Review
Feature Review
Mechanisms of top-down attention

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Attention exhibits characteristic neural signatures in brain regions that process sensory signals. An important area of future research is to understand the nature of top-down signals that facilitate attentional guidance towards behaviorally relevant locations and features. In this review, we discuss recent studies that have made progress towards understanding: (i) the brain structures and circuits involved in attentional allocation; (ii) top-down attention pathways, particularly as elucidated by microstimulation and lesion studies; (iii) top-down modulatory influences involving subcortical structures and reward systems; (iv) plausible substrates and embodiments of top-down signals; and (v) information processing and theoretical constraints that might be helpful in guiding future experiments. Understanding top-down attention is crucial for elucidating the mechanisms by which we can filter sensory information to pay attention to the most behaviorally relevant events.

Introduction

Language is infused with idiomatic expressions that make explicit the distinction between bottom-up (BU) and top-down (TD) processes of attention. We might ask someone to ‘pay attention to the road’ while driving, which implies a voluntary choice to allocate resources to a subset of the perceptual input. Alternatively, we might remark that the orange sports car really ‘caught our attention’. In this case, the resource has been involuntarily captured rather than voluntarily allocated. The distinction is not limited to idiomatic expressions, but rather stems from disparate modes of attentional processing [1]. BU attention is deployed very rapidly and depends exclusively on the properties of a sensory stimulus. By contrast, TD attention is slower and requires more effort to engage.

In the modality of vision, the two modes (BU and TD) give rise to the psychophysical phenomenon of pop-out and set-size effects. In a typical visual search experiment, a subject is presented with a number of items on a display and is asked to find a target item within this display, such as a bar with a particular orientation, or color, or a combination of the two. Pop-out occurs when the target item is significantly distinct from the surrounding items (distractors), such as a horizontal bar among several vertical bars. This different item automatically attracts BU attention (or pops-out) rapidly and independently of the number of distractors 2, 3. By contrast, when the target item is distinguished only by taking into account the conjunction of its features, such as color and orientation, BU cues alone cannot efficiently guide attention and TD attention must be recruited to scan the display. This gives rise to search times that increase with the number of distractors; in other words, a set-size effect is observed. In most real-life situations, the responses of the nervous system to a sensory input depend on both BU influences driven by the sensory stimulus and TD influences shaped by extra-retinal factors such as the current state and goal of the organism 4, 5.

A distinction is also made between two types of TD mechanisms. The first type is intuitively associated with TD and is called the volitional TD process, which can exert its influence through acts of will. The second type is known as a mandatory TD process and it is an automatic, percept-modifying TD mechanism that is pervasive and that volition cannot completely eliminate. The latter TD process can develop through experience-dependent plasticity or during development, and includes contextual modulation of perception 5, 6. A striking example of the dichotomy between these two mechanisms is presented in Figure 1.

Previous work has extensively studied the effects of TD attention on target brain regions, including modulatory effects in early sensory areas 5, 7, 8. Significant progress has been made in isolating the possible sources of TD signals [9], especially within the now well-studied frontoparietal attention network [10]. Much less understood at present are the exact pathways, contents, meaning and form of the signals that are sent from the top down. Here, we review recent findings from physiology, lesion and computational studies that have attempted to elucidate the mechanisms and signals involved in TD modulation of sensory processing. To focus this review, we mainly concern ourselves with visual perception and the volitional TD process, although similar principles can apply in other modalities.

Section snippets

Brain structures and circuits of visual attention

Visual processing begins in the retina, which sends parallel streams of information to the brain through its diverse set of retinal ganglion cells and their unique interactions within the retinal circuitry [11]. A majority of retinal projections reach the lateral geniculate nucleus (LGN) and a much smaller number (approx. 10%) connect to the superior colliculus (SC). The LGN sends projections to the primary visual cortex (V1), the initial site of processing in the cortical feed-forward visual

Pathways of TD attention

In this section, we focus on lesion and electrophysiological studies, particularly those using methods of microstimulation and simultaneous recordings in the brain areas identified in the previous section. These areas form an attentional network (Figure 2) and we consider how TD information is relayed in this network. Microstimulation, together with reversible inactivation [using either pharmacological agents such as muscimol or transcranial magnetic stimulation (TMS)] and permanent lesion

Subcortical influences on TD attention

Evidence suggesting that cortical areas have a strong influence on attention was discussed in the previous section. There are also several subcortical areas that play a crucial role in defining and communicating attentional signals (Figure 5a). It has been demonstrated that the phenomenon of change blindness, in which changes to a particular part of a visual scene go undetected, could be eliminated in monkeys by placing an attention-grabbing salient stimulus in the location where the blindness

The role of reward and emotion in TD attention

Until recently, studies of visual attention have traditionally tended to avoid non-visual aspects of cortical and subcortical neuronal responses to manipulations of attention. This has begun to change with a small number of psychophysical and electrophysiological studies that have explored the interplay between reward and attention.

To investigate the role of reward in modulating attention-related responses in the LIP, stimulus selection has been dissociated from motor selection in monkeys [71].

The role of oscillatory activity and neuromodulation in TD attention

It has recently been suggested that synchronous activity (in the gamma range, 50–80 Hz) between cortical regions might serve as the basis for attentional facilitation and cortical computations [84]. In this proposal, neuronal populations representing inputs and decision centers all consist of rhythmically active neural ensembles with distinct excitatory and inhibitory phases. Inhibitory interneurons in each ensemble rhythmically inhibit excitatory pyramidal neurons, thereby establishing a

Computational modeling

Physiological studies have guided several theoretical and computational models of attention. Building on the influential feature integration theory [2], guided search theory hypothesizes that massively parallel pre-attentive processes can be guided by TD biasing for features and locations [92]. This theory brings TD elements to a basic BU model of attention [93], which computes individual features at different scales and then combines these features to form a saliency map. A unifying

Conclusion

Attention modulates sensory signals early in the process, exerting its influence on the SC and the thalamus before further modulating signals in cortex. The cumulative effects of this modulation based on both TD and BU influences might be represented by a priority map over visual space. Although there is some debate about the exact locus of the priority map, it is clear that the LIP, FEF and SC exhibit properties that are compatible with the existence of a spatial map encoding behavioral

Acknowledgements

This work was supported by the Defense Advanced Research Projects Agency (government contract no. HR0011-10-C-0034), the National Science Foundation (CRCNS grant number BCS-0827764), General Motors Corporation, and the Army Research Office (grant no. W911NF-08-1-0360). The authors affirm that the views expressed herein are solely their own, and do not represent the views of the United States government or any agency thereof. We would also like to thank Robert Desimone, Jack Gallant, Jacqueline

Glossary

BU influence
influence on the nervous system due to extrinsic properties of the stimuli.
Conjunction search
search task in which a subject is required to find a target item among several distractors, and the target is defined by a unique conjunction of features. In this type of search task, locating the target is more difficult because distractors share some of the features of the target and thus the target does not obviously stand or pop out.
Covert attention
attention paid to a subset of the

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