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The Cortical Substrate of General Intelligence
FORUM ON INTELLIGENCE THE CORTICAL SUBSTRATE OF GENERAL INTELLIGENCE Joaquin M. Fuster (Cognitive Neuroscience Laboratory, Neuropsychiatric Institute, University of California, Los Angeles)
Intelligence is the most complex of all cognitive functions. One reason for its complexity is its close dependency on other functions – namely, perception, attention, memory, and language. The degree of contribution of any of those other functions to intelligence varies greatly with the individual and, at any given time, with the environmental demands (including those from the internal milieu). Adding to the complexity of human intelligence is the inescapable reality that, by any definition, it can have practically unlimited manifestations. This inference derives from the inextricable relationship between intelligence and creativity, the latter being open-ended and inexhaustible. In sum, any suitable definition of intelligence must be broad enough to account for the multiplicity of its cognitive supports as well as its potential outcomes. Such a definition must include the capacity to adapt by reasoning to new changes, to solve new problems, and to produce valued new forms of action and expression. In the latter respect, of course, intelligence intersects ethics and esthetics. Among the many manifestations of intelligence, only those that result from reasoning and problem solving are amenable to measurement. This measurement is the role of psychometrics. Thus, psychometrics can only measure limited aspects of intelligence. This, by itself, challenges a concept of general intelligence that is based only on psychometrics. Further, the cognitive functions that psychometrics measures, including intelligence, can only be defined operationally, however well construed those functions may be in psychological terms – and however plausible their underlying assumptions. In psychology, all operational definitions, including those that derive from psychometrics, are reducible to performance, whether the latter is measured in terms of reaction time, accuracy, correctness, or what not. Thus, Spearman’s concept of general intelligence, as well as his g-factor, result from measures of intellectual performance. Consequently, it seems that what he called general intelligence is not a kind of “energy” that supports all kinds of intellectual performance but, instead, the result of the interaction of several underlying cognitive functions that contribute to intelligence and its overt manifestations. From this conceptual perspective, we can approach the neuropsychology of general intelligence without slipping into yet another phrenological error. By reasoning backward from the performance side of Cortex, (2005) 41, 228-229
intelligence and the neural substrate of the cognitive functions that support it, this approach leads us to the frontal lobe. Let us briefly see how. A critical function of the prefrontal cortex (Fuster, 1997) is to support the ability of the organism to integrate temporal gestalts of goaldirected action in every domain – behavior, language, and thinking (e.g., logical reasoning, inductive or deductive). Whether the temporal integration of action takes place to adapt to the environment or to follow the instructions of an experimenter or psychometrician, it pre-requires the cortical formulation of a “plan,” a “schema,” or a “strategy “ to attain the goal. As I argue elsewhere (Fuster, 2003), this cortical formulation can be suitably construed as a distributed network of dispersed cortical neurons representing the task and its constituents in long-term memory. The code of that representation is a relational one, essentially based on fiber associations between neurons (a neuron or group or neurons practically anywhere in the cortex can be part of many networks, thus many memories). Because the representation formulated for impending or on-going action is, by definition, an executive representation, it is reasonable to suppose that its network contains critical neuronal nodes in the associative cortex of the frontal lobe. Further, it is reasonable to suppose that this cortex plays a fundamental role in the implementation of the integrated action (i.e., the activation and instantiation of the network). In support of these assumptions is a massive body of neuropsychological and neurophysiological evidence from the human and non-human primate. In order to mediate the execution of temporally integrated action, the association cortex of the frontal lobe, or prefrontal cortex, has to participate, concomitantly or in succession, in several cognitive operations. Perception is one of them. Any series of acts toward a goal engages neural structures at several levels of the perception-action cycle. This cycle is the circular cybernetic flow of processing of neural impulses from sensory systems to motor systems and, through the environment, back to sensory systems that controls the timing and characteristics of every action. Essential to this control is the continuous monitoring of the environment and of the changes induced in it by the organism in the pursuit of its goal. If that pursuit requires the mediation of cross-temporal contingencies between events that are novel, uncertain, or ambiguous, then the higher levels of
Cortex Forum
the cortex are engaged in the perception-action cycle. At the highest level of the executive component of the perception-action cycle is the prefrontal cortex, which is reciprocally linked through long connections with sensory association areas of posterior cortex. Attention, which is the selective allocation of neural resources to current behavior, is another of the cognitive functions that contribute to temporal integration – and thus general intelligence. Both sensory attention and executive attention come under prefrontal control in the course of temporally integrated action. Moreover, both those forms of attention have an inclusive (focus) and an exclusionary (inhibitory) component, both of these under prefrontal control. The prefrontal cortex exerts that control through its neural influences over other cortical areas (via long connections), thereby ensuring the selection among competing inputs and outputs that organized behavior necessitates (Desimone and Duncan, 1995; Fuster, 1997). A meta-analysis of neuroimaging studies of the prefrontal cortex shows that different prefrontal area participate to different degrees in a variety of temporal-integrative tasks, depending on the cognitive demands of each task (Duncan and Owen, 2000). On close analysis, it appears that the differential participation of prefrontal areas in task performance stems from a differential participation of those areas in different aspects of
229
attention. The anterior cingulate area appears mainly involved in tasks that demand the effortful focusing of attention and the resolution of conflict between alternatives; the orbital (ventral) area appears mainly involved in tasks that demand the inhibitory – exclusionary – attention control of interference. The lateral prefrontal cortex, otherwise, seems chiefly involved in the attention that is directed to internal representations of sensory character (working memory) or of motor character (executive set). In conclusion, the concept of general intelligence characterizes in operational terms, that is, in terms of performance, the joint operation of several cognitive functions, notably attention, in the temporal organization of actions. Inasmuch as those functions depend to a large degree on the physiological intervention of the prefrontal cortex, this cortex can be justifiably considered a critical neural agency of general intelligence. REFERENCES DESIMONE R and DUNCAN J. Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18: 193-222, 1995. DUNCAN J and OWEN AM. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends in NeuroSciences 23: 475-483, 2000. FUSTER JM. The Prefrontal Cortex – Anatomy Physiology, and Neuropsychology of the Frontal Lobe. Philadelphia: Lippincott-Raven, 1997. FUSTER JM. Cortex and Mind: Unifying Cognition. New York: Oxford University Press, 2003.
Intelligence is the most complex of all cognitive functions. One reason for its complexity is its close dependency on other functions – namely, perception, attention, memory, and language. The degree of contribution of any of those other functions to intelligence varies greatly with the individual and, at any given time, with the environmental demands (including those from the internal milieu). Adding to the complexity of human intelligence is the inescapable reality that, by any definition, it can have practically unlimited manifestations. This inference derives from the inextricable relationship between intelligence and creativity, the latter being open-ended and inexhaustible. In sum, any suitable definition of intelligence must be broad enough to account for the multiplicity of its cognitive supports as well as its potential outcomes. Such a definition must include the capacity to adapt by reasoning to new changes, to solve new problems, and to produce valued new forms of action and expression. In the latter respect, of course, intelligence intersects ethics and esthetics. Among the many manifestations of intelligence, only those that result from reasoning and problem solving are amenable to measurement. This measurement is the role of psychometrics. Thus, psychometrics can only measure limited aspects of intelligence. This, by itself, challenges a concept of general intelligence that is based only on psychometrics. Further, the cognitive functions that psychometrics measures, including intelligence, can only be defined operationally, however well construed those functions may be in psychological terms – and however plausible their underlying assumptions. In psychology, all operational definitions, including those that derive from psychometrics, are reducible to performance, whether the latter is measured in terms of reaction time, accuracy, correctness, or what not. Thus, Spearman’s concept of general intelligence, as well as his g-factor, result from measures of intellectual performance. Consequently, it seems that what he called general intelligence is not a kind of “energy” that supports all kinds of intellectual performance but, instead, the result of the interaction of several underlying cognitive functions that contribute to intelligence and its overt manifestations. From this conceptual perspective, we can approach the neuropsychology of general intelligence without slipping into yet another phrenological error. By reasoning backward from the performance side of Cortex, (2005) 41, 228-229
intelligence and the neural substrate of the cognitive functions that support it, this approach leads us to the frontal lobe. Let us briefly see how. A critical function of the prefrontal cortex (Fuster, 1997) is to support the ability of the organism to integrate temporal gestalts of goaldirected action in every domain – behavior, language, and thinking (e.g., logical reasoning, inductive or deductive). Whether the temporal integration of action takes place to adapt to the environment or to follow the instructions of an experimenter or psychometrician, it pre-requires the cortical formulation of a “plan,” a “schema,” or a “strategy “ to attain the goal. As I argue elsewhere (Fuster, 2003), this cortical formulation can be suitably construed as a distributed network of dispersed cortical neurons representing the task and its constituents in long-term memory. The code of that representation is a relational one, essentially based on fiber associations between neurons (a neuron or group or neurons practically anywhere in the cortex can be part of many networks, thus many memories). Because the representation formulated for impending or on-going action is, by definition, an executive representation, it is reasonable to suppose that its network contains critical neuronal nodes in the associative cortex of the frontal lobe. Further, it is reasonable to suppose that this cortex plays a fundamental role in the implementation of the integrated action (i.e., the activation and instantiation of the network). In support of these assumptions is a massive body of neuropsychological and neurophysiological evidence from the human and non-human primate. In order to mediate the execution of temporally integrated action, the association cortex of the frontal lobe, or prefrontal cortex, has to participate, concomitantly or in succession, in several cognitive operations. Perception is one of them. Any series of acts toward a goal engages neural structures at several levels of the perception-action cycle. This cycle is the circular cybernetic flow of processing of neural impulses from sensory systems to motor systems and, through the environment, back to sensory systems that controls the timing and characteristics of every action. Essential to this control is the continuous monitoring of the environment and of the changes induced in it by the organism in the pursuit of its goal. If that pursuit requires the mediation of cross-temporal contingencies between events that are novel, uncertain, or ambiguous, then the higher levels of
Cortex Forum
the cortex are engaged in the perception-action cycle. At the highest level of the executive component of the perception-action cycle is the prefrontal cortex, which is reciprocally linked through long connections with sensory association areas of posterior cortex. Attention, which is the selective allocation of neural resources to current behavior, is another of the cognitive functions that contribute to temporal integration – and thus general intelligence. Both sensory attention and executive attention come under prefrontal control in the course of temporally integrated action. Moreover, both those forms of attention have an inclusive (focus) and an exclusionary (inhibitory) component, both of these under prefrontal control. The prefrontal cortex exerts that control through its neural influences over other cortical areas (via long connections), thereby ensuring the selection among competing inputs and outputs that organized behavior necessitates (Desimone and Duncan, 1995; Fuster, 1997). A meta-analysis of neuroimaging studies of the prefrontal cortex shows that different prefrontal area participate to different degrees in a variety of temporal-integrative tasks, depending on the cognitive demands of each task (Duncan and Owen, 2000). On close analysis, it appears that the differential participation of prefrontal areas in task performance stems from a differential participation of those areas in different aspects of
229
attention. The anterior cingulate area appears mainly involved in tasks that demand the effortful focusing of attention and the resolution of conflict between alternatives; the orbital (ventral) area appears mainly involved in tasks that demand the inhibitory – exclusionary – attention control of interference. The lateral prefrontal cortex, otherwise, seems chiefly involved in the attention that is directed to internal representations of sensory character (working memory) or of motor character (executive set). In conclusion, the concept of general intelligence characterizes in operational terms, that is, in terms of performance, the joint operation of several cognitive functions, notably attention, in the temporal organization of actions. Inasmuch as those functions depend to a large degree on the physiological intervention of the prefrontal cortex, this cortex can be justifiably considered a critical neural agency of general intelligence. REFERENCES DESIMONE R and DUNCAN J. Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18: 193-222, 1995. DUNCAN J and OWEN AM. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends in NeuroSciences 23: 475-483, 2000. FUSTER JM. The Prefrontal Cortex – Anatomy Physiology, and Neuropsychology of the Frontal Lobe. Philadelphia: Lippincott-Raven, 1997. FUSTER JM. Cortex and Mind: Unifying Cognition. New York: Oxford University Press, 2003.