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

Abstract

The weakly electric fish Gnathonemus petersii uses its electric sense to actively probe the environment. Its highly mobile chin appendage, the Schnauzenorgan, is rich in electroreceptors. Physical measurements have demonstrated the importance of the position of the Schnauzenorgan in funneling the fish's self-generated electric field. The present study focuses on the trigeminal motor pathway that controls Schnauzenorgan movement and on its trigeminal sensory innervation and central representation. The nerves entering the Schnauzenorgan are very large and contain both motor and sensory trigeminal components as well as an electrosensory pathway. With the use of neurotracer techniques, labeled Schnauzenorgan motoneurons were found throughout the ventral main body of the trigeminal motor nucleus but not among the population of larger motoneurons in its rostrodorsal region. The Schnauzenorgan receives no motor or sensory innervation from the facial nerve. There are many anastomoses between the peripheral electrosensory and trigeminal nerves, but these senses remain separate in the sensory ganglia and in their first central relays. Schnauzenorgan trigeminal primary afferent projections extend throughout the descending trigeminal sensory nuclei, and a few fibers enter the facial lobe. Although no labeled neurons could be identified in the brain as the trigeminal mesencephalic root, some Schnauzenorgan trigeminal afferents terminated in the trigeminal motor nucleus, suggesting a monosynaptic, possibly proprioceptive, pathway. In this first step toward understanding multimodal central representation of the Schnauzenorgan, no direct interconnections were found between the trigeminal sensory and electromotor command system, or the electrosensory and trigeminal motor command. The pathways linking perception to action remain to be studied.

Central connections of the trigeminal motor command system in the weakly electric Elephantnose fish (Gnathonemus petersii)

“…We assume that cell bodies of proprioceptive afferents are located somewhere in the trigeminal ganglion outside the brain. This supports the results from experiments in which we traced the trigeminal nerve from the periphery and no labeled cells were found in the area described by Meek et al () as the mesV nucleus (Amey‐Özel et al, ).…”

“…In most vertebrates, mono‐ and disynaptic reflex connections are described linking the sensory and motor trigeminal systems in connection with food swallowing and associated movements of the jaw triggered by proprioceptive and somatosensory feedback (Abrahams, Anstee, Richmond, & Rose, : cat; Dessem & Luo, : rat; Luiten, ; Luiten & van der Pers, : carp; Nishino, : human). Our results have shown both direct monosynaptic, primary afferent feedback connections from the Schnauzenorgan trigeminal nerve to the V motor nucleus (Amey‐Özel et al, ) and extensive disynaptic connections from the pars oralis region of the sensory trigeminal nucleus to the V motor nucleus, as well as weaker connections with other parts of the descending trigeminal sensory nuclei.…”

“…Figure shows summary drawings of all brain centers that are afferent to the V motor nucleus (Figure a) and also those where labeled terminal fields indicate that they receive central projections from the V motor nucleus (Figure b). While the motor nucleus is defined principally by the motoneurons and their dendritic extensions (Amey‐Özel et al, ), the present study has shown that the V motor nucleus also contains a number of smaller neurons that were not labeled from the peripheral nerve.…”

“…A population of labeled neurons morphologically different to motoneurons was identified around the medial periphery and within the motor nucleus itself, especially at the mediodorsal transition from the ventral main body of the V motor nucleus to the dorsal subdivision (Figure a,c, black and white arrowheads). These cells were smaller than the motoneurons and were not seen after tracing from the peripheral nerve (Amey‐Özel et al, ). We were not able to distinguish different populations amongst these small neurons, which were sparsely distributed and whose axons were thin.…”

“…The highly mobile chin appendage—the Schnauzenorgan—of the weakly electric fish Gnathonemus petersii (Günther, 1892) has given this species its popular name: “Elephantnose fish.” The Schnauzenorgan is in fact a multisensory organ used to scan features of the environment or, probing like a finger, to explore nearby objects and to search for food on the river bed (Amey‐Özel, von der Emde, Engelmann, & Grant, ; Bacelo, Engelmann, Hollmann, von der Emde, & Grant, ; Pusch et al, ; von der Emde et al, ; von der Emde & Bleckmann, ). The Schnauzenorgan is densely covered with electroreceptors, including both mormyomasts and ampullary receptors (Bell, Zakon, & Finger, ; Bennett, ; Harder, ; Szabo, ) and has been described as an electrosensory fovea (Amey‐Özel, Hollmann, & von der Emde, ; Bacelo et al, ; Hollmann, Engelmann, & von der Emde, ; Pusch et al, ; von der Emde & Schwarz, ).…”