Orientation saliency without visual cortex and target selection in archer fish

Abstract

Our visual attention is attracted by salient stimuli in our environment and affected by primitive features such as orientation, color, and motion. Perceptual saliency due to orientation contrast has been extensively demonstrated in behavioral experiments with humans and other primates and is believed to be facilitated by the functional organization of the primary visual cortex. In behavioral experiments with the archer fish, a proficient hunter with remarkable visual abilities, we found an orientation saliency effect similar to that observed in human subjects. Given the enormous evolutionary distance between humans and archer fish, our findings suggest that orientation-based saliency constitutes a fundamental building block for efficient visual information processing.orientation contrast | visual information processing | visual saliency | orientation-based texture segregation | visual search T he vast amount of information present in early vision necessitates the operation of selection processes whose bottom-up components are commonly referred to as saliency-based attention (1-4). Some neural correlates of saliency-based processing have been observed in animals as low as Drosophila (5). In the mammalian cortex, however, and in particular primates, these processes interact with several other cortical features, such as orientation selectivity of neurons (6), their topographical organization (6-9), and their connectivity patterns (8,(10)(11)(12)(13), to result in a conspicuous form of visual saliency that is based on orientation (14, 15). Here, in a much simpler animal (the archer fish), we report on orientation-based visual saliency that is qualitatively similar to that observed in humans. These observations demonstrate how evolutionary pressures for efficient visual processing bring distant evolutionary paths to express similar functional solutions and suggest that orientation-based saliency constitutes a universal building block for efficient visual information processing.In their natural environment, archer fish exhibit remarkable preying behavior (Fig. 1A). They are capable of detecting insects resting on overhanging vegetation, knocking them down with accurate streams of water sprouted from their mouth, and efficiently inferring the ballistics of the falling prey to intercept it at the predicted impact point with the water (16,17). Recent studies have demonstrated that these fish can accurately shoot flying insects as well (18), an ability possibly facilitated by their human-like pattern of eye movements (19). Here we ask whether on top of these outstanding capacities, archer fish also exhibit such visual behaviors that are typically associated with the presence of a visual cortex, which these fish lack.Numerous behavioral studies in humans and primates have convincingly demonstrated saliency effects related to visual features such as color, motion, and orientation, through experimental configurations designed to test the so-called "pop out" effect (1,3,20). When subjects are presented with an array of lines,...

Overt attention toward oriented objects in free-viewing barn owls

“…In this sense, our research is similar to a recent study on archer fish, which have been shown to exhibit orientation-based saliency similar to humans (16). Unlike Mokeichev et al (16), however, who explored orientation-based saliency using a rapid forced choice procedure, our experiment was based on free-viewing visual search, reminiscent of the conditions under which this behavior is tested in humans. In both cases, bottom-up mechanisms are likely to play the main role in the observed behavior (although the effects of top-down influence, and of some implicit unspecified task, cannot be excluded), and in both cases the behavioral similarities in the reported findings suggest that visual processes, such as orientation-based visual search, may not necessarily require the elaborate cortical structures typically seen in humans.…”

“…This is in stark contrast to the important ecological function of search strategies in all animals, which should have been optimized according to the ecological and survival needs of a species in the course of evolution. Notable exceptions are visual search strategies reported in pigeons (4,5) and recent orientation-saliency behavior found in archer fish (16).…”

Pop-out in visual search of moving targets in the archer fish

“…To address these questions we studied the archer fish [21][22][23][24][25][26] , a species that lacks a cortex 27 but exhibits complex visual behaviours and unique hunting practices. Owing to its remarkable ability to shoot down prey found on foliage above the water level, and its ability to learn to distinguish between artificial targets presented on a computer monitor in an experimental setting 28 , the archer fish exhibits overt target selection that can be leveraged for reporting psychophysical decisions in controlled lab experiments 24,26,29,30 .…”

“…Owing to its remarkable ability to shoot down prey found on foliage above the water level, and its ability to learn to distinguish between artificial targets presented on a computer monitor in an experimental setting 28 , the archer fish exhibits overt target selection that can be leveraged for reporting psychophysical decisions in controlled lab experiments 24,26,29,30 . At the same time, electrophysiological recordings from the central nervous system of archer fish enable the necessary exploration of neural mechanisms underlying behavioural phenomena 31 .…”

Visual receptive field properties of cells in the optic tectum of the archer fish

“…IN RECENT YEARS, THE ARCHER FISH has proved to be a very productive model in the study of many aspects of visual behavior, from retinal encoding (Tsvilling et al 2012;Vasserman et al 2010), eye movements (Ben-Simon et al 2009), animal competition (Schuster 2011), and visual acuity (Ben-Simon et al 2012a;Temple et al 2010Temple et al , 2013 to tracking of moving targets (Ben-Simon et al 2012b;Schlegel and Schuster 2008;Schuster et al 2006;Timmermans 2000Timmermans , 2001) and visual search (Mokeichev et al 2010). The productivity of the model can be explained, in part, by the ability of the archer fish to overtly report its visual decisions by employing a squirt of water from its mouth aimed at selected targets.…”