Vocal-acoustic pathways in a teleost fish

Abstract

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.

Sodium channel genes and the evolution of diversity in communication signals of electric fishes: Convergent molecular evolution

“…Multiple lineages of teleost fish have independently evolved sonic communication systems by using a diversity of mechanisms, including the vibration of the swimbladder by specialized muscles at frequencies of hundreds of hertz (39)(40)(41)(42). It would be intriguing to determine whether a comparable convergent compartmentalization and specialization of Na ϩ channels genes occurs in muscles specialized for acoustic communication to allow for rapid or prolonged firing of muscle fibers needed to generate acoustic signals.…”

Temporal Coding of Concurrent Acoustic Signals in Auditory Midbrain

“…VS measures from 0 to 1 the accuracy of phase locking to a periodic signal (Goldberg and Brown, 1969). In addition, vector strength of synchronization to the beat frequency, VS dF , was measured by construct- Bass et al, 1994). B, Line drawing of cross-section at level of midbrain recording site.…”

Vocal Pathways Modulate Efferent Neurons to the Inner Ear and Lateral Line

“…Anatomical studies have shown a connection between the vocal motor system and an efferent nucleus in the rostral medulla that innervates inner ear end organs and mechanosensory lateral line receptor organs (Bass et al, 1994). Given the encoding of vocal parameters by both the auditory (for review, see Bass and McKibben, 2003) and lateral line systems in midshipman fish, we hypothesized that the efferent system is activated during sound production, leading to changes in the neuronal activity of both inner ear and lateral line primary afferents.…”