The mapping of auditory circuitry and its interface with vocal motor systems is essential to the investigation of the neural processing of acoustic signals and its relationship to sound production. Here we delineate the circuitry of a midbrain auditory center in a vocal fish, the plainfin midshipman. Biotin injections into physiologically identified auditory sites in nucleus centralis (NC) in the torus semicircularis show a medial column of retrogradely filled neurons in the medulla mainly in a dorsomedial division of a descending octaval nucleus (DO), dorsal and ventral divisions of a secondary octaval nucleus (SO), and the reticular formation (RF) near the lateral lemniscus. Biotin‐filled neurons are also located at midbrain‐pretectal levels in a medial pretoral nucleus. Terminal fields are identified in the medulla (ventral SO, RF), isthmus (nucleus praeeminentialis), midbrain (nucleus of the lateral lemniscus, medial pretoral nucleus, contralateral NC, tectum), diencephalon (lateral preglomerular, central posterior, and anterior tuber nuclei), and telencephalon (area ventralis). The medial column of toral afferent neurons is adjacent to and overlapping the positions of DO and SO neurons shown previously to be linked to the vocal pacemaker circuitry of the medulla. Midshipman are considered “hearing generalists” because they lack the peripheral adaptations of “specialists” that enhance the detection of the pressure component of acoustic signals. Whereas the results indicate a general pattern of acoustic circuitry similar to that of specialists, they also show central adaptations, namely, a vocal–acoustic interface in DO and SO related to this species' vocal abilities. J. Comp. Neurol. 419:505–531, 2000. © 2000 Wiley‐Liss, Inc.
Across all major vertebrate groups, androgen receptors (ARs) have been identified in neural circuits that shape reproductive-related behaviors, including vocalization. The vocal control network of teleost fishes presents an archetypal example of how a vertebrate nervous system produces social, context-dependent sounds. We cloned a partial cDNA of AR that was used to generate specific probes to localize AR expression throughout the central nervous system of the vocal plainfin midshipman fish (Porichthys notatus). In the forebrain, AR mRNA is abundant in proposed homologs of the mammalian striatum and amygdala, and in anterior and posterior parvocellular and magnocellular nuclei of the preoptic area, nucleus preglomerulosus, and posterior, ventral and anterior tuberal nuclei of the hypothalamus. Many of these nuclei are part of the known vocal and auditory circuitry in midshipman. The midbrain periaqueductal gray, an essential link between forebrain and hindbrain vocal circuitry, and the lateral line recipient nucleus medialis in the rostral hindbrain also express abundant AR mRNA. In the caudal hindbrain-spinal vocal circuit, high AR mRNA is found in the vocal prepacemaker nucleus and along the dorsal periphery of the vocal motor nucleus congruent with the known pattern of expression of aromatase-containing glial cells. Additionally, abundant AR mRNA expression is shown for the first time in the inner ear of a vertebrate. The distribution of AR mRNA strongly supports the role of androgens as modulators of behaviorally defined vocal, auditory, and neuroendocrine circuits in teleost fish and vertebrates in general. Keywordsvocal control system; hearing; inner ear; hypothalamus; estrogen receptor; aromatase Androgen receptors (ARs) and androgen-concentrating cells have been consistently identified in neural circuits that shape reproductive-related behaviors, including sexually dimorphic nuclei that control vocalization, across most vertebrate taxa: amphibians (Kelley, 1986;Perez et al., 1996), reptiles (Tang et al., 2001), and birds (Gahr, 2001;Ball et al., 2002;Schlinger and Brenowitz, 2002;Kim et al., 2004) (for review, see Bass, 2008). While androgenconcentrating neurons have long been known in the central nervous system (CNS) of fish as well (e.g., Morrell et al., 1975;Fine et al., 1996), recent studies have shown that androgens can strongly modulate the vocal pattern generating circuitry in teleost fish (Remage-Healey and Bass, 2004, 2006a, although the loci for possible direct androgen actions on the vocal system remain unknown. The current study delineates the position of ARs in the plainfin midshipman fish, Porichthys notatus, that has become a well-established model system for NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript studying the neural and hormonal mechanisms of vocal-acoustic communication among vertebrates (Bass and McKibben, 2003).The plainfin midshipman has two male morphs that exhibit alternative reproductive tactics including divergent vocal behaviors (Brantl...
One mechanism used by teleost fishes to produce acoustic communication signals involves the contraction of sonic "drum" muscles that appose the lateral walls of the swimbladder. In one marine species, the midshipman (Porichthys notatus), there is a sex difference in the overall size of the swimbladder as well as in the ultrastructural properties of its myofibrils. Additionally, there are two classes of sexually mature males referred to as Type I and Type II. The peripheral sonic motor system of Type I males differs from that of Type II males and females (which resemble each other) in a number of ways: (1) the mass of their swimbladder and associated sonic muscles is 50% greater, (2) their muscle fibers are several times larger and have a characteristically large volume of sarcoplasm that surrounds the myofibrils and is densely filled with mitochondria, (3) the length of z-lines of their myofibrils is about 20-fold greater, and (4) their sarcoplasmic reticulum is more highly branched. The ultrastructure of the myofibrils of Type II males and females resembles that found in the sonic muscle of males and females in other related species. The larger mass and specializations of the sonic muscle in Type I males are considered to be adaptations related to their known role in sound production and the unique long duration "humming" sounds that they generate during the breeding season. The similarity in the sonic motor system between females and Type II males is considered to be related to the utilization of an "alternative mating strategy" by Type II males. To our knowledge, this is the first documentation of a sex difference or, for that matter, a sexual polymorphism in the ultrastructural features of a vertebrate myofibril.
Toadfishes are among the best-known groups of sound-producing (vocal) fishes and include species commonly known as toadfish and midshipman. Although midshipman have been the subject of extensive investigation of the neural mechanisms of vocalization, this is the first comprehensive, quantitative analysis of the spectrotemporal characters of their acoustic signals and one of the few for fishes in general. Field recordings of territorial, nest-guarding male midshipman during the breeding season identified a diverse vocal repertoire composed of three basic sound types that varied widely in duration, harmonic structure and degree of amplitude modulation (AM): 'hum', 'grunt' and 'growl'. Hum duration varied nearly 1000-fold, lasting for minutes at a time, with stable harmonic stacks and little envelope modulation throughout the sound. By contrast, grunts were brief, ~30-140 ms, broadband signals produced both in isolation and repetitively as a train of up to 200 at intervals of ~0.5-1.0 s. Growls were also produced alone or repetitively, but at variable intervals of the order of seconds with durations between those of grunts and hums, ranging 60-fold from ~200 ms to 12 s. Growls exhibited prominent harmonics with sudden shifts in pulse repetition rate and highly variable AM patterns, unlike the nearly constant AM of grunt trains and flat envelope of hums. Behavioral and neurophysiological studies support the hypothesis that each sound type's unique acoustic signature contributes to signal recognition mechanisms. Nocturnal production of these sounds against a background chorus dominated constantly for hours by a single sound type, the multiharmonic hum, reveals a novel underwater soundscape for fish.
The plainfin midshipman fish Porichthys notatus has both inter- and intra-sexual dimorphism in the sound-producing (vocal or sonic) muscles attached to the swimbladder wall. The "Type I" and "Type II" male morphs differ in that dramatic structural changes related to sexual maturity occur in the mass, the area of mitochondria-filled sarcoplasm, and the myofiber number of the sonic muscles of Type I males, but not in those of Type II males (nor of females). Androgen implantation for 9 weeks markedly increased the relative sonic muscle size in juvenile males, juvenile females, and Type II males, whereas estradiol or cholesterol treatment did not. The principal androgen effect on myofiber structure was an increase in the area of mitochondria-filled sarcoplasm. The ratio of sarcoplasm area to myofibril area (Sr/Mf) increased by 1.4- to 2-fold in myofibers of all androgen-treated groups, with the greatest structural change occurring in juvenile males. When androgen implants were removed from juvenile males, the muscle mass and Sr/Mf ratio reverted toward the unimplanted juvenile phenotype. Total fiber number in sonic muscle increased significantly in juvenile males following androgen implantation but did not detectably change in juvenile females or Type II males. These results suggest: 1) sonic muscle in Porichthys notatus is an androgen target tissue, 2) fiber structure and fiber number are androgen-sensitive features, and 3) there exist sex- and morph-specific patterns of sonic muscle responsiveness to androgen implants.
The electric organ of mormyrid fishes is composed of action potential-generating cells called electrocytes that together produce a species-typical electric organ discharge (EOD). The electrocytes of mormyrids are disc-shaped cells with distinct anterior and posterior faces, and a series of evaginations of one face that form a stalklike structure that is the site of innervation by spinal electromotoneurons (Bass: J. Comp. Neurol. 244:313-330, '86a). Here, we describe the major ultrastructural features of mormyrid electrocytes, which include surface invaginations along each face, myonuclei, myofilaments, and neuromuscularlike junctions formed by the axons of spinal electromotoneurons. The degree of surface invaginations along the anterior face is the most dramatic interspecific variable and is usually greater for species with the longer duration EODs. Among species with sexually dimorphic EODs, natural males, or females treated with gonadal steroid hormones, have longer-duration EODs and thicker electrocytes with more surface invaginations along the anterior face. The results are discussed in relation to the action potential-generating properties of the electrocyte's membranes.
The sonic motor nucleus of the plainfin midshipman, Porichthys notatus, is a midline nucleus located at the junction of the caudal medulla and rostral spinal cord. Its motoneurons innervate sonic "drumming" muscles that are attached to the lateral walls of the swimbladder. There are two classes of sexually mature males referred to as Type I and Type II. The Type I males are larger and generate sounds during the breeding season. The Type II males are smaller and, like adult females, have not yet been shown to generate sounds. This study examined possible sex differences in the size of sonic motoneurons, and the type and distribution of their afferent terminal boutons. The average soma diameter of motoneurons of Type I males is about 50% larger than that of Type II males and females. There is also a small but significant difference in soma diameter between Type II males and females; they are smaller in the former class. There were no sex differences in the presence or distribution of different classes of axosomatic and axodendritic terminal boutons, which included: (1) active zones with either clear, round, or pleomorphic vesicles, (2) active zones with both clear, round vesicles, and larger dense core vesicles, (3) "mixed synapses" with gap junctions and active zones usually associated with pleomorphic vesicles. The results are discussed within the context of sexual differentiation of vertebrate motor systems and the functional organization of the sonic motor system in fishes. Sex differences in soma diameter correlate with a number of sex differences in the gross and ultrastructural features that distinguish the sonic muscles of Type I males from those of Type II males and females, which are similar to each other. The absence of qualitative sex differences in synaptic morphology suggest that the central neuronal circuitry of the sonic motor system is similar among all three adult morphs.
The organization of the descending and secondary octaval nuclei in the hindbrain of the Gulf toadfish, Opsanus beta, was revealed following the injection of biotin compounds into a physiologically identified auditory region of the torus semicircularis. The results show retrogradely-filled neurons mainly in a dorsomedial division of the descending octaval nucleus, and dorsal and ventral divisions of a secondary octaval nucleus; minor labeling also appeared in dorsolateral and rostromedial intermediate divisions of the descending nucleus. The pattern identified is consistent with that reported in other teleosts, including both vocal and non-vocal species, and clarifies earlier reports of the organization of hindbrain octaval nuclei in toadfish and the closely related midshipman fish.
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