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The Prefrontal Cortex of the Primate: a Synopsis

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The Prefrontal Cortex of the Primate: a Synopsis Psychobiology 2000,28 (2),125-13/ The prefrontal cortex of the primate: A synopsis JOAQuiN M. FUSTER University of California, Los Angeles, California The prefrontal cortex is one of the latest regions of the neocortex to develop, in both phylogeny and ontogeny. In the primate, the prefrontal cortex is anatomically divided into three major sectors: medial, orbital (or inferior), and dorsolateral. The dorsolateral sector is the association cortex of the convex­ ity of the frontal lobe. Phylogenetically and ontogenetically, this part of the prefrontal cortex is the one to develop last and most. It is the neural substrate of the higher cognitive functions that reach their maximum development in the human brain. The-most general and distinctive function of the dorso­ lateral prefrontal cortex is the temporal organization of goal-directed actions. In the human, this role extends to the domains of speech and reasoning. Two temporally symmetrical and mutually comple­ mentary cognitive functions-one retrospective and the other prospective-support that general pre­ frontal function of temporal organization: (1) active short-term memory, also called working memory; (2) prospective or preparatory set. The dorsolateral prefrontal cortex interacts with other cortical and subcortical structures in those two time-bridging functions at the basis of the temporal organization of behavior. This article presents in summary form the most salient the cortex of the dorsal and lateral convexity ofthe ante­ empirical facts known to date on the structure and func­ rior part of the frontal lobe (Brodmann's cytoarchitectonic tions of the prefrontal cortex of the human and nonhuman area 46, and lateral parts of areas 8, 9, 10, and 11); (2) me­ primate. The available evidence is here organized around dial and cingulate, nearly flat and facing the medial sur­ a core theory of the cognitive functions ofthis cortex that face of the contralateral frontal pole (areas 12,24, and 32, has developed for the most part during the past quarter and medial parts of8, 9, 10, and 11); and (3) inferior or century, although it has long historical roots in human and orbital, slightly concave and directly over the orbit (areas simian neuropsychology. Briefly, the theory states that 13,47, and inferior parts oflO, 11, and 13). Ofthe three, the cardinal function of the prefrontal cortex is the orga­ the dorsolateral region develops last and most. It is bor­ nization of goal-directed behavior in the temporal domain. dered posteriorly by the premotor cortex (area 6); the me­ This cardinal function of ensuring the orderly and timely dial and orbital prefrontal cortices (often considered to­ execution of sequential acts extends, in the human, to gether under the designation of "orbitomedial prefrontal speech and reasoning. Different but interconnected sub­ cortex") are anterior and contiguous to the corpus callo­ divisions of the prefrontal cortex support the temporal sum and limbic structures (piriform cortex and amygdala, organization of different aspects of behavioral and cogni­ cingulate cortex, septum, and hypothalamus). Cytoarch­ tive activity. Elsewhere (Fuster, 1997) I review in greater itecturally, the posterior orbitomedial cortex is transitional, detail both the theory and the facts that support it. with features of both limbic cortex and neocortex. It is sometimes considered "paralimbic prefrontal cortex." Morphology Phylogenetically (Brodmann, 1912; Jerison, 1994) and Functional Connectivity ontogenetically (Conel, 1939-1963; Huttenlocher, 1979), All the functions of the prefrontal cortex may be con­ the prefrontal cortex develops more slowly and further sidered components of a general role of the frontal cor­ than most other parts of the brain (Figure 1). It is one of tex in the representation and execution of actions in and the last domains of the neocortex to develop. The human by the organism. The cortex of the frontal lobe, in its en­ prefrontal cortex does not reach full structural maturation tirety, can be viewed as "motor cortex" in the broadest until young adulthood. In the adult, it constitutes nearly sense of the term. That vast cortical territory represents and one third of the entirety of the neocortex. orchestrates actions in all aspects of adaptation of the The prefrontal cortex of the primate is divided into organism to its internal and external environment. To three major parts (Figure 2): (1) dorsolateral-that is, coordinate such a wide range of activities, the prefrontal cortex in particular is connected with a wide variety of cerebral structures. The prefrontal cortex is one of the Correspondence should be addressed to 1. M. Fuster, UCLA Neuro­ best connected of all neocortical regions, at least in psychiatric Institute, 760 Westwood Plaza, Los Angeles, CA 90024 terms of the number of cerebral structures with which it (e-mail: [email protected]). is connected. 125 Copyright 2000 Psychonomic Society, Inc. 126 FUSTER ~ ~ Vrf0. SQUIRREL ~ MONKEY (fjJ CAT gpr p.l. RHESUS MONKEY p.l. DOG p.S. pd. Figure 1. The prefrontal cortex (dark shading) in six animal species. Every one of the three major prefrontal regions has its gories of prefrontal function: (I) processing of information own connections-mainly reciprocal and organized topo­ on taste and olfaction; (2) regulation of the "internal mi­ logically-with the other two regions. In addition, all three lieu" of the organism-through the hypothalamus and are connected with other structures of the brain, both the viscera-in relation to drive, motivation, and affective cortical and subcortical. The most important, for their states; and (3) control of instinctual, emotional, and so­ quantity and functional significance, are the connections cial behavior. with the mediodorsal thalamus (Akert, 1964; Van Buren The cortex of the dorsolateral prefrontal convexity is & Borke, 1972); with several limbic structures, notably profusely connected with other frontal areas homolater­ the hippocampus and the amygdala (Goldman-Rakic, ally and-through the corpus callosum-contralaterally, Selemon, & Schwartz, 1984; Morecraft, Geula, & Mesu­ with the hippocampus, and with the temporal and pari­ lam, 1992; Porrino, Crane, & Goldman-Rakic, 1981); etal cortex. All this connectivity serves cognition. It sup­ with the basal ganglia (Haber, Kunishio, Mizobuchi, & ports the associative functions of executive memory and Lynd-Balta, 1995; Selemon & Goldman-Rakic, 1985); the temporal organization of behavior. Further, the dor­ and with other regions of the cerebral cortex (Pandya & solateral prefrontal areas send important efferent fibers Yeterian, 1985). to the basal ganglia, including the caudate nucleus, and The orbital and medial prefrontal areas are especially the cerebellum. This connectivity serves the motor out­ well connected with the medial and anterior nuclei of the put functions of the prefrontal cortex through structures thalamus, the prepiriform cortex, the hippocampus, the that are involved in skeletal and ocular motilities. amygdala, and the hypothalamus. This connectivity with Two large categories of connections are of special in­ the thalamus and limbic structures supports three cate- terest as they relate to the cognitive functions of the pre- PRIMATE PREFRONTAL CORTEX: A SYNOPSIS 127 DORSOLATERAL ORBITAL MEDIAL I CINGULATE Figure 2. The three major regions ofthe prefrontal cortex in the human, with eytoarchitectonie areas numer­ ated aeeording to 8rodmann's map. frontal cortex. One is the connectivity with the hippo­ Behavioral Neurophysiology campus, reciprocal with the dorsolateral as well as the Orbital and medial prefrontal areas exert inhibitory ventromedial prefrontal cortex, though apparently more control of internal drives. Monkeys and humans with le­ abundant with the latter (Amaral, 1987; Morecraft et aI., sions of the orbitomedial cortex often manifest disinhi­ 1992). The functions of hippocampus-prefrontal connec­ bition of eating, sex, and aggression, with related alter­ tions have not been established with certainty. It is rea­ ations of social and emotional behavior. Further, insofar sonable to suppose, however, that they are involved in the as impulse control is required for the concentration of at­ formation and retrieval of memory, especially motor (ex­ tention and for new and complex goal-directed behavior, ecutive) memory. the orbitomedial prefrontal cortex serves the temporal or­ The other order of connections implicated in cogni­ ganization of such behavior. This cortex helps keep in tion are those that link the prefrontal cortex with poste­ check internal impulses that may interfere with it. The in­ rior (postrolandic) regions of the neocortex (Cavada & hibitory control function of the prefrontal cortex is prob­ Goldman-Rakic, 1989; Jones & Powell, 1970; Pandya & ably mediated, in large part, by efferent connections to the Yeterian, 1985). Most probably, these connections medi­ basal ganglia (Selemon & Goldman-Rakic, 198?) and the ate not only the establishment and retrieval of executive hypothalamus (Jacobson, Butters, & Tovsky, 1978). memory but the activation of such memory for the short The dorsolateral prefrontal cortex, on the other hand, term. It appears that loops of excitatory reverberation be­ provides the cognitive support to the temporal organiza­ tween the dorsolateral prefrontal cortex and posterior tion of behavior, as well as to language and reasoning. cortical areas are probably essential in the maintenance That cognitive support consists of two basic aspects of of working
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