The attentive homunculus: now you see it, now you don't

The nature of the neural system that directs our attention toward selective items in the extrapersonal world is a longstanding and interesting puzzle. The ability to image the human brain at work non-invasively using positron-emission tomography or functional magnetic resonance has provided the means to investigate this issue. In this article, I review the contributions of brain imaging toward the characterization of attentional control in the human brain. The majority of experiments to date have investigated visual spatial orienting. A consistent pattern of brain areas has been revealed, comprising most notably the posterior parietal cortex around the intraparietal sulcus and frontal regions including the frontal eye fields. The brain areas implicated in the control of visual spatial attention were noted to resemble those involved in the control of eye movements, and direct experimental comparisons supported a tight link between the two systems. The findings suggested a sensible view of the attentional 'homunculus' as a distributed neural system related to the control of eye movements. Eye movements form perhaps the most basic orienting response, and can be shifted rapidly and efficiently based on multiple frames of reference. Some attention experiments using objects and features instead of spatial locations as the target of selection also obtained similar patterns of parietal-frontal activations, rendering further support to this view of the attentional control system. Some recent experiments, however, have cautioned against a premature conclusion regarding the ubiquity of the attentional control system revealed by studies of visual spatial attention. Different parietal and frontal regions become engaged when attention is shifted along non-spatial dimensions, such as when attention is directed toward a particular motor act or toward a specific point in time. In these cases, the neural system resembles those involved in the control of limb movements. The attentional homunculus thus begins to dissolve. The alternative view suggested is that attentional control may be a property of specialized parietal-frontal systems that transform perception into action. Future studies will be needed to validate this view of attention, or to provide a more mature understanding of its true nature.