Secondary connections of the dorsal and ventral facial lobes in a teleost fish, the rockling (Ciliata mustela)

Abstract

In the rockling, Ciliata mustela (Teleostei), a portion of the dorsal fin is a specialized chemosensory organ possessing solitary chemoreceptor cells innervated by a recurrent branch of the facial nerve. Previous studies have demonstrated that the specialized solitary chemoreceptor cell system is represented in the dorsal segment of the medullary facial lobe (DFL), whereas the taste buds in the remainder of the facial-nerve-innervated skin are represented in the ventral division of the lobe (VFL). The carbocyanine dye DiI was used to investigate the secondary and higher order brain connections of these two distinct subdivisions of the facial lobe. Both segments of the facial lobe sent fibers into the contralateral DFL via a dorsocaudal facial commissure and to the contralateral vagal lobes and VFL via fibers arching ventrally through the reticular formation. Ascending fibers from both facial lobe segments were traced into the secondary gustatory nucleus and into the lateral superficial facial nucleus, a small area in the dorsolateral brainstem laterally adjacent to the nucleus medialis of the octavolateral complex. Additionally, the VFL had reciprocal connections with a newly described nucleus adjacent to the incoming facial nerve root. Both DFL and VFL had descending fibers reaching two portions of the funicular nuclear complex, although the VFL contribution to this area is far more extensive than the DFL input. Thus, substantial overlap exists in the connections of the two facial subsystems; i.e., the solitary chemoreceptor information is not processed in nuclei distinct from those making up the usual gustatory lemniscus.

The Physiology of Taste in Fish: Potential Implications for Feeding Stimulation and Gut Chemical Sensing

“…Morphologically speaking, the gustatory system has been extensively studied (reviewed in Hara, 1994;Kasumyan and Døving, 2003;Hansen and Reutter, 2004) and will only be briefly mentioned here. Many classical studies have described the morphology and distribution of fish taste buds (e.g., Crisp et al, 1975;Grover-Johnson and Farbman, 1976;Ezeasor, 1982;Marui et al, 1983;_ Zuwata and Jakubowski, 1993;Fishelson et al, 2004), their innervation and central organization of the gustatory system (e.g., Kotrschal and Finger, 1996;Lamb and Finger, 1996;Yoshimoto et al, 1998;Folgueira et al, 2003), and found these to be quite similar to mammals. Fish are characterized by having more taste buds than any other animal, which can have both an external (extraoral) and internal (oral) location.…”

“…Three cranial nerves are responsible for relaying gustatory information directly to the central nervous system: (1) the facial (VII) nerve, projecting into taste buds on the extraoral surface (lips, barbels, fins, and body surface) and mandibular arch, including oral taste buds of rostral palate; (2) glossopharyngeal (IX) nerve innervating the pharyngeal arches and posterior part of the oral cavity; and (3) vagus (X) nerve that projects into the branchial arches and pharynx (Hara, 1994;Kasumyan and Døving, 2003;Yasuoka and Abe, 2009). These nerves relay information to the primary gustatory centers in the medulla-facial, glossopharyngeal, and vagal lobes, respectively-and from here efferent fibers connect to the secondary gustatory nucleus, which finally project to several nuclei (or tertiary gustatory centers) in the inferior lobe of the diencephalon (Kotrschal and Finger, 1996;Lamb and Finger, 1996;Yoshimoto et al, 1998;Folgueira et al, 2003).…”

More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant‐nose Fish Gnathonemus petersii

“…Therefore, although somatosensory, taste, or chemoreceptive information from the forehead may be integrated with visceral information from the facial or vagal systems in the brain, information from the Schnauzenorgan is rarely included. Connections in the opposite direction, from the facial lobe to the funicular region of the descending trigeminal system, have been described by Kotrschal and Finger (1996) in the rockling (Ciliata mustela), which has several barbels on its head. This completes a loop linking the sensory facial system with the sensory trigeminal system.…”

Ascending gustatory pathways to the telencephalon in goldfish

“…Gustatory information detected by the taste buds is relayed via the facial, glossopharyngeal, and vagal nerves to the medullary primary gustatory centers: facial, glossopharyngeal, and vagal lobes, respectively (carp and catfishes: Herrick, 1905;carp: Luiten, 1975;Kiyohara et al, 1985; goldfish: Morita and Finger 1985a;Puzdrowski, 1987;bullhead catfishes: Finger, 1976;rockling: Kotrschal and Whitear, 1988;goatfish: Kirino et al, 2006). These primary gustatory centers send fibers mainly to the secondary gustatory nucleus (SGN) (carp and catfishes: Herrick, 1905; crucian carp: Morita et al, 1980Morita et al, , 1983bullhead catfishes: Finger, 1978a; ictarulid catfishes: Kanwal et al, 1988; brown bullhead catfish: Morita and Finger, 1985b; rockling: Kotrschal and Finger, 1996;Nile tilapia: Yoshimoto et al, 1998).…”