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Binocular depth perception mechanisms in tongue-projecting salamanders

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Abstract

Tongue-projecting salamanders (Bolitoglossini) combine extreme speed and high precision in prey capture. They possess all requirements for stereoscopic depth perception: frontally oriented eyes, a substantial amount of direct ipsilateral projection in addition to the contralateral one, and binocularly driven neurons. Extracellular recordings were made from retinal afferents in the tectum as well as from the somata of tectal neurons. RF-sizes of afferents and tectal neurons were determined, and the response properties of tectal neurons were tested under monocular and binocular conditions with stimuli of different size and velocity. While RF-sizes and response properties of binocular neurons during binocular and contralateral stimulation were similar, ipsilaterally stimulated neurons exhibited much smaller RFs, lower spike rates and different size preferences.

Furthermore, the contralateral retinotectal projection from one eye and the ipsilateral from the other are in register. While retinal afferents are distributed linearly over the tectal surface, most tectal neurons are activated by a retinal area corresponding to the frontal visual field; this results in a magnification of this region. The two monocular receptive fields of binocular neurons exhibit zero disparities (horopter) at distances that coincide with the maximum reach of the tongue. We hypothesize that bolitoglossine salamanders (as well as amphibians in general) make use of two kinds of disparities: (1) between the maps in the left and right tectal hemisphere, coding for the lateral eccentricity of an object, and (2) between the ipsilateral and contralateral retinotectal map, coding for the distance. The presence of substantial direct ipsilateral afferents in bolitoglossine salamanders appears to be the basis for a fast computation of object distance, which is characteristic of these animals.

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Abbreviations

Ax/Ay :

coordinates of a recorded afference

Nx/Ny :

coordinates of a recorded neuron

RF :

receptive field

RFc :

contralateral receptive field

RFi :

ipsilateral receptive field

RFx/RFy :

coordinates of a receptive field center

RGC :

retinal ganglion cell

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Wiggers, W., Roth, G., Eurich, C. et al. Binocular depth perception mechanisms in tongue-projecting salamanders. J Comp Physiol A 176, 365–377 (1995). https://doi.org/10.1007/BF00219062

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Key words

  • Salamander
  • Depth perception
  • Stereopsis Optic tectum
  • Visual maps