Somatotopic map of the active electrosensory sense in the midbrain of the mormyrid Gnathonemus petersii

Abstract

In many vertebrates parallel processing in topographically ordered maps is essential for efficient sensory processing. In the active electrosensory pathway of mormyrids afferent input is processed in two parallel somatotopically ordered hindbrain maps of the electrosensory lateral line lobe (ELL), the dorsolateral zone (DLZ), and the medial zone (MZ). Here phase and amplitude modulations of the self-generated electric field were processed separately. Behavioral data indicates that this information must be merged for the sensory system to categorically distinguish capacitive and resistive properties of objects. While projections between both zones of the ELL have been found, the available physiological data suggests that this merging takes place in the midbrain torus semicircularis (TS). Previous anatomical data indicate that the detailed somatotopic representation present in the ELL is lost in the nucleus lateralis (NL) of the TS, while a rough rostrocaudal mapping is maintained. In our study we investigated the projections from the hindbrain to the midbrain in more detail, using tracer injections. Our data reveals that afferents from both maps of the ELL terminate in a detailed somatotopic manner within the midbrain NL. Furthermore, we provide data indicating that phase and amplitude information may indeed be processed jointly in the NL. J. Comp. Neurol. 524:2479-2491, 2016. © 2016 Wiley Periodicals, Inc.

Estimation of distance and electric impedance of capacitive objects in the weakly electric fish,Gnathonemus petersii

“…Moreover, these studies provided evidence of a somatotopic midbrain map, from which topographical waveform images could be acquired. The somatotopic organization at the level of the midbrain, however, was found to be much weaker than in the ELL network (Hollmann et al, 2016).…”

“…When compared, the topographic organization of the amplitude map (ELL medial zone) appears much more distinct than that of the proposed waveform map (nucleus lateralis) (Hollmann et al, 2016). Because of this difference, it appears unlikely that a precise topographical and 'hardwired' combination of amplitude and waveform modulations takes place to obtain electric colour information.…”

“…Determination of waveform images, however, requires a combined processing (subtraction) of the modulation patterns of both ELL zones at a higher level (von der Emde and Bell, 1994). Anatomical studies indeed have shown that projections from the two ELL zones converge at the nucleus lateralis in the fish's midbrain (Bell, 1981;Hollmann et al, 2016). Moreover, these studies provided evidence of a somatotopic midbrain map, from which topographical waveform images could be acquired.…”

“…Topographically specific mechanisms of lateral inhibition provided by ELL interneurons (Meek et al, 1999(Meek et al, , 2001) might further improve this task by enhancing electric image contrast (von der Emde and Engelmann, 2011). In comparison, the weak somatotopic organization of the midbrain map in the lateral nucleus (Hollmann et al, 2016), which may provide only coarse waveform images, might not enable a reliable and precise edge detection circuit. Based on our electric image analysis and the anatomical and physiological findings just mentioned, we conclude that distance perception in G. petersii is based on amplitude image information and is mediated only at an early processing stage of the electrosensory pathway.…”

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

“…However, also distinct mormyrid specializations such as the heavy involvement of the valvula (and corpus) cerebelli in this ascending circuitry were revealed ( Finger et al, 1981 ; Meek et al, 1986a , b ). The midbrain optic tectum ( Lázár et al, 1984 ) and lateral nucleus of the torus semicircularis ( Hollmann et al, 2016 ) contain neural representations of the sensory periphery, one visual, the other electrosensory. Thus, these two structures are prime candidates for the neural substrate for cross-modal object recognition.…”