Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig
Corresponding Author
Manuel S. Malmierca
Department of Physiological Sciences, The Medical School, University of Newcastle Upon Tyne, United Kingdom
Laboratorio de Neurobiología de la Audición, Departamento de Biología Celular y Patología, Facultad de Medicina, Universidad de Salamanca, Avda. Campo Charro, s/n, 37007 Salamanca, SpainSearch for more papers by this authorAdrian Rees
Department of Physiological Sciences, The Medical School, University of Newcastle Upon Tyne, United Kingdom
Search for more papers by this authorFiona E. N. Le Beau
Department of Physiological Sciences, The Medical School, University of Newcastle Upon Tyne, United Kingdom
Search for more papers by this authorJan G. Bjaalie
Department of Anatomy, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway
Search for more papers by this authorCorresponding Author
Manuel S. Malmierca
Department of Physiological Sciences, The Medical School, University of Newcastle Upon Tyne, United Kingdom
Laboratorio de Neurobiología de la Audición, Departamento de Biología Celular y Patología, Facultad de Medicina, Universidad de Salamanca, Avda. Campo Charro, s/n, 37007 Salamanca, SpainSearch for more papers by this authorAdrian Rees
Department of Physiological Sciences, The Medical School, University of Newcastle Upon Tyne, United Kingdom
Search for more papers by this authorFiona E. N. Le Beau
Department of Physiological Sciences, The Medical School, University of Newcastle Upon Tyne, United Kingdom
Search for more papers by this authorJan G. Bjaalie
Department of Anatomy, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway
Search for more papers by this authorAbstract
We present a comprehensive description of the local (intrinsic and commissural) connections in the central nucleus of the inferior colliculi (CNICs) in guinea pig. Focal injections of the anterograde tracer biocytin were made into physiologically identified loci of the CNIC and the spatial organisation of the labeled fibres was revealed with computer-assisted threedimensional (3-D) reconstruction.
The intrinsic fibres form a series of V-shaped laminar plexuses composed of fibres bearing both terminal and en passant boutons. Each laminar plexus has a central wing located in the CNIC that extends into the dorsal cortex and an external wing located in the external cortex. The edge where the two wings intersect delimits the lateral border of the central nucleus with the external cortex. The density of labeled terminals was consistently lower in the cortices than in the CNIC. The laminar plexus connects points of similar frequency within the CNIC. Seen in 3-D, the location, orientation, shape, and area of the laminar plexus vary as a function of best frequency. The commissural fibres ending in the contralateral IC to the injection also form a laminar plexus which is symmetrical to the ipsilateral plexus. Electrolytic lesions placed in the contralateral IC at sites with best frequencies corresponding to those of the injection coincided with the terminals of the commissural fibres in most instances. Possible patterns for the organisation of these connections (point-to-point and diverging) are discussed.
Three systems of peripheral axons to the laminar plexus are described: parallel, oblique, and perpendicular to the central wing. The novel parallel system has terminals in both ICs that run parallel to the central wing. It might constitute the anatomical basis for across-frequency interactions. The oblique and perpendicular systems are fibres of passage projecting to the commissure and brachium of the IC, respectively. © 1995 Wiley-Liss, Inc.
Literature Cited
- Adams, J. C. (1980) Crossed and descending projections to the inferior colliculus. Neurosci. Lett. 19: 1–5.
- Adams, J. C. (1981) Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 29: 775.
-
Aitkin, L. M.
(1986)
The Auditory Midbrain.
Clifton. NJ:
Humana.
10.1385/0896030857 Google Scholar
- Aitkin, L. M., S., Fryman, D. W. Blake, and W. R. Webster (1972) Responses of neurones in the rabbit inferior colliculus. I. Frequency-specificity and topographic arrangement. Brain Res. 47: 77–90.
- Aitkin, L. M., H., Dickhaus, W. Schult, and M. Zimmermann (1978) External nucleus of inferior colliculus: auditory and spinal somatosensory afferents and their interactions. J. Neurophysiol. 41: 837–847.
- Aitkin, L. M., C. E., Kenyon, and P. Philpott (1981) The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. J. Comp. Neurol. 196: 25–40.
- Andersen, R. A., R. L. Snyder, M. M. Merzenich (1980) The tonotopic organization of the corticocollicular projections from physiologically defined loci in the AI, AII, and anterior auditory cortical fields of the cat. J. Comp. Neurol. 191: 479–497.
- Bajo, V. M., M. A., Merchán, D. E. López, and E. M. Rouiller (1993) Neuronal morphology and efferent projections of the dorsal nucleus of the lateral lemniscus in the rat. J. Comp. Neurol, 334: 241–262.
- Bjaalie, J. G. (1992) Three-dimensional computer reconstructions in neuroanatomy. Basic principles and methods for quantitative analysis. In M. G. Stewart, (ed): Quantitative Methods in Neuroanatomy. Chichester: John Wiley & Sons, pp. 249–294.
- Bjaalie, J. G., P. J., Diggle, A. Nikundiwe, T. Karagdlle, and P. Brodal (1991) Spatial segregation between populations of ponto-cerebellar neurons. Statistical analysis of multivariate spatial interactions. Anat. Rec. 231: 510–523.
- Brunso-Bechtold, J. K., G. C., Thompson, and R. B. Masterton (1981) HRP study of the organization of auditory afferents ascending to central nucleus of the inferior colliculus in cat. J. Comp. Neurol. 197: 705–722.
- Casseday, J. H. Ehrlich, D. Covey, E. (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264: 847–850.
- Coleman, J. R., and W. J. Clerici (1987) Sources of projections to subdivisions of the inferior colliculus in the rat. J. Comp. Neurol. 262: 215–226.
- Faye-Lund, H. (1985) The neocortical projection to the inferior colliculus in the albino rat. Anat. Embryol. (Berl.) 173: 53–70.
- Faye-Lund, H., and K. K. Osen (1985) Anatomy of the inferior colliculus in rat. Anat Embryol. (Berl.) 171: 1–20.
- Flecknell, P. A. (1988) Laboraccory Animal Anaesthesia. London: Academie: Press.
- FitzPatrick, K. A. (1975) Cellular architecture and topographic organization of the inferior colliculus of the squirrel monkey. J. Comp. Neurol. 164: 185–208.
-
González Hernández, T. H.,
G. Meyer, and
R. Ferres Torres
(1986)
The commissural interconnections of the inferior colliculus in the albino mouse.
Brain Res.
368:
268–276.
10.1016/0006-8993(86)90571-8 Google Scholar
- Hewitt, M. J., and R. Meddis (1994) A computer model of amplitudemodulation sensitivity of single units in the inferior colliculus. J. Acoust. Soc. Am. 95: 1–15.
- Huang, C.-M., and J. Fex (1986) Tonotopic organization in the inferior colliculus of the rat demonstrated with the 2-deoxyglucose method. Exp. Brain Res. 61: 506–512.
- Huffman, R. F., and O. W. Henson, Jr. (1990) The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res. Rev. 15: 295–323.
- Hutson, K. A., K. K., Glendenning, and R. B. Masterton (1991) Acoustic Chiasm IV: eight midbrain decussations of the auditory system in the cat. J. Comp. Neurol. 312: 105–131.
- Irvine, D. R. F. (1992) Physiology of the auditory brainstem. In A. Popper and R. R. Fay (eds): Mammalian Auditory Pathway: Neurophysiology. New York: Springer Verlag, pp. 153–231.
- Izzo, P. N. (1991) A note on the use of biocytin in anterograde tracing studies in the central nervous system: application at both light and electron microscopic level. J. Neurosci. Methods 36: 155–166.
- King, M. A., P. M., Louis, B. E. Hunter, and D. W. Walker (1989) Biocytin: a versatile anterograde neuroanatomical tract-tracing alternative. Brain Res. 497: 361–367.
- Kita, H., and W. Armstrong (1991) A biotin-containing compound N-(2-aminoethyl) biotinamide for intracellular labelling and neuronal tracing studies: comparison with biocytin. J. Neurosci. Methods 37: 141–150.
- Kudo, M., and K. Niimi (1980) Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J. Comp. Neurol. 191: 545–556.
- Langner, G. (1988) Physiological properties of units in the cochlear nucleus are adequate for model of periodicity analysis in the auditory midbrain. In J. Syka and R. B. Masterton (eds): Auditory Pathway: Structure and Function. New York: Plenum Press, pp. 207–212.
- Langner, G. (1992) Periodicity coding in the auditory system. Hearing Res. 6: 115–149.
- Langner, G., and C. E. Schreiner (1987) Spatial representation of the auditory parameters in the inferior colliculus of the cat. Neurosci. Suppl. Abstr. 22: 5721.
- Langner, G., and C. E. Schreiner (1989) Orthogonal topographical representation of characteristic and best modulation frequency in the inferior colliculus of the cat. Soc. Neurosci. Abstr. 15: 1116.
- Malmierca, M. S. (1991) Computer-assisted 3-D reconstructions of Golgi impregnated cells in the rat inferior colliculus. Doctoral thesis, Universities of Oslo and Salamanca.
- Malmierca, M. S., T. W., Blackstad, K. K. Osen, T. Karagülle, and R. L. Molowny (1993a) The central nucleus of the inferior colliculus in rat: a Golgi and computer reconstruction study of neuronal and laminar structure. J. Comp. Neurol. 333: 1–27.
- Malmierca, M. S., A. Rees, F. E. N. Le Beau (1993b) The intrinsic and commissural fibre systems of the guinea-pig inferior colliculus: morphological and physiological correlates. Assoc. Res. Otolaryngol. Abstr. 16: 127.
- Malmierca, M. S., A. Rees, F. E. N. Le Beau (1993c) The descending projections of the guinea-pig central nucleus of the inferior colliculus (CNIC). Eur. J. Neurosci. [Suppl.] 16: 204.
- Malmierca, M. S., A. Rees, F. E. N. Le Beau, and J. G. Bjaalie (1994) The topography of frequency-band laminae in the guinea-pig inferior colliculus. J. Physiol. (Lond.) 480P: 108–109.
- Malmierca, M. S., K. L., Seip, and K. K. Osen (1995) Morphological classification and identification of neurones in the inferior colliculus: a multivariate analysis. Anat. Embryol. (Berl.) 191: 343–350.
- Martin, R. L., W. R., Webster, and J. Servière (1988) The frequency organization of the inferior colliculus of the guinea-pig: a 14 C-2-deoxyglucose study. Hear. Res. 33: 245–256.
- McDonald, A. J. (1992) Neuroanatomical labeling with biocytin: a review. Neuroreport 3: 821–827.
- Merchán, M. A., E., Saldafia, and I. Plaza (1994) Dorsal nucleus of the lateral lemniscus in the rat; concentric organization and tonotopic projection to the inferior colliculus. J. Comp. Neurol. 342: 259–278.
- Merzenich, M. M., and M. D. Reid (1974) Representation of the cochlea within the inferior colliculus of the cat. Brain Res. 77: 397–415.
- Mittmann, D. H., and J. J. Wenstrup (1994) Combination-sensitive neurons in the inferior colliculus of the mustache bat. Assoc. Res. Otolaryngol. Abst. 17: 93.
- Morest, D. K. (1964) The laminar structure of the inferior colliculus of the cat. Anat. Rec. 148: 314.
- Morest, D. K., and D. L. Oliver (1984) The neuronal architecture of the inferior colliculus in the cat: defining the functional anatomy of the auditory midbrain. J. Comp. Neurol. 222: 209–236.
- Nikundiwe, A. M., J. G., Bjaalie, and P. Brodal (1994) Lamellar organization of the pontocerebellar neuronal populations. A multi-tracer and 3-D computer reconstruction study in the cat. Eur. J. Neurosci. 6: 173–186.
- Oliver, D. L. (1984) Dorsal cochlear nucleus projections to the inferior colliculus in the cat: a light and electron microscopic study. J. Comp. Neurol. 224: 155–172.
- Oliver, D. L. (1987) Projection to the inferior colliculus from the ventral cochlear nucleus in the cat: possible substrates for binaural interaction. J. Comp. Neurol. 264: 24–46.
- Oliver, D. L., and D. K. Morest (1984) The central nucleus of the inferior colliculus in the cat. J. Comp. Neurol. 222: 237–264.
- Oliver, D. L., and A. Shneiderman (1991) The anatomy of the inferior colliculus. A cellular basis for integration of monaural and binaural information. In R. A. Altschuler, R. P. Bobbin, B. M. Clopton, and D. W. Hoffmann (eds): Neurobiology of Hearing, Vol. II: The Central Auditory System New York: Raven Press, pp. 195–222.
- Oliver, D. L., S., Kuwada, T. C. T. Yin, L. B. Haberly, and C. K. Henkel (1991) Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J. Comp. Neurol. 303: 75–100.
- Rees, A. (1990) A closed-field sound system for auditory neurophysiology. J. Physiol. (Lond.) 430P: 2.
- RoBards, M. J., D. W. Watkins III, and R. B. Masterton (1976) An anatomical study of some somesthetic afferents to the intercollicular terminal zone of the midbrain of the opossum, J. Comp. Neurol. 170: 499–524.
- Rockel, A. J., and E. G. Jones (1973a) The neuronal organization of the inferior colliculus of the adult cat. I. The central nucleus. J. Comp. Neurol. 147: 11–60.
- Rockel, A. J., and E. G. Jones (1973b) The neuronal organization of the inferior colliculus of the adult cat. II. The pericentral nucleus. J. Comp. Neurol. 149: 301–334.
- Rose, J. E., D. D., Greenwood, J. M. Goldberg, and J. E. Hind (1963) 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.
- Ross, L. S., and G. D. Pollak (1989) Differential ascending projections to aural regions in the 60 kHz contour of the mustache bat's inferior colliculus. J. Neurosci. 9: 2819–2834.
- Ryan, A. F., N. K., Woolf, and F. R. Sharp (1982) Tonotopic organization in the central auditory pathway of the Mongolian gerbil: a 2-deoxyglucose study. J. Comp. Neurol. 207: 369–380.
- Ryan, A. F., Z., Furlow, N. K. Woolf, and E. M. Keithley (1988) The spatial representation of frequency in the rat dorsal cochlear nucleus and inferior colliculus. Hear. Res. 36: 181–190.
- Ryugo, D. K., F. H., Willard, and D. M. Fekete (1981) Differential afferent projections to the inferior colliculus from the cochlear nucleus in the albino mouse. Brain Res. 210: 342–349.
- Saldaña, E., and M. A. Merchán (1992) Intrinsic and commissural connections of the rat inferior colliculus. J. Comp. Neurol. 319: 417–437.
- Schreiner, C. E., and G. Langner (1988) Coding of temporal patterns in the central auditory nervous system. In G. M. Edelman, W. E. Gall, and W. M. Cowan (eds): Auditory Function. Neurobiological Bases of Hearing. New York: John Wiley & Sons, pp. 337–361.
- Semple, M. N., and Aitkin, L. M. (1979) Representation of sound frequency and laterality by units in central nucleus of cat inferior colliculus. J. Neurophysiol. 42: 1626–1639.
- Servière, J., W. R., Webster, and M. B. Calford (1984) Iso-frequency labelling revealed by a combined [14C] -2-deoxyglucose, electrophysiological, and horseradish peroxidase study of the inferior colliculus of the cat. J. Comp. Neurol. 228: 463–477.
- Shneiderman, A., D. L., Oliver, and C. K. Henkel (1988) Connections of the dorsal nucleus of the lateral lemniscus: an inhibitory parallel pathway in the ascending auditory system? J. Comp. Neurol. 276: 188–208.
- Spangler, K. M., and W. B. Warr (1991) The descending auditory system, In R. A. Altschuler, R. P. Bobbin, B. M. Clopton, and D. W. Hoffmann (eds): Neurobiology of Hearing: Vol. II, The Central Auditory System. New York: Raven Press, pp. 27–45.
- Toga, A. W. (1990) Three-Dimensional Neuroimaging. New York: Raven Press.
- van Noort, J. (1969) The structure and connections of the inferior colliculus. An investigation of the lower auditory system. Proefschrift. Leiden: van Gorcum & Comp. N. V., doctoral thesis.
- Willard, F. H., and G. F. Martin (1983) The auditory brainstem nuclei and some of their projections to the inferior colliculus in the noth american opossum. Neuroscience 10: 1203–1232.
- Whitley, J. M., and C. K. Henkel (1984) Topographical organization of the inferior collicular projection and other connections of the ventral nucleus of the lateral lemniscus in the cat. J. Comp. Neurol. 229: 257–270.
- Wiberg, M. (1986) Somatosensory projection to the mesencephalon. An anatomical study in the cat and monkey. Doctoral dissertation. University of Uppsala.
- Zook, J. M., J. A., Winer, G. D. Pollak, and R. D. Bodenhamer (1985) Topology of the central nucleus of the mustache bat's inferior colliculus: correlation of single unit properties and neuronal architecture. J. Comp. Neurol. 231: 530–546.