI] [PubMed] [Google Scholar]
- 34.Poon PWF, Brugge JF. Sensitivity of auditory nerve fibers to spectral notches. J. Neurophysiol. 1993;70:655–666. doi: 10.1152/jn.1993.70.2.655. [DOI] [PubMed] [Google Scholar]
- 35.Ramachandran R, Davis KA, May BJ. Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J. Neurophysiol. 1999;82:152–163. doi: 10.1152/jn.1999.82.1.152. [DOI] [PubMed] [Google Scholar]
- 36.Ramachandran R, Davis KA, May BJ. Rate representation of tones in noise in the inferior colliculus of decerebrate cats. J. Assoc. Res. Otolaryngol. 2000;1:144–160. doi: 10.1007/s101620010029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Ramachandran R, May BJ. Sensitivity to interaural time differences in the inferior colliculus of decerberate cats. J. Neurophysiol., in press.
- 38.Rees A, Palmer AR. Rate–intensity functions and their modification by broadband noise for neurons in the guinea pig inferior colliculus. J. Acoust. Soc. Am. 1988;83:1488–1498. doi: 10.1121/1.395904. [DOI] [PubMed] [Google Scholar]
- 39.Rice JJ, May BJ, Spirou GA, Young ED. Pinna based spectral cues for sound localization in cat. Hear. Res. 1992;58:132–152. doi: 10.1016/0378-5955(92)90123-5. [DOI] [PubMed] [Google Scholar]
- 40.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. 1963;26:294–320. doi: 10.1152/jn.1963.26.2.321. [DOI] [PubMed] [Google Scholar]
- 41.Ryan AF, Miller J. Single unit responses in the inferior colliculus of the awake and performing rhesus monkey. Exp. Brain Res. 1978;32:389–407. doi: 10.1007/BF00238710. [DOI] [PubMed] [Google Scholar]
- 42.Ryugo DK, Willard FH, Fekete DM. Differential afferent projections to the inferior colliculus from the cochlear nucleus in the albino mouse. Brain Res. 1981;210:342–349. doi: 10.1016/0006-8993(81)90907-0. [DOI] [PubMed] [Google Scholar]
- 43.Samson FK, Clarey JC, Barone P, Imig TJ. Effects of ear plugging on single-unit azimuth sensitivity in cat primary auditory cortex. I. Evidence for monaural directional cues. J. Neurophysiol. 1993;70:492–511. doi: 10.1152/jn.1993.70.2.492. [DOI] [PubMed] [Google Scholar]
- 44.Semple MN, Kitzes LM. Binaural processing of sound pressure level in the inferior colliculus. J. Neurophysiol. 1987;57:1130–1147. doi: 10.1152/jn.1987.57.4.1130. [DOI] [PubMed] [Google Scholar]
- 45.Shneiderman A, Chase MB, Rockwood JM, Benson CG, Potashner SJ. Evidence for a GABAergic projection from the dorsal nucleus of the lateral lemniscus to the inferior colliculus. J. Neurochem. 1993;60:72–82. doi: 10.1111/j.1471-4159.1993.tb05824.x. [DOI] [PubMed] [Google Scholar]
- 46.Shu ZJ, Swindale NV, Cynader MS. Spectral motion produces an auditory after-effect. Nature. 1993;364:721–723. doi: 10.1038/364721a0. [DOI] [PubMed] [Google Scholar]
- 47.Spitzer MW, Semple MN. Interaural phase coding in the auditory midbrain: Influence of dynamic stimulus features. Science. 1991;254:721–724. doi: 10.1126/science.1948053. [DOI] [PubMed] [Google Scholar]
- 48.Sutherland DP, Masterton RB, Glendenning KK. Role of acoustic striae in hearing: reflexive responses to elevated sound-sources. Behav. Brain Res. 1998;97:1–12. doi: 10.1016/S0166-4328(98)00008-4. [DOI] [PubMed] [Google Scholar]
- 49.Wightman FL, Kistler DJ. Headphone simulation of free-field listening. I. Stimulus synthesis. J. Acoust. Soc. Am. 1989;85:868–878. doi: 10.1121/1.397558. [DOI] [PubMed] [Google Scholar]
- 50.Willott JF, Parham K, Hunter KP. Response properties of inferior colliculus neurons in young and very old CBA/J mice. Hear. Res. 1998;37:1–14. doi: 10.1016/0378-5955(88)90073-1. [DOI] [PubMed] [Google Scholar]
- 51.Young ED, Brownell WE. Responses to tones and noise of single cells in the dorsal cochlear nucleus of unanesthetized cats. J. Neurophysiol. 1979;39:282–300. doi: 10.1152/jn.1976.39.2.282. [DOI] [PubMed] [Google Scholar]
- 52.Young ED, Nelken I, Conley RA, Tong SC. Somatosensory effects on neurons in dorsal cochlear nucleus. J. Neurophysiol. 1995;73:743–765. doi: 10.1152/jn.1995.73.2.743. [DOI] [PubMed] [Google Scholar]
- 53.Young ED, Rice JJ, Tong SC. Effects of pinna position on head-related transfer functions in the cat. J. Acoust. Soc. Am. 1996;99:3064–3076. doi: 10.1121/1.414883. [DOI] [PubMed] [Google Scholar]
- 54.Young ED, Spirou GA, Rice JJ, Voigt HF. Neural organization and responses to complex stimuli in the dorsal cochlear nucleus. Philos. Trans. R. Soc. Lond. Biol. Sci. 1992;336:407–413. doi: 10.1098/rstb.1992.0076. [DOI] [PubMed] [Google Scholar]