(Radiology. 2000;214:227-230.)
© RSNA, 2000
Functional Neuroanatomy of the Frontal Lobe Circuits1
John W. Burruss, MD,
Robin A. Hurley, MD,
Katherine H. Taber, PhD,
Ronald A. Rauch, MD,
Ralph E. Norton, MD and
L. Anne Hayman, MD
1 From the Departments of Psychiatry and Behavioral Sciences (J.W.B., R.A.H., K.H.T., L.A.H.) and Radiology (K.H.T., R.A.R., L.A.H.) and the Herbert J. Frensley Center for Imaging Research (K.H.T., L.A.H.), Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030-3498; the Psychiatry Service, Houston Veterans Affairs Medical Center, Tex (R.A.H.); and the Department of Radiology, Houston Northwest Medical Center, Tex (R.E.N.). Received January 18, 1999; revision requested March 18; revision received April 14; accepted April 22. J.W.B. and R.A.H. supported in part by the Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Tex. Address reprint requests to L.A.H. (e-mail: lhayman@bcm.tmc.edu).
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Abstract
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This article summarizes the current theories regarding the locations and functions of the three primary frontal lobe circuits. It forms the framework for structuring functional magnetic resonance imaging investigations. It can be used to assist in (a) detecting subtle lesions of the frontal circuits and (b) applying the current theories of neuropsychiatry to assess prognosis and to plan rehabilitation.
Index terms: Brain, anatomy, 131.92 • Brain, cortex, 131.92 • Brain, function, 131.91 • Brain, injuries, 131.43 • Brain, MR, 131.121411 • Special Reports
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Introduction
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There have been so many startling improvements in the anatomic display of brain structure and function that the new horizon for radiology is in interpreting what these changes mean in the clinical setting. This requires not only a detailed knowledge of anatomy but also a grasp of the relevant clinical information. The purpose of this article is to introduce the reader to the complex anatomy and theoretic implication of lesions in the frontal region.
In contrast to more unimodal areas of the brain, the prefrontal cortex, or the frontal lobe anterior to the frontal eye fields, is not involved in any concrete task. It does not smell, feel, see, or move a body part. It is this region that has allowed humans to rise above the remainder of the primate world (1). Its function is to assimilate data from other areas of the brain and formulate an understanding of past and current experiences that is used to design a plan for future action (2–4). It does not perform these actions but rather leaves them to the more caudal areas of the frontal lobes. The actual work of perception is likewise left for nonfrontal areas. This functional specialization preserves a basic division of the brain in which sensation and perception occur caudally and planning and action occur rostrally. Instinctual drives from the brainstem and diencephalon are balanced with cues from the outer world to moderate behavior into deliberate and socially appropriate form (5,6).
These archetypal functions of the prefrontal cortex are thought to be accomplished by a division of labor among three distinct circuits originating in the anterior frontal gray matter (7–9). These are the dorsolateral, orbitofrontal, and anterior cingulate portions of the frontal lobe. These circuits begin and end in the frontal cortex and travel primarily through the caudate nucleus, globus pallidus, and thalamus. To the extent that the neurons and axons in each circuit remain distinct and segregated from the others, damage to each circuit is thought to produce a distinct syndrome. However, as these pathways travel ever closer together through the subcortical nuclei, the clinical symptoms intermingle to produce a mixture of deficits. The clinical and anatomic details concerning each circuit are discussed in the following paragraphs.
The dorsolateral circuit is postulated to accomplish organization, planning, and attention. Damage to these so-called executive functions is thought to diminish the patient's ability to generate hypotheses. These patients exhibit concrete thinking; perseveration; impaired set shifting, or inability to change tasks; inability to filter, or ignore, environmental distractions; and inability to organize or plan (7,10). Other impairments include reduced verbal and design fluency, poor constructional strategies for copying complex designs, and impairment of sequential motor tasks (7). This circuit is thought to be composed primarily of four major anatomic regions (Fig 1). The cortical areas designated as Brodmann areas 9 and 10 contain the neuronal cell bodies that are the source and termination of the dorsolateral circuit. Neurons from these areas project to the dorsolateral caudate nucleus from which there is divergence into direct and poorly defined indirect pathways. These are thought to modulate each other through the balance of excitatory and inhibitory stimuli.
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Figure 1. Schematic shows the direct pathway of the dorsolateral circuit divided into four major neuronal groups designated 1-4. The anatomic locations of these structures are labeled as blue areas on images of myelin-stained brain slices in Figure 4.
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The direct course enters the lateral aspect of the dorsomedial globus pallidus externus and internus and the rostrolateral substantia nigra pars reticulata. The indirect tract, which is not illustrated in this article, synapses in the dorsal globus pallidus externa on its way to the lateral subthalamic nucleus. The two are then reunited in the globus pallidus interna and substantia nigra pars reticulata to pass through the ventral anterior and dorsomedial thalamic nuclei and return to their origin in the lateral surface of the anterior frontal lobe (7). Some of these connections may be reciprocal. At each level of this system, there is additional input from so-called open-loop afferents originating in the posterior temporal, parietal, and occipital association cortices, as well as the limbic cortex. The superior and inferior longitudinal fasciculi and the inferior occipitofrontal bundle carry impulses from these distant cortical areas and return reciprocal efferent information (11).
The orbitofrontal circuit is thought to mediate socially appropriate behavior and empathy. Lesions produce marked personality changes, including impulsivity, explosiveness, tactlessness, lability, and lack of interpersonal sensitivity (7,10). Left-sided lesions may produce depression or flat affect. This circuit is thought to be composed primarily of four major anatomic areas (Fig 2). The cortical areas designated as Brodmann areas 10 and 11 contain the neuronal cell bodies that are the source and termination of the orbitofrontal circuit. Axons from these areas project to the ventromedial caudate nucleus and diverge into a direct and a poorly delineated indirect loop, similar to those of the dorsolateral circuit.
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Figure 2. Schematic shows the direct pathway of the orbitofrontal circuit divided into four major neuronal groups designated A-D. The anatomic locations of these structures are labeled as red areas on images of myelin-stained brain slices in Figure 4.
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The direct loop enters the most medial portion of the dorsomedial globus pallidus externa and interna and rostromedial substantia nigra pars reticulata before proceeding to the ventral anterior and dorsomedial thalamic nuclei and back to the prefrontal cortex. Some of these connections may be reciprocal. The indirect pathway, which is not illustrated in this article, is thought to parallel the dorsolateral indirect pathway, with a route through the dorsal globus pallidus externa and on to the lateral subthalamic nucleus before joining the direct loop in the globus pallidus interna and substantia nigra (7). There are a number of open afferents to the lateral orbitofrontal circuit when compared with those of the dorsolateral circuit, most notably those from the temporal pole, amygdala, and ventral tegmental area (11). Again, there is reciprocation of information from the orbitofrontal cortex to these distant collateral areas.
The anterior cingulate circuit produces motivation by balancing the inhibitory input of the supplemental motor area with its own stimulus that supports wakefulness and arousal (10). The most severe deficits following damage to any of the prefrontal circuits occurs after bilateral lesions of the anterior cingulate circuit. These patients may show akinetic mutism, profound apathy, abulia (lack of motivation), and immobility. They may be incontinent; eat and drink only when fed; speak in monosyllables, if at all; and display no emotion, even when faced with pain (7). A similar, transient disability may occur in patients with unilateral lesions of the anterior cingulate circuit (12). This circuit is thought to be composed primarily of four major anatomic regions (Fig 3). The cortical area designated as Brodmann area 24 contains the neuronal cell bodies that are the source and termination of the cingulate circuit.
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Figure 3. Schematic shows the direct pathway of the anterior cingulate circuit divided into four major neuronal groups designated I-IV. The anatomic locations of these structures are labeled as yellow areas on images of myelin-stained brain slices in Figure 4.
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The subcortical connections of the anterior cingulate circuit are somewhat different from those of the dorsolateral and orbitofrontal circuits (Figs 1, 2). The anterior cingulate fibers run to the ventral, or limbic, striatum. This includes the ventromedial caudate nucleus, ventral putamen, nucleus accumbens, and olfactory tubercle. After reaching these areas, the circuit projects to the rostromedial and ventral globus pallidus and on to the dorsomedial nucleus of the thalamus. The circuit then returns to the anterior cingulate cortex. Some of these connections may be reciprocal. There is also evidence for an indirect pathway, which is not illustrated in this article, in this circuit. It projects to the globus pallidus externa and medial subthalamic nucleus before rejoining the circuit at the globus pallidus internus (7). Extracircuit input into this pathway occurs when axons from the hippocampus, amygdala, entorhinal cortex, and perirhinal cortex innervate the ventral striatum.
The locations of the proposed anatomic routes of each circuit were simplified and color coded on images of serial coronal myelin-stained brain slices (Fig 4). Anatomic structures were labeled on matched MR images obtained in vivo. It should be noted that these images illustrate only the primary pathways. They do not show the complex "open" input from, and reciprocal feedback to, noncircuit areas, nor do they include the less well defined indirect pathways (11,13).
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Figure 4a. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4b. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4c. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4d. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4e. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4f. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4g. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4h. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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Figure 4i. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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View larger version (123K):
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Figure 4j. Coronal serial, consecutive, color-coded images of myelin-stained brain slices and corresponding T2-weighted fast spin-echo magnetic resonance (MR) images obtained in vivo of the left hemisphere. The orbitofrontal circuit is shown in red, the dorsolateral in blue, and the anterior cingulate in yellow. Arabic numbers in blue zones show the predominant flow of information in the dorsolateral circuit (Fig 1). Letters in red zones show the connections of the orbitofrontal circuit (Fig 2). Roman numerals in yellow zones show the predominant connections of the anterior cingulate circuit (Fig 3). The appropriately colored dots indicate the incoming and outgoing fibers of each circuit. All MR images were acquired by using a fast spin-echo sequence with a repetition time of 6,000 msec, an echo time of 105 msec, a section thickness of 3 mm, an intersection gap of 0.6 mm, a field of view of 24 cm, a matrix of 512 x 512, and two signals acquired. Caudate = caudate nucleus. (a, b) Coronal images of the anterior frontal lobe immediately rostral to the genu of the corpus callosum. (a) The left frontal lobe cortex is the source and termination of the orbitofrontal circuit (A, red) and the dorsolateral circuit (1, blue). (b) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to a. (c, d) Coronal images of the frontal lobe at the tip of the frontal horn and genu of the corpus callosum. (c) Anterior cingulate (I, yellow), orbitofrontal (A, red), and dorsolateral (1, blue) cortices are shown in the left frontal lobe. (d) The Brodmann areas and gyri are labeled on the in vivo MR image corresponding to c. (e, f) Coronal images at the midbody of the head of the caudate nucleus. (e) The most caudal extent of the anterior cingulate (I, yellow) and orbitofrontal (A, red) cortices are shown in the left cerebral hemisphere. The left caudate nucleus is colored to indicate the dorsolateral circuit (2, blue) and the orbitofrontal circuit (B, red). The anterior cingulate circuit (II, yellow) in the ventral putamen, ventral caudate nucleus, and nucleus accumbens is also shown. (f) The Brodmann areas and deep structures are labeled on the in vivo MR image corresponding to e. (g, h) Coronal images at the caudal head of the caudate nucleus. (g) The left caudate nucleus is colored to indicate the dorsolateral (2, blue), orbitofrontal (B, red), and anterior cingulate (II, yellow) circuits. The anterior cingulate circuit (yellow) in the rostral part of the anterior perforated substance (II, olfactory tubercle) and the globus pallidus (III) are also shown. The dorsolateral circuit (3, blue) and the orbitofrontal circuit (C, red) in the globus pallidus are shown. The presence of fibers from all three circuits in the genu of the internal capsule explains why there are motor and sensory deficits, as well as "frontal lobe" symptoms, after damage to this area. (h) The important structures are labeled on the in vivo MR image corresponding to g. (i, j) Coronal images at the anterior thalamus. (i) The left hemisphere is colored to indicate the anterior cingulate fibers (yellow) in the dorsomedial thalamus (IV), globus pallidus (III), and caudate nucleus (II). The orbitofrontal circuit (red) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (D), the globus pallidus (C), and the caudate nucleus (B). The dorsolateral circuit (blue) is seen in the ventral anterior thalamic and dorsomedial thalamic nuclei (4), globus pallidus (3), and caudate nucleus (2). (j) The deep gray matter structures are labeled on the in vivo MR image corresponding to i. Dorsomedial and ventral anterior refer to the thalamic nuclei.
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In conclusion, anatomic and clinical work is continuing to uncover the complexities of the frontal lobe. At present, three main regions within the frontal lobe are hypothesized to produce distinctive neuropsychiatric abnormalities. These areas are the dorsolateral, orbitofrontal, and anterior cingulate cortices. Lesions in the pathways to and from these cortical areas can produce symptoms specifically related to these sites. However, difficulties arise when large lesions of the caudate nucleus, globus pallidus, or thalamus involve all three circuits and produce symptoms that have features of one or more of the circuits. The akinetic mutism produced by an anterior cingulate lesion will mask the less severe symptoms caused by orbitofrontal or dorsolateral lesions. The authors believe that knowledge of this detailed anatomy will assist in interpreting functional MR imaging data and predicting subtle neuropsychiatric abnormalities that can substantially affect prognosis and the rehabilitation of patients with lesions in the frontal lobe circuits.
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Acknowledgments
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The authors thank Archibald J. Fobbs, Jr, BS, curator of the National Museum of Health and Medicine, Armed Forces Institute of Pathology, Washington, DC, for providing the true coronal brain slices. Brenda Schubert provided expert assistance in preparing all of the images used in this text.
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References
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Abstract
Introduction
