Research on Attention Networks As a Model for the Integration of Psychological Science
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ANRV296-PS58-01 ARI 17 November 2006 1:10 Research on Attention Networks as a Model for the Integration of Psychological Science Michael I. Posner and Mary K. Rothbart1 Psychology Department, University of Oregon, Eugene, Oregon 97403-1291; email: [email protected], [email protected] Annu. Rev. Psychol. 2007. 58:1–23 Key Words First published online as a Review in attention, candidate genes, orienting, neural networks, Advance on October 9, 2006 temperament The Annual Review of Psychology is online at http://psych.annualreviews.org Abstract This article’s doi: As Titchener pointed out more than one hundred years ago, at- 10.1146/annurev.psych.58.110405.085516 tention is at the center of the psychological enterprise. Attention Copyright c 2007 by Annual Reviews. research investigates how voluntary control and subjective experi- All rights reserved ence arise from and regulate our behavior. In recent years, attention 0066-4308/07/0110-0001$20.00 has been one of the fastest growing of all fields within cognitive psy- 1We appreciate the invitation of the editors chology and cognitive neuroscience. This review examines attention of the Annual Review of Psychology to submit a as characterized by linking common neural networks with individual prefatory essay to this year’s volume. We differences in their efficient utilization. The development of atten- have taken the opportunity to propose a by UNIVERSITY OF FLORIDA on 08/22/07. For personal use only. unified basis for psychological science based tional networks is partly specified by genes, but is also open to specific upon an effort to combine experimental and experiences through the actions of caregivers and the culture. We Annu. Rev. Psychol. 2007.58:1-23. Downloaded from arjournals.annualreviews.org differential approaches to the field. This believe that the connection between neural networks, genes, and article is an improved and expanded version of an earlier one along these lines (Posner & socialization provides a common approach to all aspects of human Rothbart 2004), and its developmental cognition and emotion. Pursuit of this approach can provide a basis aspects are further expanded in a book for psychology that unifies social, cultural, differential, experimen- (Posner & Rothbart 2007). tal, and physiological areas, and allows normal development to serve as a baseline for understanding various forms of pathology. D.O. Hebb proposed this approach 50 years ago in his volume Organiza- tion of Behavior and continued with introductory textbooks that dealt with all of the topics of psychology in a common framework. Use of a common network approach to psychological science may allow a foundation for predicting and understanding human behavior in its varied forms. 1 ANRV296-PS58-01 ARI 17 November 2006 1:10 At the time Hebb wrote his monograph, Contents relatively little was known about how the structure and organization of the central ner- INTRODUCTION................. 2 vous system contribute to the functions ob- HEBB’S NETWORK served in psychological studies. This led Hebb APPROACH .................... 4 to talk in terms of the conceptual nervous New Tools ....................... 5 system, that is, ideas about its structure that IMAGING ATTENTION might be imagined or inferred from psycho- NETWORKS ................... 6 logical studies. We suggest that the meth- Simulating Attention Networks . 8 ods available to Hebb, mostly animal research INDIVIDUAL EFFICIENCY....... 9 and behavioral human experiments, were not NETWORK DEVELOPMENT .... 11 sufficient to provide empirical methods for Socialization and Culture ......... 13 linking his conceptual nervous system to real PATHOLOGY OF ATTENTION events in the human brain. This methodology NETWORKS ................... 15 has now been provided by neuroimaging. Al- Plasticity ......................... 16 though Hebb also recognized the importance INTEGRATION OF of studying individual differences in intelli- PSYCHOLOGICAL SCIENCE. 17 gence and affect, at that time there were no Generality ....................... 17 methods for exploring the specific genes that are an important source of these differences. The human genome project has provided new INTRODUCTION methods for exploring this issue. Can psychology be a unified science, or must In Hebb’s time, the idea of a network (cell it remain fragmented and subject to transient assembly or phase sequence) was a rather research interests rather than cumulative de- vague verbal abstraction that did not allow velopment? Is psychology teachable or must for models that could produce specific pre- Attention: the regulating of various psychology textbooks remain encyclopedias dictions. As a result of the rapid changes in brain networks by of often unrelated findings? In this article, cellular biology (Bullock et al. 2005) and in attentional networks we examine research on attention to suggest the mathematics of multilevel networks, this involved in ways of looking at psychological questions and too has changed (Rumelhart & McClelland maintaining the alert findings that might lead to hopeful answers to 1986). Although early versions of these net- state, orienting, or regulation of conflict these questions. We offer a model based on works were inspired by simple versions of Hebbian psychology that reaches out from neurons as all-or-none elements, more recent Neural networks: a by UNIVERSITY OF FLORIDA on 08/22/07. For personal use only. number of brain biological roots to tackle questions of emo- versions (O’Reilly & Munakata 2000) have be- areas that when tion and thought as well as behavior. We, with gun to use the details of neuroanatomy and Annu. Rev. Psychol. 2007.58:1-23. Downloaded from arjournals.annualreviews.org orchestrated carry many of our colleagues, see different levels cellular structure as provided by imaging and out a psychological of analysis in psychology as informing each cellular studies to develop networks that take function other, with each level of equal scientific valid- more realistic advantage of the structure of ity. Bridging these levels can allow a higher the human brain. Hebb’s basic idea, together level of understanding and prediction. with the new methodological tools and new We argue that D.O. Hebb (see Figure 1), disciplines (e.g., cognitive, affective, and so- beginning with his monograph in 1949 and cial neuroscience), all based on network views, continuing through a series of introductory give abundant evidence of the value of em- textbooks (1958, 1966), has convincingly pre- ploying the converging operations strategy sented the basis for such integration. This in- advocated by Sternberg (Sternberg 2004). tegration lies in understanding how genes and It is important to recognize the need for in- experience shape neural networks underlying tegrating cognitive, affective, and social neu- human thoughts, feelings, and actions. roscience with psychology because many of 2 Posner · Rothbart ANRV296-PS58-01 ARI 17 November 2006 1:10 by UNIVERSITY OF FLORIDA on 08/22/07. For personal use only. Annu. Rev. Psychol. 2007.58:1-23. Downloaded from arjournals.annualreviews.org Figure 1 Photograph of Professor Donald O. Hebb. www.annualreviews.org • Research on Attentional Networks as a Model 3 ANRV296-PS58-01 ARI 17 November 2006 1:10 the theoretical questions that need to be ad- rons and between neurons and other brain dressed by neuroimaging and genetic studies cells (Bullock et al. 2005). These develop- are exactly those that a century of psychol- ments have reduced the gap between networks ogists have explored. The neuroscience ap- revealed in imaging studies and the complex proach provides crucial constraints for psy- intracellular activity that underlies them. In chological theories, but it also benefits when particular, they show that learning may reflect a closer connection is made with the psycho- the activity of interactions at many time scales logical level of analysis. and may be modified by aspects of the organ- ism’s overall state. Hebb also introduced the concept of the HEBB’S NETWORK APPROACH phase sequence involved in the coordination In 1949, D.O. Hebb published his epic work, of multiple cell assemblies. He recognized the The Organization of Behavior. His book was importance of the temporal correspondence immediately recognized as providing the po- between assemblies. In recent years these tential for an integrated psychology. One ideas have been supported by studies show- reviewer (Attneave 1950, p. 633) wrote: ing that synchronization of brain areas may be critical to detecting stimuli (Womelsdorf et al. I believe The Organization of Behavior to be 2006) and for transfer of information between the most important contribution to psycho- remote areas (Nikolaev et al. 2001). In later logical theory in recent years. Unlike those years, Hebb (1958) developed an introductory of his contemporaries who are less interested psychology textbook that integrated much of in psychology than in some restricted as- psychology using the framework provided by pect thereof to which their principles con- his 1949 theory. He applied his network the- fine them, Hebb has made a noteworthy at- ory to heredity, learning and memory, motiva- tempt to take the experimentally determined tion, perception, thought, and development. facts of behavior, as they are, and account for In later editions, he extended his approach them in terms of events within the central to emotions in their social contexts, individ- nervous system. ual differences in intelligence, and abnormal psychology.