Journal of Neuroscience, Vol 14, 4025-4039, Copyright © 1994 by Society for Neuroscience
Vocal-acoustic pathways in a teleost fish
AH Bass, MA Marchaterre and R Baker
Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853.
Many teleost fish generate acoustic signals for vocal communication by the
synchronized, high-frequency contraction of skeletal, sonic muscles. In
midshipman, eight groups of brainstem neurons were distinguished after
biocytin application to the sonic nerve that, we propose, represent the
entire vocal motor circuit. Biocytin-filled terminals were ubiquitous
within all areas containing labeled neurons and, together with
ultrastructural evidence, suggested a serial, transneuronal transport at
synaptic sites between at least three neuronal groups. The most intensely
labeled neurons were positioned in the caudal brainstem and included a
previously characterized pacemaker- motoneuron circuit and a newly
recognized ventral medullary nucleus that itself gave rise to extensive
commissural and lateral brainstem bundles linking the pacemaker circuitry
to the rostral brainstem. Five additional groups formed a column rostrally
within the medial brainstem adjacent to eighth nerve (octaval)-recipient
nuclei largely presumed to be acoustic. This column extended dorsally up to
the ventricular cell layer and as far anterior as midbrain isthmal levels.
The best-defined group was in the octaval efferent nucleus that directly
innervates the sacculus that is considered the auditory division of the
inner ear. Saccular afferents and neurons throughout the medial column were
also filled after biocytin application to the saccular nerve. This vocal-
acoustic network overlaps low-threshold, electrical stimulation sites in
the rostral brainstem that elicit vocalizations. The medial column must
therefore be the origin of the descending pathway controlling activation of
the vocal pacemaker circuitry and likely forms the basis for acoustically
elicited vocalizations. We suggest this network, together with input from
the pacemaker circuitry, is also the origin of a vocal-related, corollary
discharge to acoustic nuclei. Direct links between vocal and acoustic brain
regions are thus traits common to aquatic and terrestrial vertebrates.
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