A biased view of attention.

At any moment, the brain is inundated with data about the sensory environment, yet we are perfectly able to focus on particular aspects of this torrent of information. In the case of vision, some selection is carried out by low-level visual mechanisms, but this stereotyped processing cannot provide the flexibility that complex organisms need to adapt to their ever-changing environment. Processing resources are limited and therefore must be dynamically allocated to deal with the task at hand. This is a job for attention.Beyond our subjective impressions, attention can be demonstrated to improve performance in many behavioral tasks (Posner 1980xPosner, M. Quart. J. Exp. Psych. 1980; 32: 3–25Crossref | PubMedSee all ReferencesPosner 1980). For example, cuing a subject to attend to a particular location enhances the ability to discriminate or react to a stimulus that appears later at that location but not at distant, uncued locations. This suggests that attention primes or biases the visual system in a spatially specific manner, changing the baseline vigilance. In this issue of NeuronKastner et al. 1999xKastner, S., Pinsk, M., De Weerd, P., Desimone, R., and Ungerleider, L. Neuron. 1999; 22: 751–761Abstract | Full Text | Full Text PDF | PubMed | Scopus (946)See all ReferencesKastner et al. 1999 offer an intriguing glimpse into the neuronal framework that might underlie this biasing property of attention. Using functional magnetic resonance imaging (fMRI) in human subjects, the authors observed spatially specific increases in the activity of visual cortex as attention is shifted to the particular location at which a visual stimulus will be presented, even before the stimulus actually becomes visible.The past several decades have seen an explosion of work on the neuronal basis of attention (Maunsell 1995xMaunsell, J. Science. 1995; 270: 764–769Crossref | PubMedSee all ReferencesMaunsell 1995). Most studies involve awake, behaving macaque monkeys trained to direct their attention to different locations on a stimulus screen. The experiments are usually designed to keep the visual stimulation to the retina constant, so that differences in neuronal activity can be specifically attributed to attention. For example, two or more stimuli may be presented at the same locations on every trial but the animal cued to attend to only one of them at a time. By training the animals to hold their gaze on a fixation point while they direct their attention to different locations, the focus of attention varies while the physical visual stimulation remains the same. The general finding is that the visual response of a neuron is larger when the animal is attending the location of that cell’s receptive field, versus attending elsewhere. The neural response is further enhanced when the distracting stimuli are placed closer to the attended stimuli, suggesting that attention may arbitrate a competition among nearby visual stimuli. This might allow neurons in later stages of visual processing to select among multiple visual stimuli that could fit in their large receptive fields (Desimone and Duncan 1995xDesimone, R. and Duncan, J. Annu. Rev. Neurosci. 1995; 18: 193–222Crossref | PubMedSee all ReferencesDesimone and Duncan 1995).Recently, noninvasive functional imaging techniques, such as fMRI and positron emission tomography (PET), have shown that visual responses in human cortex are likewise enhanced for attended stimuli (for a recent discussion, see Somers et al. 1999xSomers, D., Dale, A., Seiffert, A., and Tootell, R. Proc. Natl. Acad. Sci. USA. 1999; 96: 1663–1668Crossref | PubMed | Scopus (446)See all ReferencesSomers et al. 1999). In the fMRI study of Kastner et al. 1998xKastner, S., DeWeerd, P., Desimone, R., and Ungerleider, L.G. Science. 1998; 282: 108–111Crossref | PubMed | Scopus (605)See all ReferencesKastner et al. 1998, fixating subjects were cued to direct their attention to the upper right visual quadrant, to count the occurrences of a particular visual stimulus in a sequence of stimuli flashed at that location (attend condition). On alternate sequences, the subjects maintained fixation but ignored the flashed stimuli (unattend condition). As in fMRI studies from a number of groups, responses to the stimuli were elevated in extrastriate cortical areas in the attend condition compared to the unattend condition, and the enhancements were specific to the regions that had been activated by the unattend condition. Here, Kastner et al. go further by showing that attention enhanced cortical activity even before the stimuli were presented: rather than beginning the stimulus presentation immediately following the cue to attend to the upper right quadrant, the authors waited 11 s before beginning the stimulus sequence. During this time, the subjects could expect the stimuli to occur at the cued location, although no stimulus was actually visible. This is exactly when one might expect the priming effect of attention to be active at full force. During this expectation period, several cortical areas became more active in the attend condition compared to the equivalent period before stimulus presentation in the unattend condition—as if the baseline activity had increased. Like the enhancement of visual responses, the increase in baseline activity was retinotopically restricted to regions that were activated by the stimuli themselves.This is a remarkable finding, in that it seems to provide a neuronal correlate for the covert priming effect of attention. Previous studies in both monkeys and humans had focused on the modulation of visual responses with attention; while there are some reports in the monkey that attention can enhance baseline firing rates of single neurons, these effects are at best slight or inconsistent. The large baseline effects observed by Kastner et al. could be explained if attention provides a subthreshold increase in cortical excitability. Modulation of this sort would have little or no effect on firing rates but might still impose a metabolic burden that should generate an fMRI signal. If so, then fMRI experiments can provide information about attention that might be overlooked with single unit recording.Several issues raised by the Kastner paper could be addressed in more detail. One concern is that the increased activity during the expectation period may have been due to nonspecific “arousal” as the subjects prepared for the imminent peripheral attention task. This concern is somewhat ameliorated by the fact that the expectation effects were retinotopically confined to the representation of the upper right visual quadrant. It is also partly controlled for by the demonstration that no such increases were observed before a different visual attention task using stimuli presented at the fovea, although it was not specified whether subjects were cued in the same way before stimulus presentation in the foveal task. However, it may be difficult to compare foveal and peripheral attention tasks directly. A further concern is that the upper right quadrant was the only part of visual space that was stimulated in the experiment. An experiment in which the same peripheral attention task is also performed in a different visual quadrant, say the upper left, while observing cortical activity in the representation of the upper right quadrant, would eliminate the possibility that a nonspecific increase in activity triggered by the cue might especially involve the most recently activated regions, which may have higher metabolic demands.These concerns notwithstanding, the results raise many fascinating questions. First, what is the source and mechanism of the baseline bias? One possibility raised in the paper is that the bias signal may come from more anterior areas such as the superior parietal lobule and frontal and supplementary eye fields, which are reciprocally connected to some posterior areas. Unlike the posterior visual areas, these areas all showed baseline increases in the attend condition that did not increase further upon visual stimulation, as if providing a “pure” bias signal. Another intriguing question is the mechanism by which the bias amplifies responses to subsequent visual input. A recent result in the monkey that may address this is that attention linearly scales the strength of visual responses of single neurons (MacAdams and Maunsell 1999xMacAdams, C. and Maunsell, J. J. Neurosci. 1999; 19: 431–441PubMedSee all ReferencesMacAdams and Maunsell 1999). The baseline effect observed by Kastner et al. might then reflect a modulatory influence that acts to scale feedforward sensory input. Given this view, it would be extremely useful if the subthreshold activity of single neurons could be assessed during attentional modulation in single cell physiological studies. Finally, these findings beg comparison to results from many other experiments that report neuronal activity in the absence of visual input. These “extraretinal” signals are typically interpreted in the context of the particular behavioral task by which they are revealed, ranging from mental imagery, to working memory, to motor preparation. Perhaps these seemingly different signals share a common cellular mechanism, if not a common source. Thus, the search for the mechanisms of attention may highlight a lot more than we might expect at first glance.