The Ecological View of Selective Attention.

Accumulating evidence is supporting the hypothesis that our selective attention is a manifestation of mechanisms that evolved early in evolution and are shared by many organisms from different taxa. This surge of new data calls for the re-examination of our notions about attention, which have been dominated mostly by human psychology. Here, we present an hypothesis that challenges, based on evolutionary grounds, a common view of attention as a means to manage limited brain resources. We begin by arguing that evolutionary considerations do not favor the basic proposition of the limited brain resources view of attention, namely, that the capacity of the sensory organs to provide information exceeds the capacity of the brain to process this information. Moreover, physiological studies in animals and humans show that mechanisms of selective attention are highly demanding of brain resources, making it paradoxical to see attention as a means to release brain resources. Next, we build on the above arguments to address the question why attention evolved in evolution. We hypothesize that, to a certain extent, limiting sensory processing is adaptive irrespective of brain capacity. We call this hypothesis the ecological view of attention (EVA) because it is centered on interactions of an animal with its environment rather than on internal brain resources. In its essence is the notion that inherently noisy and degraded sensory inputs serve the animal's adaptive, dynamic interactions with its environment. Attention primarily functions to resolve behavioral conflicts and false distractions. Hence, we evolved to focus on a particular target at the expense of others, not because of internal limitations, but to ensure that behavior is properly oriented and committed to its goals. Here, we expand on this notion and review evidence supporting it. We show how common results in human psychophysics and physiology can be reconciled with an EVA and discuss possible implications of the notion for interpreting current results and guiding future research.

Optimizing intact skull intrinsic signal imaging for subsequent targeted electrophysiology across mouse visual cortex.

Understanding brain function requires repeatable measurements of neural activity across multiple scales and multiple brain areas. In mice, large scale cortical neural activity evokes hemodynamic changes readily observable with intrinsic signal imaging (ISI). Pairing ISI with visual stimulation allows identification of primary visual cortex (V1) and higher visual areas (HVAs), typically through cranial windows that thin or remove the skull. These procedures can diminish long-term mechanical and physiological stability required for delicate electrophysiological measurements made weeks to months after imaging (e.g., in subjects undergoing behavioral training). Here, we optimized and directly validated an intact skull ISI system in mice. We first assessed how imaging quality and duration affect reliability of retinotopic maps in V1 and HVAs. We then verified ISI map retinotopy in V1 and HVAs with targeted, multi-site electrophysiology several weeks after imaging. Reliable ISI maps of V1 and multiple HVAs emerged with ~ 60 trials of imaging (65 ± 6 min), and these showed strong correlation to local field potential (LFP) retinotopy in superficial cortical layers (r2 = 0.74-0.82). This system is thus well-suited for targeted, multi-area electrophysiology weeks to months after imaging. We provide detailed instructions and code for other researchers to implement this system.

Vision in chameleons-A model for non-mammalian vertebrates.

Chameleons (Chamaeleonidae, Reptilia) are known for their extreme sensory and motor adaptations to arboreal life and insectivoury. They show most distinct sequences of visuo-motor patterns in threat avoidance and in predation with prey capture being performed by tongue strikes that are unparalleled in vertebrates. Optical adaptations result in retinal image enlargement and the unique capacity to determine target distance by accommodation cues. Ocular adaptations result in complex eye movements that are context dependent, not independent, as observed in threat avoidance and predation. In predation, evidence from the chameleons' capacity to track multiple targets support the view that their eyes are under individual controls. Eye movements and body movements are lateralised, with lateralisation being a function of many factors at the population, individual, and specific-situation levels. Chameleons are considered a potentially important model for vision in non-mammalian vertebrates. They provide exceptional behavioural tools for studying eye movements as well as information gathering and analysis. They open the field of lateralisation, decision making, and context dependence. Finally, chameleons allow a deeper examination of the relationships between their unique visuo-motor capacities and the central nervous system of reptiles and ectotherms, in general, as compared with mammals.

Behavioral and neuronal study of inhibition of return in barn owls.

Inhibition of return (IOR) is the reduction of detection speed and/or detection accuracy of a target in a recently attended location. This phenomenon, which has been discovered and studied thoroughly in humans, is believed to reflect a brain mechanism for controlling the allocation of spatial attention in a manner that enhances efficient search. Findings showing that IOR is robust, apparent at a very early age and seemingly dependent on midbrain activity suggest that IOR is a universal attentional mechanism in vertebrates. However, studies in non-mammalian species are scarce. To explore this hypothesis comparatively, we tested for IOR in barn owls (Tyto alba) using the classical Posner cueing paradigm. Two barn owls were trained to initiate a trial by fixating on the center of a computer screen and then turning their gaze to the location of a target. A short, non-informative cue appeared before the target, either at a location predicting the target (valid) or a location not predicting the target (invalid). In one barn owl, the response times (RT) to the valid targets compared to the invalid targets shifted from facilitation (lower RTs) to inhibition (higher RTs) when increasing the time lag between the cue and the target. The second owl mostly failed to maintain fixation and responded to the cue before the target onset. However, when including in the analysis only the trials in which the owl maintained fixation, an inhibition in the valid trials could be detected. To search for the neural correlates of IOR, we recorded multiunit responses in the optic tectum (OT) of four head-fixed owls passively viewing a cueing paradigm as in the behavioral experiments. At short cue to target lags (<100 ms), neural responses to the target in the receptive field (RF) were usually enhanced if the cue appeared earlier inside the RF (valid) and were suppressed if the cue appeared earlier outside the RF (invalid). This was reversed at longer lags: neural responses were suppressed in the valid conditions and were unaffected in the invalid conditions. The findings support the notion that IOR is a basic mechanism in the evolution of vertebrate behavior and suggest that the effect appears as a result of the interaction between lateral and forward inhibition in the tectal circuitry.

Self-motion trajectories can facilitate orientation-based figure-ground segregation.

Segregation of objects from the background is a basic and essential property of the visual system. We studied the neural detection of objects defined by orientation difference from background in barn owls (Tyto alba). We presented wide-field displays of densely packed stripes with a dominant orientation. Visual objects were created by orienting a circular patch differently from the background. In head-fixed conditions, neurons in both tecto- and thalamofugal visual pathways (optic tectum and visual Wulst) were weakly responsive to these objects in their receptive fields. However, notably, in freely viewing conditions, barn owls occasionally perform peculiar side-to-side head motions (peering) when scanning the environment. In the second part of the study we thus recorded the neural response from head-fixed owls while the visual displays replicated the peering conditions; i.e., the displays (objects and backgrounds) were shifted along trajectories that induced a retinal motion identical to sampled peering motions during viewing of a static object. These conditions induced dramatic neural responses to the objects, in the very same neurons that where unresponsive to the objects in static displays. By reverting to circular motions of the display, we show that the pattern of the neural response is mostly shaped by the orientation of the background relative to motion and not the orientation of the object. Thus our findings provide evidence that peering and/or other self-motions can facilitate orientation-based figure-ground segregation through interaction with inhibition from the surround.NEW & NOTEWORTHY Animals frequently move their sensory organs and thereby create motion cues that can enhance object segregation from background. We address a special example of such active sensing, in barn owls. When scanning the environment, barn owls occasionally perform small-amplitude side-to-side head movements called peering. We show that the visual outcome of such peering movements elicit neural detection of objects that are rotated from the dominant orientation of the background scene and which are otherwise mostly undetected. These results suggest a novel role for self-motions in sensing objects that break the regular orientation of elements in the scene.

Behavioral Evidence and Neural Correlates of Perceptual Grouping by Motion in the Barn Owl.

Perceiving an object as salient from its surround often requires a preceding process of grouping the object and background elements as perceptual wholes. In humans, motion homogeneity provides a strong cue for grouping, yet it is unknown to what extent this occurs in nonprimate species. To explore this question, we studied the effects of visual motion homogeneity in barn owls of both genders, at the behavioral as well as the neural level. Our data show that the coherency of the background motion modulates the perceived saliency of the target object. An object moving in an odd direction relative to other objects attracted more attention when the other objects moved homogeneously compared with when moved in a variety of directions. A possible neural correlate of this effect may arise in the population activity of the intermediate/deep layers of the optic tectum. In these layers, the neural responses to a moving element in the receptive field were suppressed when additional elements moved in the surround. However, when the surrounding elements all moved in one direction (homogeneously moving), they induced less suppression of the response compared with nonhomogeneously moving elements. Moreover, neural responses were more sensitive to the homogeneity of the background motion than to motion-direction contrasts between the receptive field and the surround. The findings suggest similar principles of saliency-by-motion in an avian species as in humans and show a locus in the optic tectum where the underlying neural circuitry may exist.SIGNIFICANCE STATEMENT A critical task of the visual system is to arrange incoming visual information to a meaningful scene of objects and background. In humans, elements that move homogeneously are grouped perceptually to form a categorical whole object. We discovered a similar principle in the barn owl's visual system, whereby the homogeneity of the motion of elements in the scene allows perceptually distinguishing an object from its surround. The novel findings of these visual effects in an avian species, which lacks neocortical structure, suggest that our basic visual perception shares more universal principles across species than presently thought, and shed light on possible brain mechanisms for perceptual grouping.

Interactions between top-down and bottom-up attention in barn owls (Tyto alba).

Selective attention, the prioritization of behaviorally relevant stimuli for behavioral control, is commonly divided into two processes: bottom-up, stimulus-driven selection and top-down, task-driven selection. Here, we tested two barn owls in a visual search task that examines attentional capture of the top-down task by bottom-up mechanisms. We trained barn owls to search for a vertical Gabor patch embedded in a circular array of differently oriented Gabor distractors (top-down guided search). To track the point of gaze, a lightweight wireless video camera was mounted on the owl's head. Three experiments were conducted in which the owls were tested in the following conditions: (1) five distractors; (2) nine distractors; (3) five distractors with one distractor surrounded by a red circle; or (4) five distractors with a brief sound at the initiation of the stimulus. Search times and number of head saccades to reach the target were measured and compared between the different conditions. It was found that search time and number of saccades to the target increased when the number of distractors was larger (condition 2) and when an additional irrelevant salient stimulus, auditory or visual, was added to the scene (conditions 3 and 4). These results demonstrate that in barn owls, bottom-up attention interacts with top-down attention to shape behavior in ways similar to human attentional capture. The findings suggest similar attentional principles in taxa that have been evolutionarily separated for 300 million years.

Great cormorants (Phalacrocorax carbo) as potential vectors for the dispersal of Vibrio cholerae.

Vibrio cholerae is the cause of cholera, a devastating epidemic and pandemic disease. Despite its importance, the way of its global dissemination is unknown. V. cholerae is abundant in aquatic habitats and is known to be borne by copepods, chironomids and fishes. Our aim was to determine if fish-eating birds act as vectors in the spread of V. cholerae by consuming infected fish. We determined the existence of V. cholerae in the microbiome of 5/7 wild cormorants' intestine. In three of these V. cholerae-positive wild cormorants, the presence of a gene for cholera toxin (ctxA) was detected. We subsequently tested eight captive, hand-reared cormorants, divided into two equal groups. Prior to the experiment, the feces of the cormorants were V. cholerae-negative. One group was fed exclusively on tilapias, which are naturally infected with V. cholerae, and the other was fed exclusively on goldfish or on koi that were V. cholerae-negative. We detected V. cholerae in the feces of the tilapia-fed, but not in the goldfish/koi-fed, cormorants. Hence, we demonstrate that fish-eating birds can be infected with V. cholerae from their fish prey. The large-scale movements of many fish-eating birds provide a potential mechanism for the global distribution of V. cholerae.

Avoidance of a moving threat in the common chameleon (Chamaeleo chamaeleon): rapid tracking by body motion and eye use.

A chameleon (Chamaeleo chamaeleon) on a perch responds to a nearby threat by moving to the side of the perch opposite the threat, while bilaterally compressing its abdomen, thus minimizing its exposure to the threat. If the threat moves, the chameleon pivots around the perch to maintain its hidden position. How precise is the body rotation and what are the patterns of eye movement during avoidance? Just-hatched chameleons, placed on a vertical perch, on the side roughly opposite to a visual threat, adjusted their position to precisely opposite the threat. If the threat were moved on a horizontal arc at angular velocities of up to 85°/s, the chameleons co-rotated smoothly so that (1) the angle of the sagittal plane of the head relative to the threat and (2) the direction of monocular gaze, were positively and significantly correlated with threat angular position. Eye movements were role-dependent: the eye toward which the threat moved maintained a stable gaze on it, while the contralateral eye scanned the surroundings. This is the first description, to our knowledge, of such a response in a non-flying terrestrial vertebrate, and it is discussed in terms of possible underlying control systems.

Eye movements in chameleons are not truly independent - evidence from simultaneous monocular tracking of two targets.

Chameleons perform large-amplitude eye movements that are frequently referred to as independent, or disconjugate. When prey (an insect) is detected, the chameleon's eyes converge to view it binocularly and 'lock' in their sockets so that subsequent visual tracking is by head movements. However, the extent of the eyes' independence is unclear. For example, can a chameleon visually track two small targets simultaneously and monocularly, i.e. one with each eye? This is of special interest because eye movements in ectotherms and birds are frequently independent, with optic nerves that are fully decussated and intertectal connections that are not as developed as in mammals. Here, we demonstrate that chameleons presented with two small targets moving in opposite directions can perform simultaneous, smooth, monocular, visual tracking. To our knowledge, this is the first demonstration of such a capacity. The fine patterns of the eye movements in monocular tracking were composed of alternating, longer, 'smooth' phases and abrupt 'step' events, similar to smooth pursuits and saccades. Monocular tracking differed significantly from binocular tracking with respect to both 'smooth' phases and 'step' events. We suggest that in chameleons, eye movements are not simply 'independent'. Rather, at the gross level, eye movements are (i) disconjugate during scanning, (ii) conjugate during binocular tracking and (iii) disconjugate, but coordinated, during monocular tracking. At the fine level, eye movements are disconjugate in all cases. These results support the view that in vertebrates, basic monocular control is under a higher level of regulation that dictates the eyes' level of coordination according to context.