Evolution of neural processing for visual perception in vertebrates

Abstract

Visual perception requires both visual information and attention. This review compares, across classes of vertebrates, the functional and anatomical characteristics of (a) the neural pathways that process visual information about objects, and (b) stimulus selection pathways that determine the objects to which an animal attends. Early in the evolution of vertebrate species, visual perception was dominated by information transmitted via the midbrain (retinotectal) visual pathway, and attention was probably controlled primarily by a selection network in the midbrain. In contrast, in primates, visual perception is dominated by information transmitted via the forebrain (retinogeniculate) visual pathway, and attention is mediated largely by networks in the forebrain. In birds and nonprimate mammals, both the retinotectal and retinogeniculate pathways contribute critically to visual information processing, and both midbrain and forebrain networks play important roles in controlling attention. The computations and processing strategies in birds and mammals share some strikingly similar characteristics despite over 300 million years of independent evolution and being implemented by distinct brain architectures. The similarity of these functional characteristics suggests that they provide valuable advantages to visual perception in advanced visual systems. A schema is proposed that describes the evolution of the pathways and computations that enable visual perception in vertebrate species.

Neuronal modulation in the mouse superior colliculus during covert visual selective attention

“…Furthermore, by comparing activity across attentional conditions, we determined that the cue-related modulation was due to enhancement of SC activity at the cued location rather than suppression of SC activity at the uncued location. Stimulus competition is an important aspect of visual selective attention and the SC plays a crucial role in selecting target stimuli amongst competing distractors in many species 17,20,31 , presumably reflecting an evolutionarily conserved midbrain function 32,33 .…”

“…Stimulus competition is an important aspect of visual selective attention and the SC plays a crucial role in selecting target stimuli amongst competing distractors in many species 17,20,31 , presumably reflecting an evolutionarily conserved midbrain function 32,33 . In the primate, SC activity is modulated in a variety of paradigms that involve stimulus selection, including the selection of targets for orienting movements 34,35 and also selection of visual stimuli in the absence of orienting movements 6,36 .…”

Visual processing and fold-change detection by the larva of the simple chordateCiona

“…Results presented here, as well as published studies (Bostwick et al, 2020), point to the pBV as a sensory processing and integrating center. Thus in many ways the function of the pBV resembles that of the vertebrate midbrain visual processing centers, including the optic tectum (Knudsen, 2020). The resemblance of the pBV to the vertebrate midbrain extends to the Ciona CNS anatomy as well.…”

Experience-dependent refinement of natural approach responses towards specific visual stimuli in mice

“…It will therefore be interesting in future studies to determine whether specific information first computed in the retina and relayed via distinct retinal ganglion cell types to different projection targets is sufficient to rapidly drive each type of orienting response, or whether it must be further transformed or filtered in target regions in order to generate observed behavioral responses (El-Danaf and Huberman 2019; Lee et al 2020). Almost ninety percent of RGCs in the mouse project to the superior colliculus, which contains cells with response properties similar to those found in the retina (Gale & Murphy, 2014) and is known to mediate visual attention (Krauzlis et al 2013;Knudsen 2020) and orienting (Dean & Redgrave, 1984;Overton et al, 1985;Westby et al, 1990). In the zebrafish, discrete RGC types have indeed been shown to underlie approach, while visual stimulus feature-driven decisions to approach or avoid are computed and encoded in the optic tectum, homologous to the superior colliculus (Semmelhack et al 2014).…”

“…The ability to rapidly orient towards prey or away from predators from a distance is crucial for the survival of animals. Thus, visual systems are evolutionarily honed to extract the specific visual cues that reliably distinguish objects as potentially rewarding or threatening and rapidly drive appropriate orienting behaviors (Dean, Redgrave, and Westby 1989;Knudsen 2020).…”