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Time of origin of neurons of the rat inferior colliculus and the relations between cytogenesis and tonotopic order in the auditory pathway

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Summary

Groups of pregnant rats were injected with two successive daily doses of 3H-thymidine from gestational day 12 and 13 (E12+13) until the day before parturition (E21+22) in order to label in their embryos the proliferating precursors of neurons. At 60 days of age the proportion of neurons generated (or no longer labelled) on specific embryonic days was determined quantitatively in six vertical strips of the inferior colliculus. It was established that the neurons of the inferior colliculus are produced between days E14 and the perinatal period in an orderly sequence: the earliest generated cells are situated rostrally, laterally and ventrally in the principal nucleus, the latest generated cells are situated caudally, medially and dorsally in the pericentral nucleus. This cytogenetic gradient suggested that the cells are produced dorsally in the caudal recess of the embryonic aqueduct and are deployed in an “outsidein” pattern.

This study has brought to a conclusion our datings of neuron production in the central auditory pathway of the rat. The results revealed that in those structures in which a cytogenetic gradient could be recognized, the orientation of this gradient and the regional tonotopic order (demonstrated mostly in species other than the rat) tended to be aligned. Moreover, with the exception of the medial trapezoid nucleus and the dorsal nucleus of the lateral lemniscus (which receive contralateral input from the cochlear nuclei), sites with early-produced neurons correlated with units responding preferentially to high frequency tones and vice versa. This suggested that the orderly production of neurons within different components of the auditory system is a factor in their subsequent topographic organization. A comparison of the temporal order of neuron production in different components of the auditory pathway suggested that the establishment of orderly topographic relations between some of the structures (e.g., the medial geniculate body and the primary auditory cortex) takes place before this spatial relationship could be specified as a cochleotopic order.

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Abbreviations

ab:

cochlear nerve, ascending branch

Ai:

aqueduct, inferior collicular recess

AI:

primary auditory cortex

bi:

brachium of inferior colliculus

c:

caudal

CE:

cerebellum

CI:

central nucleus, inferior colliculus

CNa:

anteroventral cochlear nucleus

CNd:

dorsal cochlear nucleus

CNp:

posteroventral cochlear nucleus

d:

dorsal

db:

cochlear nerve, descending branch

DI:

diencephalon

ds:

dorsal acoustic stria (stria of Monakow)

DM:

dorsomedial nucleus, inferior colliculus

EX:

external nucleus, inferior colliculus

IC:

inferior colliculus

is:

intermediate acoustic stria (stria of Held)

l:

lateral

LD:

dorsal nucleus of lateral lemniscus

ll:

lateral lemniscus

LV:

ventral nucleus of lateral lemniscus

m:

medial

ME:

medulla

MG:

medial geniculate body

MS:

mesencephalon

PC:

pericentral nucleus, inferior colliculus

PR:

principal nucleus, inferior colliculus

py:

pyramidal cells, dorsal cochlear nucleus

r:

rostral

SOl:

lateral superior olivary nucleus

SOm:

medial superior olivary nucleus

TRl:

lateral trapezoid nucleus

TRm:

medial trapezoid nucleus

v:

ventral

VL:

lateral ventricle

vs:

ventral acoustic stria (trapezoid body)

V3:

third ventricle

VIIIn:

cochlear nerve

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Authors and Affiliations

  1. Laboratory of Developmental Neurobiology, Department of Biological Sciences, Purdue University, 47907, West Lafayette, IN, USA

    J. Altman & S. A. Bayer

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  1. J. Altman
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  2. S. A. Bayer
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Altman, J., Bayer, S.A. Time of origin of neurons of the rat inferior colliculus and the relations between cytogenesis and tonotopic order in the auditory pathway. Exp Brain Res 42, 411–423 (1981). https://doi.org/10.1007/BF00237506

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