Invited Symposium: What Can Genetic Models Tell Us About Attention-Deficit Hyperactivity Disorder (ADHD)?
Attention is currently being examine in terms of three major functions: orienting to sensory stimuli, executive functions, and maintaining the alert state (Posner & Raichle, 1996). Although knowledge of the precise neural mechanisms responsible for these operations is still incomplete, many of the brain areas and networks involved have been identified. Moreover, there is evidence that damage to some of these networks produces similar symptoms regardless of whether the etiology is stroke, degenerative disease, psychopathology or abnormality of development (Fernandez-Duque & Posner, in process; DiGirolamo & Posner, 1996). For this reason, a knowledge of the networks of attention may be of special use in examination of disorders with attentional symptoms whose cause is not well understood, such as ADHD. In this paper we will briefly examine the three networks in light of new findings that might relate to theories of ADHD.
Many attempts have been made to understand and characterize the deficits associate with ADHD. Recently, three different theoretical accounts have been proposed (Barkely, 1998; Sergeant et al., in press; Swanson et al., 1998a). We attempt to argue that it is possible to conceptualize all three under the umbrella of pathologies of attentional networks.
Networks of attention
Posner and Raichle (1996) summarized the three attentional networks approach, and based the localization of the different networks on the brain-imaging literature. Each attentional function is localized not in a single brain area, but as a network of interconnected brain areas.
Executive-control network. This network has been related to the control of goal directed behavior, target detection, error detection, conflict resolution and inhibition of automatic responses. The executive control network seems to include the midline frontal areas including the anterior cingulate gyrus, SMA, and portions of the basal ganglia. Neuroimaging studies have shown activity in this area during tasks that require mental effort such as in dealing with conflict, handling novelty, developing anticipations and detecting errors (Posner & DiGirolamo, 1998). Recently it has been shown that tasks involving both cognitive and emotional controls produce activation in the cingulate (Bush et al., 1998; Posner & Rothbart, in press).
Accumulating evidence shows involvement of the basal ganglia, more specifically the caudate nucleus, in cognitive functioning (Beiser, et al., 1997). Many studies showed similar behavioral deficits in animals following experimental lesions of the anterior dorsolateral frontal cortex and the caudate. Moreover, the caudate and the prefrontal cortex showed similar activity when recorded with depth electrodes during tasks as lexical decision and semantic categorization, that were not due to motor or premotor programming (Abdullaev et al., in press). In addition to that, the basal ganglia have been considered to be particularly important in mediating the connection between executive attention and other attentional networks (Jackson, Marrocco & Posner, 1994; LaBerge, 1990).
Lateral areas of the frontal cortex have also often been identified with executive attention. However, the bulk of the literature suggests to us that these areas involve representation of specific kinds of spatial, verbal or form information rather than more general attentional operations.
Alerting network. The alerting network is defined by a network of brain areas in the right frontal lobe (especially the superior region of Brodmann area 6), the right parietal lobe and the locus ceruleus (Posner & Petersen, 1990; Posner & Raichle, 1996). This network is involved in establishing a vigilant state and maintaining readiness to react. Recent alert monkey studies have shown clearly that the readiness induced by warning signals can be blocked by drugs that reduce norepineperine (Marrocco & Davidson, 1998). In addition patients with right parietal lesions show difficulty in sustaining attention and in the use of warning signals to improve behavior (Robertson et al., 1995).
Orienting network. A network for covert orienting to sensory, particularly visual signals, has been discussed in some detail previously (Posner & Dehaene, 1994). (Neuroimaging evidence has shown that covert shifts of visual attention most strongly activates the parietal lobe Moreover, other areas, related also to the oculo-motor system, are also activated (Corbetta, 1998). There is strong evidence that attending to a spatial location increases blood flow and electrical activity in extrastriate visual regions particularly the fusiform gyrus (Magnun, et al., in press).
Leading theories of ADHD
As mentioned in the introduction, three theoretical accounts explaining ADHD have been recently proposed. Swanson et al. (1998a) charaterized ADHD as a combination of executive attention and alerting deficits. This approach focuses on two of the attentional networks and predicts brain pathology in areas related to these networks, i.e., midline frontal cortex (cingulate and SMA), basal ganglia (especially caudate), anterior prefrontal cortex, anterior right parietal cortex. According to Barkley (1998), the core of ADHD pathology are Executive Functions. By executive functions he referred to working memory, internalization of self-directed speech, control of emotion arousal and motivation. Barkley suggests that during normal development children switch from external cues to internal guidance of behavior. Although the definition of executive functions varies somewhat in the literature, most of the functions included by Barkley have been conceptualized, as being part of the executive attention network. Activation of both emotional and cognitive tasks has been shown to occur in the anterior cingulate (Bush et al., 1998). Posner & Rothbart (in press) have argued that emotional control mechanisms arise in early infancy and this same general system is later used for control of conflict and other executive functions. Barkely, too, although using a different nomenclature, ties the dishinhibition behavioral symptoms of ADHD as being secondary to the main executive control deficit. Sergeant et al., (in press), on the other hand, emphasize the energetic factors, as the most critical deficit in ADHD. According to their framework, ADHD suffer from a deficit in the energetic maintenance and allocation of resources (which leads to the secondary symptoms of dishinhibitory behavior). This approach identifies the activation pool with the basal ganglia and corpus striatum, and suggest it operates mainly through criteria shifts in the criterion for responding. According to an attentional network framework, this frontal activation could, too, be part of the executive control network.
Brain pathologies in ADHD
Filipek (Filipek, 1996; Filipek et al., 1997) found that despite similar hemispheric volumes, ADHD subjects had smaller volumes of left caudate and caudate head, with reverse asymmetry than controls and right anterior-superior frontal region en bloc and white matter. Moreover, possible structural correlates of ADHD response to stimulants were found. Castellanos et al. (1996) found smaller right anterior frontal, caudate and globus pallidus regions in ADHD compared to control. Aylward et al. (1996), too, report volumetric differences in caudate and globus pallidus, between ADHD children and control (for review, see Swanson et al. (1998b)).
Behavioral studies support the basic idea that ADHD is a deficit in executive control and regulation that extends to emotional and cognitive processes (Barkley, 1998). There is evidence of difficulty in controlling the activation state (Sergeant et al., 1998). This result may relate to basal ganglia and frontal control system deficits, rather than more direct NE or parietal abnormalities. There is little empirical support of the involvement of the orienting network in ADHD pathology. Although a few studies have tested endogenous and exogenous orienting of attention, in ADHD, the results are ambiguous as to abnormalities in the basal ganglia and frontal control structures, versus parietal structures.
For many years, psychiatrists and psychologists have been trying to define and understand the deficits that underlie ADHD. Evidence is consistent with difficulties in two of the attentional networks: executive functions / effortful control, and vigilance and alerting regulation. We believe that a better understanding of the functions and neuroanatomical bases of attentional networks in normal development, will be helpful in understanding ADHD.
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|Berger, A.; Posner, M.I.; (1998). Pathologies of Brain Attentional Networks. Presented at INABIS '98 - 5th Internet World Congress on Biomedical Sciences at McMaster University, Canada, Dec 7-16th. Invited Symposium. Available at URL http://www.mcmaster.ca/inabis98/sadile/berger0855/index.html|
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