Neural mechanisms behind shifts of attention

Introduction
The environment around us is full of various objects, features and scenes that compete for our attention. Unfortunately the human mind is limited in its ability to process information, and simultaneous processing cannot occur without a substantial cost (Gazzaniga et al., 2002). Therefore, shifting of attention is necessary because it allows us to redirect attention to aspects of the environment we want to focus on, and subsequently process. Research has shown that when an object or area is attended, processing operates more efficiently (Posner, 1980; Gazzaniga et al., 2002). Additionally, we are limited by the size of our visual field. With multiple objects in a scene, only some may show up in our field of vision at one time. Therefore, the eyes, along with one’s attention must constantly be moved and, in a sense, refocused in order to process multiple stimuli. It is this practice of refocusing one’s attention which involves an attentional shift.

Defining shifts of attention
According to Webster’s Dictionary a ‘shift’ is defined as either a transfer to another place, or a change of locations or positions. While ‘attention’ is defined by Webster's Dictionary as the pointing of the mind to either an item or an idea (Morehead et al., 1981). William James provided one of the first descriptions of attention, stating, “It is the taking possession of the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought. Focalization, concentration, of consciousness are of its essence. It implies withdrawal from some things in order to deal effectively with others...” (James, 1890) As attention is a broad concept, it can be broken down into different types. With regards to shifting attention, what we are really interested in is the concept of selective or focused attention, in which the mind is processing one stimulus at a time (Eysenck & Keane, 2005). These shifts of attention can therefore help facilitate the processing of multiple stimuli.

The Spotlight Theory
In attention research, one prominent theory attempting to explain how visual attention is shifted is the moving-spotlight theory. The primary idea being that attention is like a movable spotlight that is directed towards intended targets, focusing on each target in a serial manner. When information is illuminated by the spotlight, hence attended, processing proceeds in a more efficient manner. However, when a shift of spatial attention occurs, the spotlight is, in effect, turned off while attention shifts to the next attended location (Sperling & Weichselgartner, 1995; LaBerge et al., 1997).

Three stages of attention orienting
Another influential idea came from Posner and Petersen in 1990, breaking orienting of attention into three distinct stages. The concept is that in order for a person to reorient to a new location, they first would have to disengage, or take attention away from where it is currently focusing. Next, the physical shifting of one’s attention would occur from one location to another. And finally, attention would be engaged, or focused onto the new location (Eysenck & Keane, 2005). This review attempts to look at the research regarding neural correlates of these physical shifts of attention, specifically focusing on the areas of covert and overt attention, as well as, voluntary and automatic attention shifts. Research often disagrees about the amount of overlap in the neural systems for these different types of attention, and therefore research supporting both views is discussed below.

Overt vs. Covert Attention
Changes in spatial attention can occur with the eyes moving, overtly, or with the eyes remaining fixated, covertly. Within the human eye only a small part, the fovea, is able to bring objects into sharp focus. However, it is this high visual acuity that is needed to perform actions such as reading words or recognizing facial features, for example. Therefore, the eyes must continually move in order to direct the fovea to the desired goal. Prior to an overt eye movement, where the eyes move to a target location, covert attention shifts to this location (Hoffman & Subramaniam, 1995; Kowler et al., 1995; Deubel & Schneider, 1996 Peterson, Kramer, & Irwin, 2004). However, it is important to keep in mind that attention is also able to shift covertly to objects, locations, or even thoughts while the eyes remain fixated. For example, when a person is driving and keeping their eyes on the road, but then, even though their eyes don’t move, their attention shifts from the road to thinking about what they need to get at the grocery store. The eyes may remain focused on the previous object attended to, yet attention has shifted (Hoffman, 1998).

Patient studies and attention shifts
Some of the first research into the neurology behind attention shifts came from examining brain damaged patients. First, Posner et al., studied persons affected by progressive supranuclear palsy, a condition wherein it is difficult to exert eye movements voluntarily, particularly vertical movements. Patients were found to have damage present in the mid-brain area and associated cortical areas. Although patients were not able to move their eyes, they were still able to shift attention covertly. However, there was a slowing of the process of shifting attention in these patients, suggesting that the mid-brain and cortical areas must be associated with covert attention shifts. Additionally, previous research has shown support for covert attention shifts being associated with activity in the parietal lobe. On the other hand, research seems to indicate differences in brain areas activated for overt attention shifts, as compared to covert shifts. Previous evidence has shown that the superior colliculus is associated with eye movements, or overt attention shifts  (Posner et al., 1982). Additionally, the medial cerebellum has shown activation only during eye movements (Corbetta et al., 1998).

Neural overlap for overt and covert attention
Although, after reviewing Posner’s research, it may seem logical to conclude that covert and overt attention shifts utilize different neural mechanisms, other more recent studies have shown more overlap than not. Multiple studies have shown activity evident in the frontal cortex, concentrating in the precentral sulcus, the parietal cortex, specifically in the intraparietal sulcus, and in the lateral occipital cortex for both overt and covert attention shifts (Beauchamp et al., 2001). This is in support of the premotor theory of attention. While these studies may agree on the areas, they are not always in agreement on whether an overt or covert attentional shift causes more activation. Utilizing functional magnetic resonance imaging (fMRI) technology, Corbetta et al., found that overt and covert attention shift tasks showed activation within the same areas, namely, the frontal, parietal and temporal lobes. Additionally, this study reported that covert shifts of attention showed greater activity levels than in the overt attention condition. However, it is important to note that different tasks were used for the covert versus the overt condition. One task involved a probe being flashed to the subject’s fovea, while another task showed the probe in the participant’s peripheral vision, making it questionable whether these results can be directly compared (Corbetta et al., 1998). Nobre et al also sought to determine whether covert and overt attention shifts revealed activation in the same brain areas. Once again fMRI technology was utilized, as well as, two separate tasks, one for covert attention and one for overt attention. Results showed overlap in activated areas for overt and covert attention shifts, mainly in the parietal and frontal lobes. However, one area was shown to be specific to covert attention, which was the right dorsolateral cortex; typically associated with voluntary attention shifts and working memory. One should question whether this additional activation has to do with the selected task for the covert condition, or rather if it is specific to a covert shift of attention (Nobre et al., 2000).

Beauchamp et al. more recently attempted to reproduce these same results by performing a study utilizing the same task for both conditions, as well as, across multiple shift rates. Results were in agreement that covert and overt attentional shifts engage the same neural mechanisms. However, this study differed in that overt shifts of attention showed greater activation in these neural areas, and this occurred even at multiple shift rates. Once again, the neural regions implicated in this study included the intraparietal sulcus, the precentral sulcus, and the lateral occipital cortex. This larger activation evident with overt attention shifts was attributed to the added involvement of eye movements (Beauchamp et al., 2001).

Voluntary vs. Automatic Attention
Attention can be directed either voluntarily, also referred to as endogenous control, or automatically, which is also called  exogenous or reflexive attention. While endogenous control involves one choosing of their own volition to direct their attention, exogenous control occurs when an external object or event, for example, a bee flying by, grabs attention away from the book one is reading, and attracts it involuntarily. The neural mechanisms in the brain have been shown to produce differt patterns of activity for endogenous and exogenous attention (Gazzaniga, et al., 2002).

Separate neural mechanisms
Corbetta and Shulman, who are proponents of the belief that separate neural systems exist for endogenous and exogenous control, conducted a meta-analysis of multiple studies showing brain activation due to either of the two attentional processes. Specifically, the dorsal posterior parietal and frontal cortex region are mainly implicated with voluntary attention, while activity is transiently shown in the occipital region. The endogenous mechanisms are thought to integrate previous knowledge, expectations and goals to voluntarily decide where to shift attention. On the other hand, neural areas involved in reflexive attention are believed to have the purpose of focusing attention on events or objects that stand out in the environment. The temporoparietal cortex and ventral frontal cortex region, particularly in the right brain hemisphere, have shown involvement with reflexive attention (Corbetta and Shulman, 2002). Even though separate regions are thought to be in existence for these two attentional processes, the question still remains on whether these regions interact with one another, indicating more research on this point is still needed (Eysenck & Keane, 2005).

Neural overlap for voluntary and reflexive attention
There appears to be agreement that multiple areas of the brain are involved in shifts of attention, however research is not quite as conclusive regarding the amount of overlap evident with voluntary versus reflexive attention. Rosen et al.’s study found a fair amount of overlap between endogenous and exogenous shifts of attention. Both conditions showed activation in the dorsal and parietal premotor areas. However, the voluntary condition also showed activation in the right dorsolateral prefrontal cortex, which did not appear in the reflexive condition. As this area has been shown to be associated with working memory, it may indicate that working memory is engaged voluntarily. The subcortical global pallidus region was also activated only in the voluntary condition. Additionally, the activation shown in the temporoparietal junction [TPJ] was slightly different in both conditions, with the endogenous condition showing more spreading to the lateral, anterior and superior regions. Although these differences did exist, overall there was a lot of overlap demonstrated for voluntary and reflexive shifts of attention. Specifically both showed activations in the dorsal premotor region, the frontal eye field area, and the superior parietal cortex (SPC), although, the SPC exhibited greater activation in the endogenous condition (Rosen et al., 1999).

Conclusion
In conclusion, many neural mechanisms are involved in shifts of attention. While the type of attentional shift can dictate different brain regions becoming active, there is a lot of overlap seen. For instance, with regards to covert and overt attentional shifts, much of the research seems to point to a shared neural network. Although common brain areas may be activated, they do tend to differ in terms of the amount of activation. For endogenous and exogenous attention, research was less clear about the amount of overlap in the neural areas. Voluntary and reflexive attentional shifts may have some overlap, but other studies do not support this. Additionally, even if the same neural areas are being utilized, one should question whether the same processes are being engaged within the same region. Further research, as neuroscience methods are able to gather more detailed and precise information may shed light on this. Finally, research can be reviewed in other areas of attention to give more insight into the shifting of attention. This review concentrated on visual shifts of attention, but it has also been shown that we can shift attention to an auditory target and selectively attend to this stimulus (Eysenck & Keane, 2005). In the future, it might be interesting to look at attention shifts due to different modalities to ascertain whether similar neural mechanisms are utilized as are with visual shifts of attention.