Vocal Motor and Auditory Systems of the Plainfin Midshipman

Vocal Motor System

The type I male's vocal system is composed of various nuclei in the central nervous system, which ultimately innervate the sonic muscles on the swim bladder. The pathway begins at the preoptic area and projects to the hypothalamic ventral and anterior tuberal nuclei. Both of these forebrain nuclei innervate cell bodies in the periaqueductal gray (Goodson and Bass, 2002). Then via the medial longitudinal fasciculus, the cell bodies in the periaqueductal gray project to the vocal prepacemaker nucleus, which innervates the vocal pacemaker nucleus (Chagnaud et al., 2011). The vocal prepacemaker and pacemaker nuclei determine the call duration and fundamental frequency of a hum (Chagnaud et al., 2011). The vocal pacemaker nucleus finally synapses on the vocal motor nucleus that translates the premotor code into synchronous vocal motor output and modulates amplitude (Chagnaud et al., 2011). The vocal prepacemaker nucleus

Side view of the brain showing sites of steroid hormone receptor and aromatase (estrogen synthase) in the vocal motor system. Solid dots represent somata, and lines represent axonal projection pathways. Two connected dots indicate reciprocal connections. Preoptic (POA) and hypothalamic ventral (vT) and anterior (AT) tuberal nuclei project to the midbrain periaqueductal gray (PAG) which innervates the vocal pattern generator circuit (VPG) in the hindbrain-spinal cord. The VPG consists of vocal prepacemaker (VPP), pacemaker (VPN) and motor (VMN) nuclei. VMN axons exit the brain via occipital nerve roots to sound-producing vocal muscle attached to the swim bladder. Modified from Forlano et al. (2010).

also projects to the octavolateralis efferent nucleus to provide a copy of the call to the auditory system (Chagnaud et al., 2011).

Fluctuations in the steroid hormones during breeding season can influence these circuits via the presence of aromatase, an enzyme that converts testosterone into estradiol, and numerous androgen and estrogen receptors. Aromatase cell bodies are found along the ventricular surface throughout the midshipman fish brain (Forlano et al, 2001). These cells extend projections to neurons in the preoptic nuclei, anterior tuberal and ventral tuberal hypothalamus, periaqueductal gray, vocal prepacemaker nucleus, and vocal motor nucleus (Forlano et al., 2001). In terms of receptors, the vocal motor nuclei were found to express ERα, ERβ1, and ERβ2 (Forlano et al., 2005; Fergus and Bass, 2013). Furthermore, ARβ was found to be expressed in almost all parts of the vocal motor pathway, including the vocal muscle (Forlano et al., 2010).

Auditory System

Photo of exposed midshipman brain and inner ear. Photo by Bass Lab..

The midshipman’s primary auditory end organ is the saccule, which contains a bed of sensory hair cells (Cohen & Winn, 1967). On top of these hair cells lays a dense otolith (Sisneros 2009). When particle motion produced by sound hits the fish, the otolith lags behind the rest of the fish’s body causing a sheering action on the sensory hair cells (Cohen & Winn, 1967). The saccule then sends this information to nuclei in the hindbrain such as the descending octaval nucleus and secondary octaval populations via the eight-cranial nerve (Bass et al., 2000). Both of these nuclei project to the torus semicircularis, which is homologous to the inferior colliculus (Bass et al., 2005). The torus semicircularis innervates several diencephalic nuclei such as the anterior tuberal hypothalamus and thalamic central posterior nucleus, which relay information to the pallial and subpallial nuclei (Bass et al.,

2000). Finally, auditory information reaches the dorsomedial telencephalon (Bass et al., 2000). These nuclei in the auditory system are extensively interconnected to vocal nuclei throughout the forebrain, midbrain, and hindbrain (Bass et al., 2000; Goodson and Bass, 2002). Furthermore, the hindbrain octavolateralis efferent project to the saccule to modulate its output (Weeg et al., 2005).

Like the vocal motor system, the auditory system contains multiple sites for steroid action. The torus semicircuilaris was found to express both ARβ and ERβ2 (Forlano et al., 2005; Forlano et al., 2010). The saccule also expresses ARβ in addition to ERα, ERβ1, and ERβ2 (Forlano et al., 2001; Forlano et al., 2005). Anatomically, ERα and ARβ are expressed adjacent to hair cells, while ERβ1 is expressed at the apical end of hair cells and ERβ2 is expressed variably in the cytoplasm (Fergus & Bass, 2013).

Side view of the brain showing sites of steroid hormone receptor and aromatase (estrogen synthase) in the auditory system. Solid dots represent somata, and lines represent axonal projection pathways. Two connected dots indicate reciprocal connections. Sounds are detected by auditory saccule which projects via the VIIIth nerve to auditory nuclei in the hindbrain that innervate the auditory midbrain torus semicircularis (TS). A dorsal thalamic nucleus (central posterior nucleus, CP) contains reciprocal connections to the telencephalon (dorsomedial/Dm) and ventral supracommissural (Vs) that receives input from anterior hypothalamus-posterior tubercle. TS and CP also connect to forebrain (anterior hypothalamus, POA) and midbrain (PAG, isthmal/tegmentum) vocal sites, while auditory-recipient hindbrain nuclei connect to the pattern generating VPG circuit. Modified from Forlano & Bass (2011).

References

Bass, A. H., Bodnar, D. A., & Marchaterre, M. A. (2000). Midbrain acoustic circuitry in a vocalizing fish. Journal of Comparative Neurology, 419(4), 505-531.

Bass, A. H., Rose, G. J., & Pritz, M. B. (2005). Auditory midbrain of fish, amphibians, and reptiles: model systems for understanding auditory function. In The inferior colliculus (pp. 459-492). Springer, New York, NY.

Chagnaud, B. P., Baker, R., & Bass, A. H. (2011). Vocalization frequency and duration are coded in separate hindbrain nuclei. Nature communications, 2, 346.

Cohen, M. J., & Winn, H. E. (1967). Electrophysiological observations on hearing and sound production in the fish, Porichthys notatus. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 165(3), 355-369.

Fergus, D. J., & Bass, A. H. (2013). Localization and divergent profiles of estrogen receptors and aromatase in the vocal and auditory networks of a fish with alternative mating tactics. Journal of Comparative Neurology, 521(12), 2850-2869.

Forlano, P. M., Deitcher, D. L., & Bass, A. H. (2005). Distribution of estrogen receptor alpha mRNA in the brain and inner ear of a vocal fish with comparisons to sites of aromatase expression. Journal of Comparative Neurology, 483(1), 91-113.

Forlano, P. M., Deitcher, D. L., Myers, D. A., & Bass, A. H. (2001). Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. Journal of Neuroscience, 21(22), 8943-8955.

Forlano, P. M., Marchaterre, M., Deitcher, D. L., & Bass, A. H. (2010). Distribution of androgen receptor mRNA expression in vocal, auditory, and neuroendocrine circuits in a teleost fish. Journal of Comparative Neurology, 518(4), 493-512.

Goodson, J.L., Bass, A.H., (2002). Vocal-acoustic circuitry and descending vocal pathways in teleost fish: convergence with terrestrial vertebrates

reveals conserved traits. Journal of Comparative Neurology, 448, 298–322.

Weeg, M. S., B. R. Land and A. H. Bass (2005) Temporal modulation of efferents to the inner ear and lateral line by central vocal pathways. The

Journal of Neuroscience 25, 5967-5974. doi:10.1523/JNEUROSCI.0019-05.2005