Top-down control of visual attention
Introduction
Selective attention is the basic cognitive faculty that allows us to filter out irrelevant sensory information in favor of the relevant. Disorders of attention are frequently occurring among the symptoms of many neuropsychiatric disorders [33], most notably attention-deficit hyperactivity disorder (ADHD), which afflicts more than 4% of the population [34]. To date, the neural circuits and neural computations underlying normal and abnormal attention are only poorly understood. However, recent experimental work suggests that an understanding of how networks of neurons control the selection of relevant sensory input might be at hand. Much of what is known so far about the neural basis of attention comes from studies of the primate visual system, particularly that of the macaque monkey, which has proven to be a highly valuable model system. In recent years, neurophysiological studies have not only provided a more rigorous description of the correlates and signatures of attention in neural activity, but they have begun identifying the sources of attentional influences on neural activity and perception.The deployment of attention to a particular location in space (spatial attention) or to a particular feature or object (feature-based or object-based attention) can occur either by virtue of a stimulus’ physical salience (exogenous, involuntary or bottom-up attention) or according to internal, behavioral goals (endogenous, voluntary or top-down attention). Most of the studies over the past few years that we discuss, particularly those aimed at identifying neural circuits controlling attention, have focused primarily on top-down, spatial attention. Although it is clear that feature-based attention (e.g. [23, 35]) and bottom-up attention (e.g. [12•, 36]) both modulate neuronal activity within the visual system, the neurophysiological effects of these forms of attention are less well understood.
Section snippets
Signatures of attention
Attention provides a means of dynamically selecting specific neural representations for further processing, and this filtering involves amplifying behaviorally relevant information at the expense of other information. The objective of attention can be viewed as increasing the signal-to-noise ratio (SNR) of the readout from subpopulations of neurons encoding the selected representation. In theory, this can be accomplished in a number of ways, including strengthening selected signals, improving
Sources of attention
Experimental evidence of a role of prefrontal and parietal cortex in the control of attention, and particularly of brain structures involved in oculomotor or gaze functions, dates back to at least the late 19th century [45]. Only in recent years, however, has the relationship between the neural control of gaze and attention been tested directly. Several studies have employed electrical microstimulation to probe the role of saccade-related structures in the deployment of spatial attention. Moore
Circuits of attention
Although recent evidence has begun to identify sources of top-down effects of attention, the particular circuits involved in generating its signatures within visual cortex remain to be identified. The set of known connections between possible sources of attentional control (i.e. the FEF, LIP, and the SC) and visual cortical areas are obvious candidates. Direct corticocortical projections exist from both the FEF and LIP to most extrastriate areas in which signatures of attention have been
The role of neuromodulators
Although the involvement of neuromodulators such as acetylcholine (Ach), noradrenaline (NA), and dopamine (DA) in arousal and attention is widely accepted, it remains to be established how that involvement intersects with known signatures of attention in visual cortex. A recent study however found evidence of a cholinergic contribution to attentional modulation within macaque V1 through muscarinic receptors [5•]. The role of Ach in attention may either be achieved via gating of information
Spatial attention and spatial working memory
Top-down attention is often directed according to information held in working memory [68, 69, 70]. Many psychophysical studies have demonstrated a reciprocal relationship between spatial attention, spatial working memory, and oculomotor control, suggesting that the maintenance of visual spatial information may be achieved via some combination of attention-based rehearsal and motor preparation [71, 72, 73, 74]. Other studies in humans show enhanced processing of visual targets at locations held
Conclusions
Neurophysiological studies have made significant progress both in describing how top-down visual attention alters signals within the visual system as well as in beginning to identifying their causal basis. Nevertheless, our understanding of the neural circuitry of attention remains fairly rudimentary. Evidence to date falls far short of allowing one to identify the specific neurons, synaptic operations, or local and distributed neural computations that are both necessary and sufficient to
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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