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Front. Neuroanat. | doi: 10.3389/fnana.2018.00079

The mormyrid optic tectum is a topographic interface for active electrolocation and visual sensing

  • 1Universität Bonn, Germany
  • 2Department of Neuroscience, Ludwig-Maximilians-Universität München, Germany

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 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 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.

Keywords: mormyrid, Electrosensation, Gnathonemus petersii, optic tectum, torus semicircularis, Vision

Received: 12 Jul 2018; Accepted: 13 Sep 2018.

Edited by:

Luis Puelles, Universidad de Murcia, Spain

Reviewed by:

Manuel A. Pombal, University of Vigo, Spain
Ramon Anadon, Universidade de Santiago de Compostela, Spain  

Copyright: © 2018 Zeymer, von der Emde and Wullimann. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Mario F. Wullimann, Ludwig-Maximilians-Universität München, Department of Neuroscience, Munich, D-82152, Germany, wullimann@biologie.uni-muenchen.de