Anatomy of Attentional Networks

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Anatomy of Attentional Networks THE ANATOMICAL RECORD (PART B: NEW ANAT.) 281B:21–36, 2004 FEATURE ARTICLE Anatomy of Attentional Networks AMIR RAZ Attention is a central theme in psychological science. As with other biological systems, attention has a distinct anatomy that carries out basic psychological functions. Disparate attentional networks correlate with discrete neural circuitry and can be influenced by specific brain injuries, states, and drugs. Accordingly, thinking about attention as an organ system is advantageous for understanding the details of this complex cognitive process. In the context of an influential model of attention, this article introduces the broad notion of attention, then addresses its prominent characteristics, mechanisms, and theories. The presentation emphasizes the role of recent neuroimaging data in outlining the functional neuroanatomy subserving distinct attentional networks. A discussion of pertinent results connects attentional networks with self-regulation, development, and rehabilitation training. Anat Rec (Part B: New Anat) 281B:21–36, 2004. © 2004 Wiley-Liss, Inc. KEY WORDS: attentional networks; imaging; neuroimaging; cognitive control; neuroscience; hemispheres INTRODUCTION one out of what seem several simulta- plying formal information theory, neous objects or trains of thought.” Broadbent likened attention to a filter. One of the oldest and most central James’ account strongly joins atten- He proposed that attention was issues in psychological science, atten- tion with subjective experience. More- bounded by the amount of informa- tion is the process of selecting for ac- over, James’s addressing of attention tive processing ideas stored in mem- tion located between parallel sensory both to objects and to “trains of ory in our minds, or aspects of our systems and a limited-capacity per- thought” is important for understand- physical environment, such as ob- ceptual system (Broadbent, 1958). ing current approaches to sensory ori- jects. The study of attention has be- This view facilitated objective studies enting and executive control (Driver come a huge enterprise; last year of the limitations of the human ability and Frackowiak, 2001; Fernandez- alone about 300 articles were pub- to deal with multiple signals at a time Duque and Posner, 2001; Fan et al., lished on attention (Fig. 1). Through- in a variety of practical tasks. 2003a,b). However, as outlined below, out history, many great minds have As psychology moved toward the wrestled with the definition of atten- study of cognitive mechanisms, new tion. In 370 B.C., Aristotle regarded objective methods allowed for inves- attention as a narrowing of the senses. tigation into the processes of selec- Centuries later, William James (1890) Attention is not, as the tion. For example, studies showed contended that “everyone knows what quote from William that words could activate their se- attention is. It is the taking possession mantic associates without aware- of the mind in clear and vivid form of James implies, the same ness of the word’s identity (i.e., as being aware. priming). The parallel organization of sensory information extends to se- Dr. Raz is on the faculty of the MRI Unit mantic processing. The act of select- in the Department of Psychiatry, Divi- ing a word meaning for active atten- sion of Child and Adolescent Psychiatry, at Columbia University College of Phy- attention in the sense of orienting to tion appears to suppress the sicians and Surgeons and New York sensory objects can actually be invol- availability of other meanings of the State Psychiatric Institute. untary and can occur unconsciously. selected item and of competing *Correspondence to: Amir Raz, MRI Unit, Department of Psychiatry, Division So attention is not, as the quote from items. Consequently, attention has of Child and Adolescent Psychiatry, Co- William James implies, the same as since been viewed more as a mecha- lumbia University College of Physicians and Surgeons and New York State Psy- being aware (see Table 1 for a list of nism for providing priority for mo- chiatric Institute, 1051 Riverside Drive, important terms and definitions in tor acts than as a filter or bottleneck. Box 74, New York, NY 10032. Fax: 212- this field of study). For example, the premotor theory 543-6660; E-mail: [email protected] Following a lull in the field during suggests that attention is simply a DOI 10.1002/ar.b.20035 the early 1900s, Donald Broadbent re- preparation for response, or a select- Published online in Wiley InterScience (www.interscience.wiley.com). sumed the quest after World War II to ing of the goal of an intended action discover attentional mechanisms. Ap- (Rizzolatti et al., 1987). The focus on © 2004 Wiley-Liss, Inc. 22 THE ANATOMICAL RECORD (PART B: NEW ANAT.) FEATURE ARTICLE tion. These similar and demanding GROSS CHARACTERISTICS OF tasks can at first only be done in alter- ATTENTION nation, but after months of practice can be efficiently combined (Spelke et al., Visual attention often serves as a con- 1976). Given these examples, theories venient lens to examine the character- of attentional limits must also account istics of attention. Researchers and for how these limits can be eliminated clinicians have investigated the optics, (e.g., following practice) when the bot- anatomy, development, pathology, tleneck is seemingly bypassed and the and underlying neural processes of vi- correct action is effortlessly performed. sion, making it the most widely stud- TABLE 1. Terms and definitions related to attentional network research Figure 1. Research into Attention. Relative Foveate To look at directly so the image being viewed numbers of publications for each of five key falls on the fovea of the retina words, normalized to their relative frequen- Attention The mental ability to select stimuli, responses, cies in the 1960-1969 decade. The 2000 memories, and thoughts that are data span only the years 2000 to 2003. The behaviorally relevant among a host of others relative frequency values were computed by adding up all the papers that used each that are behaviorally irrelevant of these keywords in 1960–1969 in PubMed Attentional networks Neural circuits subserving attentional and finding the proportion using each key- processing, which preserve a degree of word. These were the base proportions. The anatomical and functional independence relative proportions were then the propor- but interact in many practical situations tions in each subsequent decade divided Executive network The mechanism for monitoring and resolving by the original proportions from 1960–1969. conflict among thoughts, feelings, and From Cavanagh (2003, 2004). responses; an attentional system concerned with such tasks as working memory, response may explain why atten- planning, switching, and inhibitory control tional systems seem to differ for Orienting The process of selecting information from sensory input space that is within reach and space Alerting The process of achieving and maintaining a that lies beyond. However, intended state of high sensitivity to incoming stimuli actions are probably not the only Top-down A downstream effect such as cognitive sources of capacity limits and atten- modulation control, as opposed to a bottom-up effect tional selection. After all, even when Cognitive control Processes such as conflict resolution, error we have no intention to act and pas- correction, inhibitory control, planning, and sively watch scenes go by (e.g., at the resource allocation movies), we still select only a subset Self-regulation A key mediator between genetic of the information that reaches the predisposition, early experience, and adult senses. Attention, therefore, was fur- functioning (e.g., in controlling the reaction to stress, the capacity to maintain focused ther operationalized as facilitating attention or the ability to interpret mental some kinds of memory and even states both internally and in others) consciousness. Neuroimaging Technologically advanced, often noninvasive, Other views construe attention in tools for tapping neurophysiological aspects the context of resource limitation/ of the behaving brain selection. Attentional limits are typ- Mismatch negativity An electrophysiological manifestation of ically found in unpracticed tasks. (MMN) involuntary preattentive processing occurring However, with practice, most atten- when some regularity in the auditory stream tion-demanding tasks can be ren- is violated by a change (deviant stimulus); dered attention-independent, or au- the MMN is advantageous with regard to the neural processing of unattended input tomatized. One example of this Anterior cingulate Part of the brain’s limbic system classically phenomenon involves visually cortex (ACC) related to affect but also active in many searching for a set of letters among studies of cognition; the ACC might be the other random letters. This task ini- brain’s error detection and correction tially demands attention and gives device part of a circuit involved in a form of steep slopes of latencies against dis- attention that serves to regulate both play size. However, after weeks of cognitive and emotional processing practice, the slopes become flat Functional magnetic A noninvasive neuroimaging technique that (Spelke et al., 1976; Schneider and resonance registers blood flow to functioning areas of Shiffrin, 1977). Another example imaging (fMRI) the brain in high magnetic fields Positron emission A neuroimaging technique measuring the flow comes from a demonstration involv- tomography (PET) of blood containing
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