The Mormyrid Optic Tectum Is a Topographic Interface for Active Electrolocation and Visual Sensing

Abstract

The African weakly electric fish Gnathonemus petersii is capable of cross-modal object recognition using its electric sense or vision. Thus, object features stored in the brain are accessible by multiple senses, either through connections between unisensory brain regions or because of multimodal representations in multisensory areas. Primary electrosensory information is processed in the medullary electrosensory lateral line lobe, which projects topographically to the lateral nucleus of the torus semicircularis (NL). Visual information reaches the optic tectum (TeO), which projects to various other brain regions. We investigated the neuroanatomical connections of these two major midbrain visual and electrosensory brain areas, focusing on the topographical relationship of interconnections between the two structures. Thus, the neural tracer DiI was injected systematically into different tectal quadrants, as well as into the NL. Tectal tracer injections revealed topographically organized retrograde and anterograde label in the NL. Rostral and caudal tectal regions were interconnected with rostral and caudal areas of the NL, respectively. However, dorsal and ventral tectal regions were represented in a roughly inverted fashion in NL, as dorsal tectal injections labeled ventral areas in NL and vice versa. In addition, tracer injections into TeO or NL revealed extensive inputs to both structures from ipsilateral (NL also contralateral) efferent basal cells in the valvula cerebelli; the NL furthermore projected back to the valvula. Additional tectal and NL connections were largely confirmatory to earlier studies. For example, the TeO received ipsilateral inputs from the central zone of the dorsal telencephalon, torus longitudinalis, nucleus isthmi, various tegmental, thalamic and pretectal nuclei, as well as other nuclei of the torus semicircularis. Also, the TeO projected to the dorsal preglomerular and dorsal posterior thalamic nuclei as well as to nuclei in the torus semicircularis and nucleus isthmi. Beyond the clear topographical relationship of NL and TeO interconnections established here, the known neurosensory upstream circuitry was used to suggest a model of how a defined spot in the peripheral sensory world comes to be represented in a common associated neural locus both in the NL and the TeO, thereby providing the neural substrate for cross-modal object recognition.

Anatomy and Connectivity of the Torus Longitudinalis of the Adult Zebrafish

“…Golgi studies reported axonal projections from TL granule cells to the most superficial layer of the tectum, the marginal layer or stratum marginale (Sala, 1895;Sajovic and Levinthal, 1982). This TL efferent connection was then traced experimentally to the optic tectum in the holostean longnose gar (Lepisosteus osseus; Northcutt and Butler, 1980) and several teleosts (Grover and Sharma, 1981;Luiten, 1981;Northcutt, 1982;Wullimann and Northcutt, 1990;Ito et al, 2003;Xue et al, 2003;Folgueira et al, 2007;Zeymer et al, 2018). Granule cell axons run in the marginal layer parallel to the surface of the tectum, in a manner that is similar to cerebellar parallel fibers, and synapse onto the spiny, branched dendrites of pyramidal or type I cells Vanegas et al, 1974).…”

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

“…In the present study, we have demonstrated that the V motor system receives visual information from the optic tectum and via the two pretectal nuclei, as mentioned above. Recent experiments done by Zeymer et al () have revealed new anatomical evidence for an ascending afferent projection from the trigeminal sensory column to the optic tectum and to the lateral nucleus of the torus semicircularis. This suggests that the optic tectum is also an interface for the integration of visual, electrosensory and somatosensory information, providing afferent input to the V motor nucleus.…”

“…However, some considerable variation is present in the labeling used in studies by different authors. The most recent study has been published by Zeymer, von der Emde, and Wullimann () using an updated nomenclature established by Wullimann, where possible concordances are identified.…”

Neural connections of the torus semicircularis in the adult Zebrafish

“…Thus, the zebrafish OT appears involved as a higher center of the lateral line circuitry, but hardly of the auditory one. Torotectal projections were reported in goldfish (Grober and Sharma, 1981), and in mormyrids, the OT is also topographically related to the mediodorsal and lateral regions of the TS (Haugedé‐Carré, 1983; Zeymer et al., 2018). The midbrain tegmentum does not show toral (TSc) afferent neurons in zebrafish, unlike that reported in carp (Echteler, 1984, 1985).…”