Holding visual attention for 400 million years: A model of tectum and torus longitudinalis in teleost fishes

Abstract

Only ray-finned fishes possess a torus longitudinalis (TL), a paired, elongated body attached to the medial margins of the optic tectum. Its granule cells project large numbers of fine fibers running laterally over adjacent tectum, synapsing excitatorily on the spiny dendrites of pyramidal cells. Sustained TL activity is evoked visuotopically by dark stimuli; TL bursting is a corollary discharge of saccadic eye movements. To suggest a function for this ancient structure, neural network models were constructed to show that: (1) pyramidal cells could form an attentional locus, selecting one out of several moving objects to track, but rapid image shifts caused by saccades disrupt tracking; (2) TL could supply both the pre-saccade position of a locus, and the shift predicted from a saccade so as to prime pyramidal dendrites at the target location, ensuring the locus stays with the attended object; (3) that the specific pattern of synaptic connections required for such predictive priming could be learned by an unsupervised rule; (4) temporal and spatial filtering of visual pattern input to TL allows learning from a complex scene. The principles thus evinced could apply to trans-saccadic attention and visual stability in other species.

Neuron types in the zebrafish optic tectum labeled by an id2b transgene

“…It is interesting to note that two of these neuron types are components of a reciprocal circuit between optic tectum and TL. The apical dendrite of PyrNs targets the SM sublayer of the tectum, which receives marginal fiber input from TL (Northmore, ), whereas the dendrite targeting deep SFGS most likely receives direct RGC input. Their connectivity suggests a role for PyrNs in synthesizing visual information transmitted by RGC axons and TL‐derived information.…”

“…However, the brains of teleost fish contain several other accessory visual areas, including first-order, directly retinorecipient subregions of thalamus, hypothalamus, and pretectum (Fraley & Sharma, 1984;Kramer, Wu, Baier, & Kubo, 2019;Robles et al, 2014;Springer & Mednick, 1985), as well as secondorder visual areas that do not receive direct retinal input, such as torus longitudinalis (TL; Northmore, 1984), nucleus isthmi (NI; Henriques, Rahman, Jackson, & Bianco, 2019;Northmore, 1991), and nucleus of the dorsolateral tegmentum (DLT; Grover & Sharma, 1981). Notably, all three of these areas are reciprocally connected with tectum, forming feedback projections that may modulate visual responses in tectum based on factors such as eye position or attentional state (King & Schmidt, 1991;Northmore, 2017). The TL is a neural structure unique to actinopterygians (ray-finned fishes) and is situated adjacent to the dorsal midline of the teleost tectum (Northmore, 2017).…”

“…The SM contains presynaptic TL marginal fibers and TL-recipient apical dendrites of pyramidal neurons (PyrNs; Vanegas, Laufer, & Amat, 1974;Ito & Kishida, 1978;Folgueira et al, 2007), which are analogous to the Type I neurons described in goldfish (Meek & Schellart, 1978). Sophisticated models of TL-tectum circuit function have been proposed (Meek, 1992;Northmore, 2017); direct tests of these models in zebrafish larvae will require the ability to monitor specific circuit elements during presentation of visual stimuli.…”

Anatomy and Connectivity of the Torus Longitudinalis of the Adult Zebrafish

“…Other cerebellumlike systems include the medial and dorsal octavolateralis nucleus (present in some aquatic vertebrates), the electrosensory lobe (present in some bony fish), the rostrolateral nucleus (present in a few bony fish), and the dorsal cochlear nucleus (present in most mammals) (see Bell, 2002 andBell et al, 2008 for reviews on cerebellum-like structures). Why and how such systems appeared during evolution are still open questions (Bell, 2002;Bell et al, 2008;Northmore, 2017).…”

Melatonin receptor expression in vocal, auditory, and neuroendocrine centers of a highly vocal fish, the plainfin midshipman (Porichthys notatus)

“…The torus longitudinalis has strong connections with the tectum, pretectum, preglomerular complex, nucleus lateralis valvulae, and cerebellum in teleosts (Folgueira et al, ), all of which show mel1b label in midshipman and in sea bass with the exception of nucleus lateralis valvulae. Together, these findings suggest a broader role for melatonin in both the processing of visual information received directly from the retina as well as in the modulation of visuomotor‐related behaviors (Northmore, ).…”