Functional specialization within the dorsolateral prefrontal cortex: A review of anatomical and physiological studies of non-human primates

doi:10.1016/j.neures.2005.10.013

Neuroscience Research

Volume 54, Issue 2, February 2006, Pages 73-84

https://doi.org/10.1016/j.neures.2005.10.013 Get rights and content

Abstract

The dorsolateral prefrontal cortex (DLPFC) possesses cortico-cortical connections with the parietal and premotor cortices that are involved in visuomotor control of actions. Studies have shown that the DLPFC, especially the caudal part, has a crucial role in cognitive control of motor behavior, and that it uses spatial information in conjunction with information such as object identity, behavioral rules, and rewards. Current anatomical and physiological studies indicate that the DLPFC may not be a single entity. Anatomical studies show that preferential anatomical connections exist between subregions of the DLPFC and the parietal/premotor cortices. Physiological studies based on data obtained from monkeys performing a variety of cognitive tasks report region-specific neuronal activity within the DLPFC. In this article, I review evidence for functional segregation within the DLPFC and postulate that at least two distinct subregions, i.e., the dorsal and ventral parts, can be identified.

Introduction

A large body of evidence indicates that the prefrontal cortex plays a central role in the cognitive control of behavior (e.g., Goldman-Rakic, 1987, Goldman-Rakic, 1996, Passingham, 1993, Wise et al., 1996, Fuster, 1997, Miller, 2000, Miller and Cohen, 2001, Tanji and Hoshi, 2001, Funahashi, 2001). The dorsolateral prefrontal cortex (DLPFC) lies in the middle frontal gyrus of humans (i.e., lateral part of Brodmann's area 9/46, Brodmann, 1909) and in and around the principal sulcus of macaque monkeys (i.e., in Walker's area 46, Walker, 1940). Lesion and physiological studies show that the DLPFC has a crucial role in visuospatial control of actions (e.g., Mishkin, 1957, Kubota and Niki, 1971, Fuster and Alexander, 1971, Passingham, 1975, Funahashi et al., 1993a, Curtis and D’Esposito, 2004), as indicated by its cortico-cortical connections with the parietal and premotor cortices (Barbas and Pandya, 1987, Bates and Goldman-Rakic, 1993, Lu et al., 1994, Petrides and Pandya, 1999, Petrides and Pandya, 2002, Takada et al., 2004, Miyachi et al., 2005).

However, detailed anatomical studies show that subparts of the DLPFC receive their main input from distinct subparts of the parietal cortex (Petrides and Pandya, 1984), where each subpart represents spatial information with distinct reference frames (Mountcastle et al., 1975, Andersen et al., 1997, Colby and Goldberg, 1999, Andersen and Buneo, 2002). This raises the intriguing possibility that some functional specialization exists within the DLPFC. Here, I review anatomical and physiological evidence suggesting that this is the case and discuss its functional significance.

Section snippets

Dorsal and ventral subparts within the DLPFC and their anatomical connections

In this review, I focus on the anatomical connections of the DLPFC of the macaque monkey because this species has been most precisely studied, both anatomically and physiologically. Barbas and Pandya (1989) identified two trends in architectonic organization in the prefrontal cortex. The first originates from the periallocortex around the rostral portion of the corpus callosum and ends in the dorsal part of the DLPFC and area 8. The second originates from the periallocortex in the caudal

Integrative functions of the DLPFC

In the following two sections, I will focus on physiological studies aimed at revealing the response properties of neurons in the DLPFC. The studies most relevant to this review are summarized in Table 1. Neurons in the DLPFC have been shown to reflect spatial aspects of visual signals and motor acts (Niki and Watanabe, 1976b, Kojima and Goldman-Rakic, 1982, Funahashi et al., 1989, Funahashi et al., 1993b, Quintana and Fuster, 1992, Hasegawa et al., 1998, Chafee and Goldman-Rakic, 1998,

Distinct roles of the DLPFCd and DLPFCv in visuomotor transformation

Many physiological studies have examined the neuronal mechanisms underlying visuomotor transformation in the prefrontal cortex. An important factor characterizing the lateral prefrontal cortex is its ability to collect and represent wide varieties of information. Large numbers of neurons reflect either only object information or only spatial information, and both types are located in the prefrontal cortex (Wilson et al., 1993, Rao et al., 1997, O Scalaidhe et al., 1997, Rainer et al., 1998a,

Summary

In this review, I collected two lines of evidence for functional segregation within the DLPFC, which was originally viewed as an area specialized for spatial information processing, and I argued that at least two distinct subregions can be identified: the dorsal part (DLPFCd) and the ventral part (DLPFCv).

First, I reviewed data obtained from anatomical studies, which clearly indicate that the DLPFCd and DLPFCv can be viewed as two distinct areas based on the following five anatomical grounds:

Acknowledgments

I thank my mentors, Drs. J. Féger, K. Kurata, P.L. Strick, J. Tanji, and L. Tremblay for their excellent advice and Dr. Petrides for allowing me to reproduce his original figures. I was supported by a postdoctoral fellowship from the Japan Society for the Promotion of Science, a long-term fellowship from the Human Frontier Science Program Organization, and a Center of Excellence (COE) grant from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. Finally, I thank Drs.

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Update articleFunctional specialization within the dorsolateral prefrontal cortex: A review of anatomical and physiological studies of non-human primates

Abstract

Introduction

Section snippets

Dorsal and ventral subparts within the DLPFC and their anatomical connections

Integrative functions of the DLPFC

Distinct roles of the DLPFCd and DLPFCv in visuomotor transformation

Summary

Acknowledgments

Neuron

Neuroscience

Behav. Brain Res.

Neurosci. Res.

Behav. Brain Res.

Neurosci. Lett.

Neuron

Prog. Brain Res.

J. Neurosci. Methods

Neuron

Curr. Opin. Neurobiol.

Neuron

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands

Eur. J. Neurosci.

Intentional maps in posterior parietal cortex

Annu. Rev. Neurosci.

Multimodal representation of space in the posterior parietal cortex and its use in planning movements

Annu. Rev. Neurosci.

Alpha 2-adrenergic mechanisms in prefrontal cortex associated with cognitive decline in aged nonhuman primates

Science

Parallel processing of serial movements in prefrontal cortex

Proc. Natl. Acad. Sci. U.S.A.

Neural activity in prefrontal cortex during copying geometrical shapes. I. Single cells encode shape, sequence, and metric parameters

Exp. Brain Res.

Neural activity in prefrontal cortex during copying geometrical shapes. II. Decoding shape segments from neural ensembles

Exp. Brain Res.

Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey

J. Comp. Neurol.

Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey

J. Comp. Neurol.

Prefrontal cortex and spatial sequencing in macaque monkey

Exp. Brain Res.

Prefrontal cortex and decision making in a mixed-strategy game

Nat. Neurosci.

Prefrontal connections of medial motor areas in the rhesus monkey

J. Comp. Neurol.

Primate frontal cortex: effects of stimulus and movement

Exp. Brain Res.

Primate frontal cortex: neuronal activity following attentional versus intentional cues

Exp. Brain Res.

Vergleichende Lokalisationslehre der Groβhirnrinde

Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys

J. Comp. Neurol.

Posterior parietal cortex in rhesus monkey. II: Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe

J. Comp. Neurol.

Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task

J. Neurophysiol.

Cortical connections of the frontoparietal opercular areas in the rhesus monkey

J. Comp. Neurol.

Selectivity for the spatial and nonspatial attributes of auditory stimuli in the ventrolateral prefrontal cortex

J. Neurosci.

Space and attention in parietal cortex

Annu. Rev. Neurosci.

The sensory nature of mnemonic representation in the primate prefrontal cortex

Nat. Neurosci.

The effects of prefrontal lesions on working memory performance and theory

Cogn. Affect. Behav. Neurosci.

Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades

J. Neurophysiol.

Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate

J. Neurosci.

Cortical mechanism for the visual guidance of hand grasping movements in the monkey: a reversible inactivation study

Brain

Representation of action sequence boundaries by macaque prefrontal cortical neurons

Science

Prefrontal neuronal activity encodes spatial target representations sequentially updated after nonspatial target-shift cues

J. Neurophysiol.

Update article
Functional specialization within the dorsolateral prefrontal cortex: A review of anatomical and physiological studies of non-human primates