Selective attention without a neocortex

Abstract

Selective attention refers to the ability to restrict neural processing and behavioral responses to a relevant subset of available stimuli, while simultaneously excluding other valid stimuli from consideration. In primates and other mammals, descriptions of this ability typically emphasize the neural processing that takes place in the cerebral neocortex. However, non-mammals such as birds, reptiles, amphibians and fish, which completely lack a neocortex, also have the ability to selectively attend. In this article, we survey the behavioral evidence for selective attention in non-mammals, and review the midbrain and forebrain structures that are responsible. The ancestral forms of selective attention are presumably selective orienting behaviors, such as prey-catching and predator avoidance. These behaviors depend critically on a set of subcortical structures, including the optic tectum (OT), thalamus and striatum, that are highly conserved across vertebrate evolution. In contrast, the contributions of different pallial regions in the forebrain to selective attention have been subject to more substantial changes and reorganization. This evolutionary perspective makes plain that selective attention is not a function achieved de novo with the emergence of the neocortex, but instead is implemented by circuits accrued and modified over hundreds of millions of years, beginning well before the forebrain contained a neocortex. Determining how older subcortical circuits interact with the more recently evolved components in the neocortex will likely be crucial for understanding the complex properties of selective attention in primates and other mammals, and for identifying the etiology of attention disorders.

Keywords: Attention; Evolution; Neocortex; Optic tectum; Striatum; Thalamus.

Figure 1. Evolution and comparison of the brain plans in mammals and non-mammals

A. Simplified cladogram illustrating the divergence of vertebrate lines during the course of evolution. Mammals diverged about 200 million years ago (mya) from a line of animals (therapsids) that are now extinct, while birds are believed to have diverged more recently (150 mya) from a line that gave rise to modern reptiles (E. D. Jarvis et al., 2005). Vertebrates highlighted in bold are discussed in detail in the article. B. Diagram illustrating a lateral view of a simplified and generic mammalian brain, based loosely on the monkey brain. Regions implicated in selective attention are highlighted in color. C. Lateral view of a simplified and generic non-mammalian brain, based loosely on the bird brain. Brain regions implicated in selective attention are again highlighted, using colors matching those in (B) to indicate homologies.

Figure 2. Behavioral evidence of selective attention in chickens

A. Schematic of the behavioral task. Chickens performed a target localization task that required them to report the vertical location of a target stimulus while ignoring a task-irrelevant distracter. On trials with no cue, the chicken could not know which of the two stimuli was the target until the response boxes were presented at the end of the trial. On trials with a cue, the chicken had prior information about which stimulus was behaviorally relevant and could ignore the other one. B. Psychometric functions showing performance (percent correct) as a function of relative target strength (target to distracter contrast ratio). Performance on trials with a cue (red) was better than performance on trials with no cue (gray). C. Response times with and without cues, plotted as a function of relative target strength. Reaction times on trials with a cue (red) were faster than on trials with no cue (gray). Adapted with permission from (Sridharan et al., 2014).

Figure 3. Schematic diagram of the bird brain

The lateral view illustrates the prominent position of the optic tectum (OT) in the midbrain, and outlines the locations of the visual Wulst and entopallium in the forebrain. The midbrain slice shows the spatial relationship between the optic tectum, and the adjacent nucleus isthmi pars parvocellularis (Ipc) and nucleus isthmi pars magnocellularis (Imc). The sagittal section provides a cut-away view that makes other attention-related structures visible: the isthmo-optic nucleus (ION) in the midbrain, the nucleus rotundus (Rt) and lateral geniculate nucleus pars dorsalis (GLd) in the thalamus, and the striatum and arcopallial gaze field (AGF) in the forebrain.

Figure 4. Brain and prey-catching in the frog

A. Lateral view of the frog brain, showing the location of the optic tectum (OT) and pretectal nucleli (pT) in the midbrain, and the striatum and dorsal pallium in the forebrain. B. Dorsal view of the frog brain (left) and schematic illustration (right) of the range of visual field locations that elicit prey-catching responses in the intact frog. C. Dorsal view of the frog brain after removal of the left optic tectum (left), and illustration (right) of the loss of prey-catching behavior in the affected portion of the right visual field. Prey-catching diagrams in panels (B) and (C) are a schematic reconstruction of the data presented in (Kostyk & Grobstein, 1982; 1987).

Figure 5. Brain and behavior in the zebrafish

A. Dorsal view of a zebrafish illustrating the J-turn tail movement and convergent eye movements elicited by the presentation of a visual prey stimulus. B. Dorsal schematic view of the zebrafish brain showing the locations of the optic tectum and pallium. C. Image of larval zebrafish brain obtained using light-sheet microscopy while animal was presented with moving visual stimuli. Because the brain is small and the tissues are transparent, it is possible to image individual neurons throughout the tectum and pallium. Individual neurons are color-coded based on their preferred direction of motion, with magenta indicating preference for rightward motion and yellow indicating preference for leftward motion. Image reproduced with permission from (Freeman et al., 2014). D. Schematic diagram of the aquarium tank used in a 2-alternative choice task. After being introduced in the holding area, a trial was started when the opaque barriers were removed and the fish gained access to the choice zone and food delivery areas. Fish expressed their choice by swimming into one of the two food delivery areas and approaching the colored visual stimulus. E. The number of trials required to reach criterion performance (6 consecutive correct trials) during the four phases of the experiment. Panels (D) and (E) adapted with permission from (Parker et al., 2012).

Figure 6. Behavioral evidence of selective attention in archer fish

A. Typical experimental arrangement with archer fish. Visual stimuli were presented on a visual display suspended over an aquarium. Reaction time was determined by contact of the water jet with a glass sheet protecting the visual display, and correct shots were rewarded with a small pellet of food. B. Schematic of a behavioral task using valid and invalid cues. On most trials (80%), the valid cue was presented that correctly indicated the location of the target stimulus. On a minority of trials (20%), an invalid cue was presented instead. Reaction time of the shot depended on the validity of the cue and the time delay between the cue and target appearance. C. Behavioral task using symbolic cues. The cue was presented at a central location on the display and its color (red or green) indicated the likely location of the upcoming target.