Visual and electrosensory circuits of the diencephalon in mormyrids: an evolutionary perspective

Mormyrids are one of two groups of teleost fishes known to have evolved electroreception, and the concomitant neuroanatomical changes have confounded the interpretation of many of their brain areas in a comparative context, e.g., the diencephalon, where different sensory systems are processed and relayed. Recently, cerebellar and retinal connections of the diencephalon in mormyrids were reported. The present study reports on the telencephalic and tectal connections, specifically in Gnathonemus petersii, as these data are critical for an accurate interpretation of diencephalic nuclei in teleosts. Injections of horseradish peroxidase into the telencephalon retrogradely labeled neurons ipsilaterally in various thalamic, preglomerular, and tuberal nuclei, the nucleus of the locus coeruleus (also contralaterally), the superior raphe, and portions of the nucleus lateralis valvulae. Telencephalic injections anterogradely labeled the dorsal preglomerular and the dorsal tegmental nuclei bilaterally. Injections into the optic tectum retrogradely labeled neurons bilaterally in the central zone of area dorsalis telencephali and ipsilaterally in the torus longitudinalis, various thalamic, pretectal, and tegmental nuclei, some nuclei in the torus semicircularis, the nucleus of the locus coeruleus, the nucleus isthmi and the superior reticular formation, basal cells in the ipsilateral valvula cerebelli, and eurydendroid cells in the contralateral lobe C4 of the corpus cerebelli. Weaker contralateral projections were also observed to arise from the ventromedial thalamus and various pretectal and tegmental nuclei, and from the locus coeruleus and superior reticular formation. Tectal injections anterogradely labeled various pretectal nuclei bilaterally, as well as ipsilaterally the dorsal preglomerular and dorsal posterior thalamic nuclei, some nuclei in the torus semicircularis, the dorsal tegmental nucleus, nucleus isthmi, and, again bilaterally, the superior reticular formation. A comparison of retinal, cerebellar, tectal, and telencephalic connections in Gnathonemus with those in nonelectrosensory teleosts reveals several points: (1) the visual area of the diencephalon is highly reduced in Gnathonemus, (2) the interconnections between the preglomerular area and telencephalon in Gnathonemus are unusually well developed compared to those in other teleosts, and (3) two of the three corpopetal diencephalic nuclei are homologues of the central and dorsal periventricular pretectum in other teleosts. The third is a subdivision of the preglomerular area, rather than an accessory optic or pretectal nucleus, and is related to electroreception. The preglomerulo-cerebellar connections in Gnathonemus are therefore interpreted as uniquely derived characters for mormyrids.