Evolution of neural processing for visual perception in vertebrates.

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.

Neural Circuits That Mediate Selective Attention: A Comparative Perspective.

Selective attention is central to cognition. Dramatic advances have been made in understanding the neural circuits that mediate selective attention. Forebrain networks, most elaborated in primates, control all forms of attention based on task demands and the physical salience of stimuli. These networks contain circuits that distribute top-down signals to sensory processing areas and enhance information processing in those areas. A midbrain network, most elaborated in birds, controls spatial attention. It contains circuits that continuously compute the highest priority stimulus location and route sensory information from the selected location to forebrain networks that make cognitive decisions. The identification of these circuits, their functions and mechanisms represent a major advance in our understanding of how the vertebrate brain mediates selective attention.

Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network.

Perceptual decisions require both analysis of sensory information and selective routing of relevant information to decision networks. This study explores the contribution of a midbrain network to visual perception in chickens. Analysis of visual orientation information in birds takes place in the forebrain sensory area called the Wulst, as it does in the primary visual cortex (V1) of mammals. In contrast, the midbrain, which receives parallel retinal input, encodes orientation poorly, if at all. We discovered, however, that small electrolytic lesions in the midbrain severely impair a chicken's ability to discriminate orientations. Focal lesions were placed in the optic tectum (OT) and in the nucleus isthmi pars parvocellularis (Ipc)-key nodes in the midbrain stimulus selection network-in chickens trained to perform an orientation discrimination task. A lesion in the OT caused a severe impairment in orientation discrimination specifically for targets at the location in space represented by the lesioned location. Distracting stimuli increased the deficit. A lesion in the Ipc produced similar but more transient effects. We discuss the possibilities that performance deficits were caused by interference with orientation information processing (sensory deficit) versus with the routing of information in the forebrain (agnosia). The data support the proposal that the OT transmits a space-specific signal that is required to gate orientation information from the Wulst into networks that mediate behavioral decisions, analogous to the role of ascending signals from the superior colliculus (SC) in monkeys. Furthermore, our results indicate a critical role for the cholinergic Ipc in this gating process.

Does the Superior Colliculus Control Perceptual Sensitivity or Choice Bias during Attention? Evidence from a Multialternative Decision Framework.

Distinct networks in the forebrain and the midbrain coordinate to control spatial attention. The critical involvement of the superior colliculus (SC)-the central structure in the midbrain network-in visuospatial attention has been shown by four seminal, published studies in monkeys (Macaca mulatta) performing multialternative tasks. However, due to the lack of a mechanistic framework for interpreting behavioral data in such tasks, the nature of the SC's contribution to attention remains unclear. Here we present and validate a novel decision framework for analyzing behavioral data in multialternative attention tasks. We apply this framework to re-examine the behavioral evidence from these published studies. Our model is a multidimensional extension to signal detection theory that distinguishes between two major classes of attentional mechanisms: those that alter the quality of sensory information or "sensitivity," and those that alter the selective gating of sensory information or "choice bias." Model-based simulations and model-based analyses of data from these published studies revealed a converging pattern of results that indicated that choice-bias changes, rather than sensitivity changes, were the primary outcome of SC manipulation. Our results suggest that the SC contributes to attentional performance predominantly by generating a spatial choice bias for stimuli at a selected location, and that this bias operates downstream of forebrain mechanisms that enhance sensitivity. The findings lead to a testable mechanistic framework of how the midbrain and forebrain networks interact to control spatial attention. SIGNIFICANCE STATEMENT: Attention involves the selection of the most relevant information for differential sensory processing and decision making. While the mechanisms by which attention alters sensory encoding (sensitivity control) are well studied, the mechanisms by which attention alters decisional weighting of sensory evidence (choice-bias control) are poorly understood. Here, we introduce a model of multialternative decision making that distinguishes bias from sensitivity effects in attention tasks. With our model, we simulate experimental data from four seminal studies that microstimulated or inactivated a key attention-related midbrain structure, the superior colliculus (SC). We demonstrate that the experimental effects of SC manipulation are entirely consistent with the SC controlling attention by changing choice bias, thereby shedding new light on how the brain mediates attention.

Spatially precise visual gain control mediated by a cholinergic circuit in the midbrain attention network.

A primary function of the midbrain stimulus selection network is to compute the highest-priority location for attention and gaze. Here we report the contribution of a specific cholinergic circuit to this computation. We functionally disconnected the tegmental cholinergic nucleus isthmi pars parvocellularis (Ipc) from the optic tectum (OT) in barn owls by reversibly blocking excitatory transmission in the Ipc. Focal blockade in the Ipc decreases the gain and spatial discrimination of OT units specifically for the locations represented by the visual receptive fields (VRFs) of the disconnected Ipc units, and causes OT VRFs to shift away from that location. The results demonstrate mechanisms by which this cholinergic circuit controls bottom-up stimulus competition and by which top-down signals can bias this competition, and they establish causal linkages between a particular circuit, gain control and dynamic shifts of VRFs. This circuit may perform the same function in all vertebrate species.

Cholinergic control of gamma power in the midbrain spatial attention network.

The modulation of gamma power (25-90 Hz) is associated with attention and has been observed across species and brain areas. However, mechanisms that control these modulations are poorly understood. The midbrain spatial attention network in birds generates high-amplitude gamma oscillations in the local field potential that are thought to represent the highest priority location for attention. Here we explore, in midbrain slices from chickens, mechanisms that regulate the power of these oscillations, using high-resolution techniques including intracellular recordings from neurons targeted by calcium imaging. The results identify a specific subtype of neuron, expressing non-α7 nicotinic acetylcholine receptors, that directly drives inhibition in the gamma-generating circuit and switches the network into a primed state capable of producing high-amplitude oscillations. The special properties of this mechanism enable rapid, persistent changes in gamma power. The brain may employ this mechanism wherever rapid modulations of gamma power are critical to information processing.

Gamma oscillations in the midbrain spatial attention network: linking circuits to function.

Gamma-band (25-140Hz) oscillations are ubiquitous in mammalian forebrain structures involved in sensory processing, attention, learning and memory. The optic tectum (OT) is the central structure in a midbrain network that participates critically in controlling spatial attention. In this review, we summarize recent advances in characterizing a neural circuit in this midbrain network that generates large amplitude, space-specific, gamma oscillations in the avian OT, both in vivo and in vitro. We describe key physiological and pharmacological mechanisms that produce and regulate the structure of these oscillations. The extensive similarities between midbrain gamma oscillations in birds and those in the neocortex and hippocampus of mammals, offer important insights into the functional significance of a midbrain gamma oscillatory code.

Selective disinhibition: A unified neural mechanism for predictive and post hoc attentional selection.

The natural world presents us with a rich and ever-changing sensory landscape containing diverse stimuli that constantly compete for representation in the brain. When the brain selects a stimulus as the highest priority for attention, it differentially enhances the representation of the selected, "target" stimulus and suppresses the processing of other, distracting stimuli. A stimulus may be selected for attention while it is still present in the visual scene (predictive selection) or after it has vanished (post hoc selection). We present a biologically inspired computational model that accounts for the prioritized processing of information about targets that are selected for attention either predictively or post hoc. Central to the model is the neurobiological mechanism of "selective disinhibition" - the selective suppression of inhibition of the representation of the target stimulus. We demonstrate that this mechanism explains major neurophysiological hallmarks of selective attention, including multiplicative neural gain, increased inter-trial reliability (decreased variability), and reduced noise correlations. The same mechanism also reproduces key behavioral hallmarks associated with target-distracter interactions. Selective disinhibition exhibits several distinguishing and advantageous features over alternative mechanisms for implementing target selection, and is capable of explaining the effects of selective attention over a broad range of real-world conditions, involving both predictive and post hoc biasing of sensory competition and decisions.

Descending control of neural bias and selectivity in a spatial attention network: rules and mechanisms.

The brain integrates stimulus-driven (exogenous) activity with internally generated (endogenous) activity to compute the highest priority stimulus for gaze and attention. Little is known about how this computation is accomplished neurally. We explored the underlying functional logic in a critical component of the spatial attention network, the optic tectum (OT, superior colliculus in mammals), in awake barn owls. We found that space-specific endogenous influences, evoked by activating descending forebrain pathways, bias competition among exogenous influences, and substantially enhance the quality of the categorical neural pointer to the highest priority stimulus. These endogenous influences operate across sensory modalities. Biologically grounded modeling revealed that the observed effects on network bias and selectivity require a simple circuit mechanism: endogenously driven gain modulation of feedback inhibition among competing channels. Our findings reveal fundamental principles by which internal and external information combine to guide selection of the next target for gaze and attention.

Distinguishing bias from sensitivity effects in multialternative detection tasks.

Studies investigating the neural bases of cognitive phenomena increasingly employ multialternative detection tasks that seek to measure the ability to detect a target stimulus or changes in some target feature (e.g., orientation or direction of motion) that could occur at one of many locations. In such tasks, it is essential to distinguish the behavioral and neural correlates of enhanced perceptual sensitivity from those of increased bias for a particular location or choice (choice bias). However, making such a distinction is not possible with established approaches. We present a new signal detection model that decouples the behavioral effects of choice bias from those of perceptual sensitivity in multialternative (change) detection tasks. By formulating the perceptual decision in a multidimensional decision space, our model quantifies the respective contributions of bias and sensitivity to multialternative behavioral choices. With a combination of analytical and numerical approaches, we demonstrate an optimal, one-to-one mapping between model parameters and choice probabilities even for tasks involving arbitrarily large numbers of alternatives. We validated the model with published data from two ternary choice experiments: a target-detection experiment and a length-discrimination experiment. The results of this validation provided novel insights into perceptual processes (sensory noise and competitive interactions) that can accurately and parsimoniously account for observers' behavior in each task. The model will find important application in identifying and interpreting the effects of behavioral manipulations (e.g., cueing attention) or neural perturbations (e.g., stimulation or inactivation) in a variety of multialternative tasks of perception, attention, and decision-making.

Selective attention in birds.

The natural world constantly inundates our senses with an abundance of information. Selective attention enables us to navigate this abundance intelligently by selecting the information that is most relevant, at each moment in time, for differential processing and decision-making. The attributes of attention have been studied in humans for over a century. In his influential 19(th) century treatise, The Principles of Psychology, philosopher and psychologist William James defined attention as: "… the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought … It implies withdrawal from some things in order to deal effectively with others." (James, 1890). James' definition elegantly captures two key hallmarks of attention: the enhanced processing of task-relevant information (target information) and the suppression of task-irrelevant information (distracting information).

Visuospatial selective attention in chickens.

Voluntary control of attention promotes intelligent, adaptive behaviors by enabling the selective processing of information that is most relevant for making decisions. Despite extensive research on attention in primates, the capacity for selective attention in nonprimate species has never been quantified. Here we demonstrate selective attention in chickens by applying protocols that have been used to characterize visual spatial attention in primates. Chickens were trained to localize and report the vertical position of a target in the presence of task-relevant distracters. A spatial cue, the location of which varied across individual trials, indicated the horizontal, but not vertical, position of the upcoming target. Spatial cueing improved localization performance: accuracy (d') increased and reaction times decreased in a space-specific manner. Distracters severely impaired perceptual performance, and this impairment was greatly reduced by spatial cueing. Signal detection analysis with an "indecision" model demonstrated that spatial cueing significantly increased choice certainty in localizing targets. By contrast, error-aversion certainty (certainty of not making an error) remained essentially constant across cueing protocols, target contrasts, and individuals. The results show that chickens shift spatial attention rapidly and dynamically, following principles of stimulus selection that closely parallel those documented in primates. The findings suggest that the mechanisms that control attention have been conserved through evolution, and establish chickens--a highly visual species that is easily trained and amenable to cutting-edge experimental technologies--as an attractive model for linking behavior to neural mechanisms of selective attention.

Spatially reciprocal inhibition of inhibition within a stimulus selection network in the avian midbrain.

Reciprocal inhibition between inhibitory projection neurons has been proposed as the most efficient circuit motif to achieve the flexible selection of one stimulus among competing alternatives. However, whether such a motif exists in networks that mediate selection is unclear. Here, we study the connectivity within the nucleus isthmi pars magnocellularis (Imc), a GABAergic nucleus that mediates competitive selection in the midbrain stimulus selection network. Using laser photostimulation of caged glutamate, we find that feedback inhibitory connectivity is global within the Imc. Unlike typical lateral inhibition in other circuits, intra-Imc inhibition remains functionally powerful over long distances. Anatomically, we observed long-range axonal projections and retrograde somatic labeling from focal injections of bi-directional tracers in the Imc, consistent with spatial reciprocity of intra-Imc inhibition. Together, the data indicate that spatially reciprocal inhibition of inhibition occurs throughout the Imc. Thus, the midbrain selection circuit possesses the most efficient circuit motif possible for fast, reliable, and flexible selection.

Magnetic tracking of eye position in freely behaving chickens.

Research on the visual system of non-primates, such as birds and rodents, is increasing. Evidence that neural responses can differ dramatically between head-immobilized and freely behaving animals underlines the importance of studying visual processing in ethologically relevant contexts. In order to systematically study visual responses in freely behaving animals, an unobtrusive system for monitoring eye-in-orbit position in real time is essential. We describe a novel system for monitoring eye position that utilizes a head-mounted magnetic displacement sensor coupled with an eye-implanted magnet. This system is small, lightweight, and offers high temporal and spatial resolution in real time. We use the system to demonstrate the stability of the eye and the stereotypy of eye position during two different behavioral tasks in chickens. This approach offers a viable alternative to search coil and optical eye tracking techniques for high resolution tracking of eye-in-orbit position in behaving animals.

Spatial probability dynamically modulates visual target detection in chickens.

The natural world contains a rich and ever-changing landscape of sensory information. To survive, an organism must be able to flexibly and rapidly locate the most relevant sources of information at any time. Humans and non-human primates exploit regularities in the spatial distribution of relevant stimuli (targets) to improve detection at locations of high target probability. Is the ability to flexibly modify behavior based on visual experience unique to primates? Chickens (Gallus domesticus) were trained on a multiple alternative Go/NoGo task to detect a small, briefly-flashed dot (target) in each of the quadrants of the visual field. When targets were presented with equal probability (25%) in each quadrant, chickens exhibited a distinct advantage for detecting targets at lower, relative to upper, hemifield locations. Increasing the probability of presentation in the upper hemifield locations (to 80%) dramatically improved detection performance at these locations to be on par with lower hemifield performance. Finally, detection performance in the upper hemifield changed on a rapid timescale, improving with successive target detections, and declining with successive detections at the diagonally opposite location in the lower hemifield. These data indicate the action of a process that in chickens, as in primates, flexibly and dynamically modulates detection performance based on the spatial probabilities of sensory stimuli as well as on recent performance history.

A shared inhibitory circuit for both exogenous and endogenous control of stimulus selection.

The mechanisms by which the brain suppresses distracting stimuli to control the locus of attention are unknown. We found that focal, reversible inactivation of a single inhibitory circuit in the barn owl midbrain tegmentum, the nucleus isthmi pars magnocellularis (Imc), abolished both stimulus-driven (exogenous) and internally driven (endogenous) competitive interactions in the optic tectum (superior colliculus in mammals), which are vital to the selection of a target among distractors in behaving animals. Imc neurons transformed spatially precise multisensory and endogenous input into powerful inhibitory output that suppressed competing representations across the entire tectal space map. We identified a small, but highly potent, circuit that is employed by both exogenous and endogenous signals to exert competitive suppression in the midbrain selection network. Our findings reveal, to the best of our knowledge, for the first time, a neural mechanism for the construction of a priority map that is critical for the selection of the most important stimulus for gaze and attention.

Gamma oscillations are generated locally in an attention-related midbrain network.

Gamma-band (25-140 Hz) oscillations are a hallmark of sensory processing in the forebrain. The optic tectum (OT), a midbrain structure implicated in sensorimotor processing and attention, also exhibits gamma oscillations. However, the origin and mechanisms of these oscillations remain unknown. We discovered that in acute slices of the avian OT, persistent (>100 ms) epochs of large amplitude gamma oscillations can be evoked that closely resemble those recorded in vivo. We found that cholinergic, glutamatergic, and GABAergic mechanisms differentially regulate the structure of the oscillations at various timescales. These persistent oscillations originate in the multisensory layers of the OT and are broadcast to visual layers via the cholinergic nucleus Ipc, providing a potential mechanism for enhancing the processing of visual information within the OT. The finding that the midbrain contains an intrinsic gamma-generating circuit suggests that the OT could use its own oscillatory code to route signals to forebrain networks.

Reciprocal inhibition of inhibition: a circuit motif for flexible categorization in stimulus selection.

As a precursor to the selection of a stimulus for gaze and attention, a midbrain network categorizes stimuli into "strongest" and "others." The categorization tracks flexibly, in real time, the absolute strength of the strongest stimulus. In this study, we take a first-principles approach to computations that are essential for such categorization. We demonstrate that classical feedforward lateral inhibition cannot produce flexible categorization. However, circuits in which the strength of lateral inhibition varies with the relative strength of competing stimuli categorize successfully. One particular implementation--reciprocal inhibition of feedforward lateral inhibition--is structurally the simplest, and it outperforms others in flexibly categorizing rapidly and reliably. Strong predictions of this anatomically supported circuit model are validated by neural responses measured in the owl midbrain. The results demonstrate the extraordinary power of a remarkably simple, neurally grounded circuit motif in producing flexible categorization, a computation fundamental to attention, perception, and decision making.

The role of a midbrain network in competitive stimulus selection.

A midbrain network interacts with the well-known frontoparietal forebrain network to select stimuli for gaze and spatial attention. The midbrain network, containing the superior colliculus (SC; optic tectum, OT, in non-mammalian vertebrates) and the isthmic nuclei, helps evaluate the relative priorities of competing stimuli and encodes them in a topographic map of space. Behavioral experiments in monkeys demonstrate an essential contribution of the SC to stimulus selection when the relative priorities of competing stimuli are similar. Neurophysiological results from the owl OT demonstrate a neural correlate of this essential contribution of the SC/OT. The multi-layered, spatiotopic organization of the midbrain network lends itself to the analysis and modeling of the mechanisms underlying stimulus selection for gaze and spatial attention.

Control from below: the role of a midbrain network in spatial attention.

Spatial attention enables the brain to analyse and evaluate information selectively from a specific location in space, a capacity essential for any animal to behave adaptively in a complex world. We usually think of spatial attention as being controlled by a frontoparietal network in the forebrain. However, emerging evidence shows that a midbrain network also plays a critical role in controlling spatial attention. Moreover, the highly differentiated, retinotopic organization of the midbrain network, especially in birds, makes it amenable to detailed analysis with modern techniques that can elucidate circuit, cellular and synaptic mechanisms of attention. The following review discusses the role of the midbrain network in controlling attention, the neural circuits that support this role and current knowledge about the computations performed by these circuits.