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Attentional Networks in the Parietal Cortex
Attentional Networks in the Parietal Cortex
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Attentional Networks in the Parietal Cortex G H Patel, B J He, and M Corbetta, Washington University School of Medicine, St. Louis, MO, USA ã 2009 Elsevier Ltd. All rights reserved.
Introduction The brain is continuously flooded with information from different senses: vision, audition, touch, smell, and taste. As the inflow of sensory information is much greater than what the brain can process at any given time, one of the fundamental interests of neuroscience is to understand which brain mechanisms are responsible for the selection of those few bits of information that are relevant to the ongoing goals of an individual, and how irrelevant information is filtered out. Attended objects tend to be perceived and remembered much better than unattended objects are, and only objects that are attended become the target of motor plans, such as when we look at and reach for an apple. Accordingly, attention is defined as the ensemble of psychological and neural operations that mediate selection of sensory stimuli and link them to response and memory systems. The parietal lobe, from the Latin paries, or ‘walls of a house,’ is the part of the brain that sits between the occipital, temporal, and frontal lobes, and that includes the lateral superior part of each hemisphere. The parietal lobe is situated between sensory (visual, tactile, and auditory) areas and contains cells that respond predominantly to behaviorally relevant stimuli. The parietal lobe is also active when individuals prepare to look or move toward a stimulus, and is heavily connected with the frontal lobe, in which the actions are planned. The parietal lobe of the brain is therefore well suited to perform operations that are neither strictly sensory nor motor, but rather operations that integrate sensory and motor information. Because of the integrative nature of the parietal lobe, the functions of the cortical areas contained within it are complex and diverse, and damage to the parietal lobe often results in multifaceted deficits. In this article we first describe the anatomical organization of the parietal lobe; next, we turn to what we know about the functional organization of parietal cortex, and finally, we consider some of the behavioral deficits that arise after it is damaged.
Organization and Connectivity The parietal lobe is bordered on the posterior and ventral sides by visual and auditory cortex, respectively, and the anterior portion of the parietal lobe is
occupied by somatosensory cortex. Anterior to the parietal lobe is the frontal lobe, much of which is devoted to the planning and execution of movements. The parietal lobe is divided into smaller parts based on gross anatomy. The most prominent anatomical feature of the parietal lobe is the intraparietal sulcus (IPS), which runs anterior–posteriorly along the lateral aspect of the parietal lobe. The IPS divides the parietal lobe into two lobules: the superior parietal lobule (SPL), which encompasses the lateral aspect of the parietal lobe dorsal to the IPS as well as the medial wall, and the inferior parietal lobule (IPL), which encompasses all of the parietal lobe ventral to the IPS. The part of the parietal lobe on the medial wall is also often called the precuneus. Using histological techniques, investigators have subdivided the parietal lobe in several ways. Perhaps one of the best known schemes for subdividing parietal cortex was proposed by Brodmann in 1909. In this scheme, the human parietal cortex is subdivided into seven areas: areas 1–3, which comprise the anterior edge of the parietal lobe and cover somatosensory cortex; area 5, which is immediately posterior to area 2 and covers the anterior part of the SPL; area 7, which is posterior to area 5 and covers much of the lateral and medial SPL and some of the IPL; and areas 39 and 40, which cover much of the IPL (see Figure 1(a)). Beyond these coarse divisions, however, not much was known for many years about the anatomical organization of parietal cortex, in part because invasive techniques necessary to trace connections and study the function of this part of the brain in humans were not available. As a result, most of the detailed information that we have on the parietal lobe’s organization and on other parts of the human brain comes from anatomical and physiological studies of nonhuman primates, especially macaques, the brains of which share many of the same sensory and motor functions of the human brain. The gross and histological organization of macaque parietal lobe is similar to that of the human parietal lobe in many ways: an IPS separates the parietal lobe into an SPL and IPL, somatosensory cortex makes up the anterior edge of the parietal lobe, and visual areas lie along the posterior edge. Areas 1, 2, 3, 5, and 7 are also present in macaque; however, the relative position of areas 5 and 7 is more ventral, given that areas 39 and 40, which occupy the ventral part of the human IPL, are not present in the macaque (see Figure 1(b)). Despite these potential differences, the macaque continues to serve as a useful model of how human parietal areas may be involved in attention.
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Figure 1 (a) Human Brodmann areas 1–3, 5, 7, 39, and 40, and the intraparietal sulcus (IPS). (b) Macaque Brodmann areas. (c) Cortical damage underlying neglect. (d) Areas in and around the macaque IPS (PO, parietal-occipital; MIP, medial intraparietal; PIP, posterior intraparietal; LOP, lateral occipitoparietal zone; VIP, ventral intraparietal; DP, dorsal prelunate; AIP, anterior intraparietal; 5, area 5; 7a, area 7a). Adapted from Lewis JW and Van Essen DC (2000) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. Journal of Comparative Neurology 428: 79–111.
In the 1970s, the advent of anatomical methods to trace connections between areas allowed for the partition of posterior parietal cortex into multiple areas based on their profile of feed-forward and feedback connections. Feed-forward connections refer to connections from lower to higher levels of a sensory hierarchy of cortical areas, whereas feedback connections refer to connections from higher to lower levels. There are several proposed schemes to divide the parietal cortex. Along the IPS, one common scheme divides the cortex into ten areas: dorsal prelunate (DP), posterior intraparietal (PIP), parietal-occipital (PO), the lateral occipitoparietal zone (LOP), medial intraparietal (MIP), ventral intraparietal (VIP; divided into medial and lateral), lateral intraparietal (LIP; divided into dorsal and ventral), anterior intraparietal (AIP), area 5, and area 7a (see Figure 1(d)). Other similar schemes have also been proposed. Tracer studies have shown that these areas receive input from other brain structures involved in the processing of vision, audition, and sensation, and may send output to the same sensory areas and/or to various motor and motorplanning areas. The IPS areas residing more posteriorly and laterally receive most of their input from visual areas and send output to oculomotor structures, whereas the more medial and anterior areas also receive input from somatosensory areas and send output to hand and arm motor areas. For an area to be involved in the selective operations of visual spatial attention, it is likely to be
connected to the visual areas responsible for the processing of incoming stimuli. It is also likely to be connected to areas involved in the planning and execution of saccades, since after the selection of a stimulus of interest, a saccade is often made to bring the stimulus into the fovea for further scrutiny. Area LIP in the macaque fits this description. It occupies the caudal half of the lateral bank of the IPS, and is demarcated histologically from surrounding parietal areas by increased myelination of layers 3–5. This area receives feed-forward connections from and sends feedback connections to many extrastriate visual areas, including areas V4, V3a, and middle temporal complex (MT), an area known to be involved in processing visual motion. LIP is also heavily interconnected with oculomotor structures, such as the superior colliculus in the midbrain, the pulvinar in the thalamus, and the frontal eye fields (FEFs) in prefrontal cortex. Area 7a has a profile of connections with cortical areas similar to that of LIP, except rather than FEF, it is connected with area 46 in prefrontal cortex. Area 46 is an area known to be involved in spatial working memory, implying that 7a may also play a role in working memory and attention. Other posterior parietal areas, such as DP and PO, connect mainly with extrastriate areas and more anterior IPS areas, such as LIP, indicating that they play a role in relaying information from visual cortex to the higher level planning areas in IPS.
Attentional Networks in the Parietal Cortex
In general, the many anatomical studies of parietal cortex over the past several decades have shown that it appears to be divided into many areas, each of which appears to play a role in translating sensory information into motor plans. But what exactly this role entailed remained a mystery until the technology to study these areas in vivo was developed, first in macaques and then later in humans.
Function In 1975 Mountcastle and colleagues first reported on electrophysiological recordings of macaque parietal cortex neurons while the monkey performed various tasks. They found that neurons in the IPS ‘‘appear[ed] to direct visual attention to objects of interest and motivational power, and to issue commands for maintaining directed fixation of the object when it [was] stationary, and to track it if it mov[ed].’’ In the decades since these early experiments, electrophysiological recordings of parietal cortex neural activity have determined that the SPL and IPL are subdivided into many smaller functional areas that appear to roughly correspond with the subdivisions determined by histological techniques. Each of these areas appears to extract the spatial information from one or more sensory inputs, and then play some role in transforming that information into a general movement plan in the same spatial coordinates. Because of its involvement in spatial processing, the parietal cortex is said to be part of the ‘where’ pathway (as opposed to the ventral ‘what’ pathway, which appears to be involved in processing the identity of a stimulus regardless of spatial location). For instance, the area LIP is involved in the planning of upcoming saccadic eye movements. The neurons in this area respond transiently to visual stimuli presented within a specific part of the visual field, which is known as a receptive field. Moreover, if a saccade is to be performed to that stimulus at some point in the future, the neurons continue to fire until the saccade has been executed. In this way, they are said to represent the planned target of the saccade until the action is completed, even if the visual stimulus is no longer in the receptive field. This characteristic is often used to define the boundaries of LIP in electrophysiological recording experiments. LIP neurons have large visual receptive fields that cover on average a quarter of the visual field, and these receptive fields move with the position of gaze (gaze centered). They are also more likely to respond to stimuli in the contralateral visual hemifield than in the ipsilateral, and may contain a coarse but continuous map of the contralateral visual field (otherwise known as being retinotopically organized). LIP neurons, then,
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appear to represent the plan of an upcoming saccadic eye movement in a rough spatial map of the visual environment. LIP neurons will also respond to a visual stimulus that is not the target of a planned saccade, but is otherwise task relevant. For instance, if the monkey is instructed to maintain fixation on a central point, and to indicate with his hand when a visual stimulus in the periphery dims just slightly, the LIP neurons representing the location of this stimulus continue to fire until the task is completed, and this increased level of firing is directly correlated to increased performance of whatever perceptual decision needs to be made at that location. Moreover, chemically deactivating LIP will result in the reduction of the monkey’s ability to discriminate an oddball stimulus from other stimuli (such as a red circle among a field of green circles). It appears, then, that LIP neurons also represent the current locus of visuospatial attention. Are these two purported functions of LIP neurons in conflict, or do they represent two ways of saying the same thing? The answer to this has been the source of a contentious debate. Thus far we have seen that LIP is involved both in covert shifts of attention (marking a location of interest so that processing of objects in that location can be enhanced) and in overt shifts of attention (making a saccade to a location so that it can be studied in more detail). One side of the debate holds that all covert shifts of attention represent potential saccades, and that the enhanced processing at that location is merely a side effect of planning a movement to that location. As evidence for this view, they point to other parietal areas, which appear to play the same planning role for other effectors, such as arm and hand movements. The ‘intentional map,’ then, might be a general principle of what the parietal cortex contributes to a sensorimotor transformation. The other side, however, contends that the LIP is a ‘salience map’ of the visual world, marking locations of interest for any number of systems to use, including the visual attention and oculomotor system. Part of the evidence for this view is that LIP neurons track the location of salient objects independently of stored oculomotor plans. While the differences between these two sides may seem minute, the resolution of this debate will give us insight into both what specific calculations parietal cortex neurons are performing on incoming information and in what terms the brain represents the external world – as a distorted version of reality, skewed toward the most interesting and relevant stimuli, or always in terms of a motor plan for interacting with the world? Other parietal areas in the macaque may also play roles in selective attention, though these areas have
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not been as thoroughly investigated as LIP. Areas caudal to LIP, such as DP, appear to play a role in visuospatial processing, though probably at an earlier stage than LIP (again fitting with their profiles of connections). Area 7a, which covers much of the IPL lateral to LIP, also appears to be involved in visuospatial processing. Like LIP, its neurons have large receptive fields, though it appears to evenly represent both the contralateral and ipsilateral hemifields. The neurons in this area appear to respond to the novel appearance of behaviorally relevant visual stimuli, but not as many of the 7a neurons have presaccadic activity as compared to LIP cells. This may indicate that rather than representing the current focus of attention, 7a neurons may be involved in detecting novel but potentially relevant stimuli, a counterpart of sorts to LIP. How other macaque parietal areas are involved in spatial attention is less clear, as they have generally been studied under the rubric of motor planning. Another important organizing principle for thinking about parietal cortex is to consider how space is coded in this region of the brain. There is evidence that parietal cortex subregions may be specialized for coding spatial location away from the body (or extrapersonal space) or near the body (or peripersonal space). This wealth of information about monkey’s parietal cortex until recently did not have a counterpart in the human work, because studies were limited to clinical observations (see later). This state of affairs changed in the late 1980s with the advent of positron emission tomography (PET), and then again in the 1990s with the advent of functional magnetic resonance imaging (fMRI). These neuroimaging technologies allowed, for the first time, in vivo studies of neural activity with sufficient spatial and temporal resolution to discern areas of the brain that were active in different tasks. Early PET studies confirmed that in humans the parietal lobe is also part of the dorsal ‘where’ pathway and is involved in the control of both spatial attention and eye movements. Several subsequent fMRI studies have also shown that, like in the macaque, the parietal region activated during covert shifts of attention largely overlaps with the region activated during saccades. This region includes much of the cortex in and around the IPS. Parts of this region are also activated during nonspatial shifts of attention, such as changing the focus of attention from the direction of moving dots to the color of the moving dots. Because of this profile of activity, the region along the human IPS has been thought of as generally homologous to the macaque IPS. However, due to the combination of relatively poor spatial resolution of fMRI and the high degree of variability in the location of sulci and gyri among
human individuals, it has been difficult to subdivide this region into functional areas as has been done in the macaque. Two foci of neural activity are consistently activated in different tasks requiring shifting or maintenance of attention. The first is in the SPL, on the dorsal–medial bank of the IPS. Because it is thought to be homologous to the macaque LIP, it is sometimes called human LIP (hLIP). Like macaque LIP, hLIP appears to be gaze centered in its spatial reference frame, responds more strongly to stimuli in the contralateral visual hemifield than in the ipsilateral, and appears to be loosely retinotopically organized. This area is activated if there is an attention shift to a peripheral location, and activity is sustained in this area if either attention remains focused on, or a saccade is being planned to, the peripheral location. Activity in this area seems to track both the locus of visuospatial attention and the target of an upcoming eye movement, extending the debate about parietal function to the human parietal cortex. While much of the functional profile of hLIP appears to be broadly similar to that of macaque LIP, the lack of direct comparisons of histological data or neural activity during tasks requiring shifts of attention prevents a more thorough assessment of the homology of these areas. Areas posterior to hLIP are also often activated in tasks requiring shifts of spatial attention. One of the most prominent is in the fundus of the caudal section of the IPS, and is variously termed ventral IPS (vIPS) or V7. This area is preferentially activated by attending to the contralateral hemifield, but appears to be more visual in nature than hLIP. V7 most likely represents an earlier stage of the ‘where’ pathway that probably relays visual information to hLIP, and is a potential homolog to one of the posterior parietal areas in the macaque. While the aforementioned areas in the human SPL are activated during voluntary and involuntary shifts of attention, the IPL appears to play a different role in attention. Regions in the IPL are only activated in response to the appearance of a salient, behaviorally relevant object, and even more so if attention has to be reoriented from another location (known as stimulus-driven reorienting of attention). Moreover, while activity in the SPL areas is increased during sustained covert shifts of attention, activity in the IPL is suppressed. It has been proposed that these areas play a role in stimulus-driven attention, especially when the focus of attention is captured by a salient and relevant novel stimulus. In macaques, area 7a (on the macaque IPL) is one possible candidate for a homolog to the human IPL. Another important feature of human parietal cortex is that it is anatomically and functionally asymmetrical. Several studies have now shown that
Attentional Networks in the Parietal Cortex
functional regions of the supramarginal and angular gyrus at the temporoparietal junction (TPJ) in humans show hemispheric asymmetries of attention (rightdominant) or verbal memory (left-dominant) tasks. This asymmetry is even more dramatic when one considers the behavioral effects of stroke in the middle cerebral artery (MCA) distribution that feeds the parietal cortex. Whereas left MCA strokes commonly result in aphasia (language deficits), strokes of the right MCA commonly result in a syndrome termed ‘neglect,’ which is a collection of spatial attention– perception–premotor deficits (see Figure 1(c)). An important goal for the future will be to reconcile monkey and human data in a common evolutionary framework that takes into account both commonalities and differences in functional organization. An important technological advance that will help this line of research is the development of fMRI studies in awake-behaving monkeys.
Lesions Damage to the right IPL often results in spatial neglect, a common syndrome following stroke in which patients are biased toward attending to the right side of visual space more than to the left side. Neglect can leave patients unable to perform simple tasks requiring spatial attention, and occurs in about 30% of all stroke-affected individuals. Patients with neglect often act as if part of the left side of their world does not exist. This inattention to the left side can occur in extrapersonal space or about the patient’s own body, and can occur in different reference frames: gaze-centered frame (left with respect to the center of gaze), body-centered frame (left with respect to the midline of the body), or world-centered frame (left with respect to the environment). Less commonly, patients can manifest socalled object-centered neglect, where the left side of an object is ignored, no matter if it is presented in the left or right side of the visual space. For instance, if a page of text with three columns is presented, a patient with body-centered or world-centered neglect will miss the words on the left side of the page, whereas a patient with object-centered neglect will miss the left side of each column or the left side of each word. Functionally, neglect patients may ‘forget’ to shave, groom, or dress the left side of body. They also have major problems with driving a car. Severely affected patients might also display a tonic rotation of the body or eyes toward the right, due to a coexisting motor imbalance. Some of these patients may still be able to detect a stimulus presented alone in the left hemifield, but when presented with stimuli simultaneously to both visual fields, patients tend to
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see only those in the right hemispace. This deficit is referred to as ‘extinction.’ Extinction is often tested by snapping fingers in one or both of the patient’s visual fields and asking the patient to point to which hand they saw or heard snapping. When fingers are snapped simultaneously in both visual fields, neglect patients will inexorably point to the hand in their right visual field. This test is one of the many routine exams in clinical settings to assess the severity of neglect. Other commonly used neuropsychological tests for diagnosis of neglect include line bisection, in which patients with neglect bisect a horizontal line to the right of the true center; a series of cancellation tasks, in which neglect patients commonly miss marking targets on the left side of a paper; clock drawing, in which neglect patients may draw only the right half of a clock; and a baking-tray task, in which neglect patients usually cluster cookies on the right side of a baking tray. In addition to the lack of awareness of the left side of space, neglect patients can also manifest deficits in planning hand or eye movements toward the left side of space. In this type of neglect, patients may not demonstrate a bias in awareness to either visual field, but will be less inclined to reach or look for objects located in the left visual field. This form of neglect is called motor or premotor neglect, or directional hypokinesia, to emphasize its relationship to action. In addition to lateralized (i.e., left worse than right space) deficits, a number of so-called nonlateralized deficits (i.e., similar across left and right visual fields) have also been described, including impairment of spatial working memory, sustained attention, and an overall lower level of alertness. An important focus of current research is to assess the functional effect of different deficits, their importance for final outcome, their recovery over time, and their localization in the brain. Shall we think of neglect as a homogeneous or heterogeneous syndrome? What are the regions more responsible for one or another deficit? We know that spatial neglect can occur as a clinical syndrome for lesions in many parts of the brain, including parietal, temporal, frontal cortex, basal ganglia, thalamus, and in various white-matter tracts. It is still unknown how these different lesions may or may not cause different behavioral profiles of neglect, and how the effect of lesions in the brain relates to the functional organization observed in healthy individuals. An alternative view considers neglect not to be the effect of damage to specific cortical areas, but rather the result of a distributed and combined anatomical– functional dysfunction of large parts of parietal and frontal cortices and their connections. In general, the areas that are damaged in neglect are located ventrally in the brain, including the IPL regions
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specialized for stimulus-driven attention. Conversely, damage to more dorsal IPS and SPL regions does not produce strong neglect; rather, these lesions produce primarily eye- or arm-movement planning problems, which is also consistent with the results of functional imaging studies in healthy volunteers. However, only a few patients with damage restricted to the SPL have been studied. One model of neglect postulates that damage by stroke or trauma to the IPL in the region of the TPJ could give rise to both spatial and nonspatial deficits by interrupting input to the SPL attentional areas from the TPJ. This disruption would then reduce the brain’s ability to detect important sensory events in both visual fields. In addition, this lack of input into ipsilesional dorsal areas may induce a relative interhemispheric imbalance in the dorsal attentional areas that code for spatial locations and eye and arm movements. The imbalance due to the competitive nature of interhemispheric processing will lead to a relative hyperorienting toward right space, with consequent problems of attention and detection in left space. This model of spatial bias based on interhemispheric competition is also supported by a number of animal studies in which neglect has been cured by inactivating homologous parietal regions of the intact hemisphere.
Conclusion Parietal cortex is subdivided into different areas, based on both anatomical and functional criteria; these areas have connections with both sensory processing and motor planning regions of the brain. Some of these areas appear to be involved in the selection and representation of locations and objects of interest in the immediate environment. The spatial information in parietal cortex can then be ‘read out’ by other brain areas, both for the planning of movements and for the enhancement of sensory processing. Attention can be directed to a location or object by a premeditated plan, or by the appearance of a novel stimulus that may require additional processing. Area LIP in the macaque and its putative homolog in the SPL of humans appear to be involved in representing the locations of interest, whereas IPL areas appear to play the role of reorienting attention whenever a novel stimulus enters awareness. Damage to these areas results in the syndrome of neglect, which fundamentally involves a lack of awareness for
spatial information, as well as problems with vigilance and motor planning. See also: Attention and Eye Movements; Attention: Models; Attentional Functions in Learning and Memory; Attentional Mechanisms in Ventral Pathway; Attentional Networks; Decision-Making and Vision; Neglect Syndrome and the Spatial Attention Network; Parietal Cortex and Spatial Attention; Psychophysics of Attention; Visual Attention.
Further Reading Andersen RA and Buneo CA (2002) Intentional maps in posterior parietal cortex. Annual Review of Neuroscience 25: 189–220. Colby CL and Goldberg ME (1999) Space and attention in parietal cortex. Annual Review of Neuroscience 22: 319–349. Corbetta M and Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience 3: 201–215. Desimone R and Duncan J (1995) Neural mechanisms of selective visual attention. Annual Review of Neuroscience 18: 193–222. Egeth HE and Yantis S (1997) Visual attention: Control, representation, and time course. Annual Review of Psychology 48: 269–297. Goldman-Rakic PS (1988) Topography of cognition: Parallel distributed networks in primate association cortex. Annual Review of Neuroscience 11: 137–156. Hillis AE (2006) Neurobiology of unilateral spatial neglect. Neuroscientist 12: 153–163. Husain M and Rorden C (2003) Non-spatially lateralized mechanisms in hemispatial neglect. Nature Reviews Neuroscience 4: 26–36. Kastner S and Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annual Review of Neuroscience 23: 315–341. Lewis JW and Van Essen DC (2000) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipetal complex. Journal of Comparative Neurology 428: 79–111. Avaliable at URL: http://sumsdb.wustl.edu:8081/ sums/directory.do?id=679531. Mesulam MM (1999) Spatial attention and neglect: Parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 354: 1325–1346. Mountcastle VB, Lynch JC, Georgopoulos A, et al. (1975) Posterior parietal association cortex of the monkey: Command function for operations within extrapersonal space. Journal of Neurophysiology 38: 871–908. Orban GA, VanEssen D, and Vanduffel W (2004) Comparative mapping of higher visual areas in monkeys and humans. Trends in Cognitive Science 8: 315–324. Pashler HE (1998) The Psychology of Attention. Cambridge, MA: MIT Press. Posner MI and Petersen SE (1990) The attention system of the human brain. Annual Review of Neuroscience 13: 25–42.
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Attentional Networks in the Parietal Cortex G H Patel, B J He, and M Corbetta, Washington University School of Medicine, St. Louis, MO, USA ã 2009 Elsevier Ltd. All rights reserved.
Introduction The brain is continuously flooded with information from different senses: vision, audition, touch, smell, and taste. As the inflow of sensory information is much greater than what the brain can process at any given time, one of the fundamental interests of neuroscience is to understand which brain mechanisms are responsible for the selection of those few bits of information that are relevant to the ongoing goals of an individual, and how irrelevant information is filtered out. Attended objects tend to be perceived and remembered much better than unattended objects are, and only objects that are attended become the target of motor plans, such as when we look at and reach for an apple. Accordingly, attention is defined as the ensemble of psychological and neural operations that mediate selection of sensory stimuli and link them to response and memory systems. The parietal lobe, from the Latin paries, or ‘walls of a house,’ is the part of the brain that sits between the occipital, temporal, and frontal lobes, and that includes the lateral superior part of each hemisphere. The parietal lobe is situated between sensory (visual, tactile, and auditory) areas and contains cells that respond predominantly to behaviorally relevant stimuli. The parietal lobe is also active when individuals prepare to look or move toward a stimulus, and is heavily connected with the frontal lobe, in which the actions are planned. The parietal lobe of the brain is therefore well suited to perform operations that are neither strictly sensory nor motor, but rather operations that integrate sensory and motor information. Because of the integrative nature of the parietal lobe, the functions of the cortical areas contained within it are complex and diverse, and damage to the parietal lobe often results in multifaceted deficits. In this article we first describe the anatomical organization of the parietal lobe; next, we turn to what we know about the functional organization of parietal cortex, and finally, we consider some of the behavioral deficits that arise after it is damaged.
Organization and Connectivity The parietal lobe is bordered on the posterior and ventral sides by visual and auditory cortex, respectively, and the anterior portion of the parietal lobe is
occupied by somatosensory cortex. Anterior to the parietal lobe is the frontal lobe, much of which is devoted to the planning and execution of movements. The parietal lobe is divided into smaller parts based on gross anatomy. The most prominent anatomical feature of the parietal lobe is the intraparietal sulcus (IPS), which runs anterior–posteriorly along the lateral aspect of the parietal lobe. The IPS divides the parietal lobe into two lobules: the superior parietal lobule (SPL), which encompasses the lateral aspect of the parietal lobe dorsal to the IPS as well as the medial wall, and the inferior parietal lobule (IPL), which encompasses all of the parietal lobe ventral to the IPS. The part of the parietal lobe on the medial wall is also often called the precuneus. Using histological techniques, investigators have subdivided the parietal lobe in several ways. Perhaps one of the best known schemes for subdividing parietal cortex was proposed by Brodmann in 1909. In this scheme, the human parietal cortex is subdivided into seven areas: areas 1–3, which comprise the anterior edge of the parietal lobe and cover somatosensory cortex; area 5, which is immediately posterior to area 2 and covers the anterior part of the SPL; area 7, which is posterior to area 5 and covers much of the lateral and medial SPL and some of the IPL; and areas 39 and 40, which cover much of the IPL (see Figure 1(a)). Beyond these coarse divisions, however, not much was known for many years about the anatomical organization of parietal cortex, in part because invasive techniques necessary to trace connections and study the function of this part of the brain in humans were not available. As a result, most of the detailed information that we have on the parietal lobe’s organization and on other parts of the human brain comes from anatomical and physiological studies of nonhuman primates, especially macaques, the brains of which share many of the same sensory and motor functions of the human brain. The gross and histological organization of macaque parietal lobe is similar to that of the human parietal lobe in many ways: an IPS separates the parietal lobe into an SPL and IPL, somatosensory cortex makes up the anterior edge of the parietal lobe, and visual areas lie along the posterior edge. Areas 1, 2, 3, 5, and 7 are also present in macaque; however, the relative position of areas 5 and 7 is more ventral, given that areas 39 and 40, which occupy the ventral part of the human IPL, are not present in the macaque (see Figure 1(b)). Despite these potential differences, the macaque continues to serve as a useful model of how human parietal areas may be involved in attention.
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Figure 1 (a) Human Brodmann areas 1–3, 5, 7, 39, and 40, and the intraparietal sulcus (IPS). (b) Macaque Brodmann areas. (c) Cortical damage underlying neglect. (d) Areas in and around the macaque IPS (PO, parietal-occipital; MIP, medial intraparietal; PIP, posterior intraparietal; LOP, lateral occipitoparietal zone; VIP, ventral intraparietal; DP, dorsal prelunate; AIP, anterior intraparietal; 5, area 5; 7a, area 7a). Adapted from Lewis JW and Van Essen DC (2000) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. Journal of Comparative Neurology 428: 79–111.
In the 1970s, the advent of anatomical methods to trace connections between areas allowed for the partition of posterior parietal cortex into multiple areas based on their profile of feed-forward and feedback connections. Feed-forward connections refer to connections from lower to higher levels of a sensory hierarchy of cortical areas, whereas feedback connections refer to connections from higher to lower levels. There are several proposed schemes to divide the parietal cortex. Along the IPS, one common scheme divides the cortex into ten areas: dorsal prelunate (DP), posterior intraparietal (PIP), parietal-occipital (PO), the lateral occipitoparietal zone (LOP), medial intraparietal (MIP), ventral intraparietal (VIP; divided into medial and lateral), lateral intraparietal (LIP; divided into dorsal and ventral), anterior intraparietal (AIP), area 5, and area 7a (see Figure 1(d)). Other similar schemes have also been proposed. Tracer studies have shown that these areas receive input from other brain structures involved in the processing of vision, audition, and sensation, and may send output to the same sensory areas and/or to various motor and motorplanning areas. The IPS areas residing more posteriorly and laterally receive most of their input from visual areas and send output to oculomotor structures, whereas the more medial and anterior areas also receive input from somatosensory areas and send output to hand and arm motor areas. For an area to be involved in the selective operations of visual spatial attention, it is likely to be
connected to the visual areas responsible for the processing of incoming stimuli. It is also likely to be connected to areas involved in the planning and execution of saccades, since after the selection of a stimulus of interest, a saccade is often made to bring the stimulus into the fovea for further scrutiny. Area LIP in the macaque fits this description. It occupies the caudal half of the lateral bank of the IPS, and is demarcated histologically from surrounding parietal areas by increased myelination of layers 3–5. This area receives feed-forward connections from and sends feedback connections to many extrastriate visual areas, including areas V4, V3a, and middle temporal complex (MT), an area known to be involved in processing visual motion. LIP is also heavily interconnected with oculomotor structures, such as the superior colliculus in the midbrain, the pulvinar in the thalamus, and the frontal eye fields (FEFs) in prefrontal cortex. Area 7a has a profile of connections with cortical areas similar to that of LIP, except rather than FEF, it is connected with area 46 in prefrontal cortex. Area 46 is an area known to be involved in spatial working memory, implying that 7a may also play a role in working memory and attention. Other posterior parietal areas, such as DP and PO, connect mainly with extrastriate areas and more anterior IPS areas, such as LIP, indicating that they play a role in relaying information from visual cortex to the higher level planning areas in IPS.
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In general, the many anatomical studies of parietal cortex over the past several decades have shown that it appears to be divided into many areas, each of which appears to play a role in translating sensory information into motor plans. But what exactly this role entailed remained a mystery until the technology to study these areas in vivo was developed, first in macaques and then later in humans.
Function In 1975 Mountcastle and colleagues first reported on electrophysiological recordings of macaque parietal cortex neurons while the monkey performed various tasks. They found that neurons in the IPS ‘‘appear[ed] to direct visual attention to objects of interest and motivational power, and to issue commands for maintaining directed fixation of the object when it [was] stationary, and to track it if it mov[ed].’’ In the decades since these early experiments, electrophysiological recordings of parietal cortex neural activity have determined that the SPL and IPL are subdivided into many smaller functional areas that appear to roughly correspond with the subdivisions determined by histological techniques. Each of these areas appears to extract the spatial information from one or more sensory inputs, and then play some role in transforming that information into a general movement plan in the same spatial coordinates. Because of its involvement in spatial processing, the parietal cortex is said to be part of the ‘where’ pathway (as opposed to the ventral ‘what’ pathway, which appears to be involved in processing the identity of a stimulus regardless of spatial location). For instance, the area LIP is involved in the planning of upcoming saccadic eye movements. The neurons in this area respond transiently to visual stimuli presented within a specific part of the visual field, which is known as a receptive field. Moreover, if a saccade is to be performed to that stimulus at some point in the future, the neurons continue to fire until the saccade has been executed. In this way, they are said to represent the planned target of the saccade until the action is completed, even if the visual stimulus is no longer in the receptive field. This characteristic is often used to define the boundaries of LIP in electrophysiological recording experiments. LIP neurons have large visual receptive fields that cover on average a quarter of the visual field, and these receptive fields move with the position of gaze (gaze centered). They are also more likely to respond to stimuli in the contralateral visual hemifield than in the ipsilateral, and may contain a coarse but continuous map of the contralateral visual field (otherwise known as being retinotopically organized). LIP neurons, then,
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appear to represent the plan of an upcoming saccadic eye movement in a rough spatial map of the visual environment. LIP neurons will also respond to a visual stimulus that is not the target of a planned saccade, but is otherwise task relevant. For instance, if the monkey is instructed to maintain fixation on a central point, and to indicate with his hand when a visual stimulus in the periphery dims just slightly, the LIP neurons representing the location of this stimulus continue to fire until the task is completed, and this increased level of firing is directly correlated to increased performance of whatever perceptual decision needs to be made at that location. Moreover, chemically deactivating LIP will result in the reduction of the monkey’s ability to discriminate an oddball stimulus from other stimuli (such as a red circle among a field of green circles). It appears, then, that LIP neurons also represent the current locus of visuospatial attention. Are these two purported functions of LIP neurons in conflict, or do they represent two ways of saying the same thing? The answer to this has been the source of a contentious debate. Thus far we have seen that LIP is involved both in covert shifts of attention (marking a location of interest so that processing of objects in that location can be enhanced) and in overt shifts of attention (making a saccade to a location so that it can be studied in more detail). One side of the debate holds that all covert shifts of attention represent potential saccades, and that the enhanced processing at that location is merely a side effect of planning a movement to that location. As evidence for this view, they point to other parietal areas, which appear to play the same planning role for other effectors, such as arm and hand movements. The ‘intentional map,’ then, might be a general principle of what the parietal cortex contributes to a sensorimotor transformation. The other side, however, contends that the LIP is a ‘salience map’ of the visual world, marking locations of interest for any number of systems to use, including the visual attention and oculomotor system. Part of the evidence for this view is that LIP neurons track the location of salient objects independently of stored oculomotor plans. While the differences between these two sides may seem minute, the resolution of this debate will give us insight into both what specific calculations parietal cortex neurons are performing on incoming information and in what terms the brain represents the external world – as a distorted version of reality, skewed toward the most interesting and relevant stimuli, or always in terms of a motor plan for interacting with the world? Other parietal areas in the macaque may also play roles in selective attention, though these areas have
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not been as thoroughly investigated as LIP. Areas caudal to LIP, such as DP, appear to play a role in visuospatial processing, though probably at an earlier stage than LIP (again fitting with their profiles of connections). Area 7a, which covers much of the IPL lateral to LIP, also appears to be involved in visuospatial processing. Like LIP, its neurons have large receptive fields, though it appears to evenly represent both the contralateral and ipsilateral hemifields. The neurons in this area appear to respond to the novel appearance of behaviorally relevant visual stimuli, but not as many of the 7a neurons have presaccadic activity as compared to LIP cells. This may indicate that rather than representing the current focus of attention, 7a neurons may be involved in detecting novel but potentially relevant stimuli, a counterpart of sorts to LIP. How other macaque parietal areas are involved in spatial attention is less clear, as they have generally been studied under the rubric of motor planning. Another important organizing principle for thinking about parietal cortex is to consider how space is coded in this region of the brain. There is evidence that parietal cortex subregions may be specialized for coding spatial location away from the body (or extrapersonal space) or near the body (or peripersonal space). This wealth of information about monkey’s parietal cortex until recently did not have a counterpart in the human work, because studies were limited to clinical observations (see later). This state of affairs changed in the late 1980s with the advent of positron emission tomography (PET), and then again in the 1990s with the advent of functional magnetic resonance imaging (fMRI). These neuroimaging technologies allowed, for the first time, in vivo studies of neural activity with sufficient spatial and temporal resolution to discern areas of the brain that were active in different tasks. Early PET studies confirmed that in humans the parietal lobe is also part of the dorsal ‘where’ pathway and is involved in the control of both spatial attention and eye movements. Several subsequent fMRI studies have also shown that, like in the macaque, the parietal region activated during covert shifts of attention largely overlaps with the region activated during saccades. This region includes much of the cortex in and around the IPS. Parts of this region are also activated during nonspatial shifts of attention, such as changing the focus of attention from the direction of moving dots to the color of the moving dots. Because of this profile of activity, the region along the human IPS has been thought of as generally homologous to the macaque IPS. However, due to the combination of relatively poor spatial resolution of fMRI and the high degree of variability in the location of sulci and gyri among
human individuals, it has been difficult to subdivide this region into functional areas as has been done in the macaque. Two foci of neural activity are consistently activated in different tasks requiring shifting or maintenance of attention. The first is in the SPL, on the dorsal–medial bank of the IPS. Because it is thought to be homologous to the macaque LIP, it is sometimes called human LIP (hLIP). Like macaque LIP, hLIP appears to be gaze centered in its spatial reference frame, responds more strongly to stimuli in the contralateral visual hemifield than in the ipsilateral, and appears to be loosely retinotopically organized. This area is activated if there is an attention shift to a peripheral location, and activity is sustained in this area if either attention remains focused on, or a saccade is being planned to, the peripheral location. Activity in this area seems to track both the locus of visuospatial attention and the target of an upcoming eye movement, extending the debate about parietal function to the human parietal cortex. While much of the functional profile of hLIP appears to be broadly similar to that of macaque LIP, the lack of direct comparisons of histological data or neural activity during tasks requiring shifts of attention prevents a more thorough assessment of the homology of these areas. Areas posterior to hLIP are also often activated in tasks requiring shifts of spatial attention. One of the most prominent is in the fundus of the caudal section of the IPS, and is variously termed ventral IPS (vIPS) or V7. This area is preferentially activated by attending to the contralateral hemifield, but appears to be more visual in nature than hLIP. V7 most likely represents an earlier stage of the ‘where’ pathway that probably relays visual information to hLIP, and is a potential homolog to one of the posterior parietal areas in the macaque. While the aforementioned areas in the human SPL are activated during voluntary and involuntary shifts of attention, the IPL appears to play a different role in attention. Regions in the IPL are only activated in response to the appearance of a salient, behaviorally relevant object, and even more so if attention has to be reoriented from another location (known as stimulus-driven reorienting of attention). Moreover, while activity in the SPL areas is increased during sustained covert shifts of attention, activity in the IPL is suppressed. It has been proposed that these areas play a role in stimulus-driven attention, especially when the focus of attention is captured by a salient and relevant novel stimulus. In macaques, area 7a (on the macaque IPL) is one possible candidate for a homolog to the human IPL. Another important feature of human parietal cortex is that it is anatomically and functionally asymmetrical. Several studies have now shown that
Attentional Networks in the Parietal Cortex
functional regions of the supramarginal and angular gyrus at the temporoparietal junction (TPJ) in humans show hemispheric asymmetries of attention (rightdominant) or verbal memory (left-dominant) tasks. This asymmetry is even more dramatic when one considers the behavioral effects of stroke in the middle cerebral artery (MCA) distribution that feeds the parietal cortex. Whereas left MCA strokes commonly result in aphasia (language deficits), strokes of the right MCA commonly result in a syndrome termed ‘neglect,’ which is a collection of spatial attention– perception–premotor deficits (see Figure 1(c)). An important goal for the future will be to reconcile monkey and human data in a common evolutionary framework that takes into account both commonalities and differences in functional organization. An important technological advance that will help this line of research is the development of fMRI studies in awake-behaving monkeys.
Lesions Damage to the right IPL often results in spatial neglect, a common syndrome following stroke in which patients are biased toward attending to the right side of visual space more than to the left side. Neglect can leave patients unable to perform simple tasks requiring spatial attention, and occurs in about 30% of all stroke-affected individuals. Patients with neglect often act as if part of the left side of their world does not exist. This inattention to the left side can occur in extrapersonal space or about the patient’s own body, and can occur in different reference frames: gaze-centered frame (left with respect to the center of gaze), body-centered frame (left with respect to the midline of the body), or world-centered frame (left with respect to the environment). Less commonly, patients can manifest socalled object-centered neglect, where the left side of an object is ignored, no matter if it is presented in the left or right side of the visual space. For instance, if a page of text with three columns is presented, a patient with body-centered or world-centered neglect will miss the words on the left side of the page, whereas a patient with object-centered neglect will miss the left side of each column or the left side of each word. Functionally, neglect patients may ‘forget’ to shave, groom, or dress the left side of body. They also have major problems with driving a car. Severely affected patients might also display a tonic rotation of the body or eyes toward the right, due to a coexisting motor imbalance. Some of these patients may still be able to detect a stimulus presented alone in the left hemifield, but when presented with stimuli simultaneously to both visual fields, patients tend to
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see only those in the right hemispace. This deficit is referred to as ‘extinction.’ Extinction is often tested by snapping fingers in one or both of the patient’s visual fields and asking the patient to point to which hand they saw or heard snapping. When fingers are snapped simultaneously in both visual fields, neglect patients will inexorably point to the hand in their right visual field. This test is one of the many routine exams in clinical settings to assess the severity of neglect. Other commonly used neuropsychological tests for diagnosis of neglect include line bisection, in which patients with neglect bisect a horizontal line to the right of the true center; a series of cancellation tasks, in which neglect patients commonly miss marking targets on the left side of a paper; clock drawing, in which neglect patients may draw only the right half of a clock; and a baking-tray task, in which neglect patients usually cluster cookies on the right side of a baking tray. In addition to the lack of awareness of the left side of space, neglect patients can also manifest deficits in planning hand or eye movements toward the left side of space. In this type of neglect, patients may not demonstrate a bias in awareness to either visual field, but will be less inclined to reach or look for objects located in the left visual field. This form of neglect is called motor or premotor neglect, or directional hypokinesia, to emphasize its relationship to action. In addition to lateralized (i.e., left worse than right space) deficits, a number of so-called nonlateralized deficits (i.e., similar across left and right visual fields) have also been described, including impairment of spatial working memory, sustained attention, and an overall lower level of alertness. An important focus of current research is to assess the functional effect of different deficits, their importance for final outcome, their recovery over time, and their localization in the brain. Shall we think of neglect as a homogeneous or heterogeneous syndrome? What are the regions more responsible for one or another deficit? We know that spatial neglect can occur as a clinical syndrome for lesions in many parts of the brain, including parietal, temporal, frontal cortex, basal ganglia, thalamus, and in various white-matter tracts. It is still unknown how these different lesions may or may not cause different behavioral profiles of neglect, and how the effect of lesions in the brain relates to the functional organization observed in healthy individuals. An alternative view considers neglect not to be the effect of damage to specific cortical areas, but rather the result of a distributed and combined anatomical– functional dysfunction of large parts of parietal and frontal cortices and their connections. In general, the areas that are damaged in neglect are located ventrally in the brain, including the IPL regions
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specialized for stimulus-driven attention. Conversely, damage to more dorsal IPS and SPL regions does not produce strong neglect; rather, these lesions produce primarily eye- or arm-movement planning problems, which is also consistent with the results of functional imaging studies in healthy volunteers. However, only a few patients with damage restricted to the SPL have been studied. One model of neglect postulates that damage by stroke or trauma to the IPL in the region of the TPJ could give rise to both spatial and nonspatial deficits by interrupting input to the SPL attentional areas from the TPJ. This disruption would then reduce the brain’s ability to detect important sensory events in both visual fields. In addition, this lack of input into ipsilesional dorsal areas may induce a relative interhemispheric imbalance in the dorsal attentional areas that code for spatial locations and eye and arm movements. The imbalance due to the competitive nature of interhemispheric processing will lead to a relative hyperorienting toward right space, with consequent problems of attention and detection in left space. This model of spatial bias based on interhemispheric competition is also supported by a number of animal studies in which neglect has been cured by inactivating homologous parietal regions of the intact hemisphere.
Conclusion Parietal cortex is subdivided into different areas, based on both anatomical and functional criteria; these areas have connections with both sensory processing and motor planning regions of the brain. Some of these areas appear to be involved in the selection and representation of locations and objects of interest in the immediate environment. The spatial information in parietal cortex can then be ‘read out’ by other brain areas, both for the planning of movements and for the enhancement of sensory processing. Attention can be directed to a location or object by a premeditated plan, or by the appearance of a novel stimulus that may require additional processing. Area LIP in the macaque and its putative homolog in the SPL of humans appear to be involved in representing the locations of interest, whereas IPL areas appear to play the role of reorienting attention whenever a novel stimulus enters awareness. Damage to these areas results in the syndrome of neglect, which fundamentally involves a lack of awareness for
spatial information, as well as problems with vigilance and motor planning. See also: Attention and Eye Movements; Attention: Models; Attentional Functions in Learning and Memory; Attentional Mechanisms in Ventral Pathway; Attentional Networks; Decision-Making and Vision; Neglect Syndrome and the Spatial Attention Network; Parietal Cortex and Spatial Attention; Psychophysics of Attention; Visual Attention.
Further Reading Andersen RA and Buneo CA (2002) Intentional maps in posterior parietal cortex. Annual Review of Neuroscience 25: 189–220. Colby CL and Goldberg ME (1999) Space and attention in parietal cortex. Annual Review of Neuroscience 22: 319–349. Corbetta M and Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience 3: 201–215. Desimone R and Duncan J (1995) Neural mechanisms of selective visual attention. Annual Review of Neuroscience 18: 193–222. Egeth HE and Yantis S (1997) Visual attention: Control, representation, and time course. Annual Review of Psychology 48: 269–297. Goldman-Rakic PS (1988) Topography of cognition: Parallel distributed networks in primate association cortex. Annual Review of Neuroscience 11: 137–156. Hillis AE (2006) Neurobiology of unilateral spatial neglect. Neuroscientist 12: 153–163. Husain M and Rorden C (2003) Non-spatially lateralized mechanisms in hemispatial neglect. Nature Reviews Neuroscience 4: 26–36. Kastner S and Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annual Review of Neuroscience 23: 315–341. Lewis JW and Van Essen DC (2000) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipetal complex. Journal of Comparative Neurology 428: 79–111. Avaliable at URL: http://sumsdb.wustl.edu:8081/ sums/directory.do?id=679531. Mesulam MM (1999) Spatial attention and neglect: Parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 354: 1325–1346. Mountcastle VB, Lynch JC, Georgopoulos A, et al. (1975) Posterior parietal association cortex of the monkey: Command function for operations within extrapersonal space. Journal of Neurophysiology 38: 871–908. Orban GA, VanEssen D, and Vanduffel W (2004) Comparative mapping of higher visual areas in monkeys and humans. Trends in Cognitive Science 8: 315–324. Pashler HE (1998) The Psychology of Attention. Cambridge, MA: MIT Press. Posner MI and Petersen SE (1990) The attention system of the human brain. Annual Review of Neuroscience 13: 25–42.