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Diffuse Cortical Projection Systems: Anatomical Organization and Role in Cortical Function

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Abstract

The sections in this article are:

1 An Overview of Diffuse Cortical Projection Systems
1.1 Thalamocortical Diffuse Projection Systems
1.2 Claustrocortical Projection
1.3 Amygdalocortical Projection
1.4 Magnocellular Basal Nucleus‐Cortical Projection
1.5 Hypothalamocortical Projection Systems
1.6 Mesocortical Projection System
1.7 Locus Coeruleus‐Cortical Projection
1.8 Raphe‐Cortical Projection
1.9 Pontocortical Projection Systems
2 Conclusions
2.1 Is the Concept of a Nonspecific Cortical Projection System Still Useful?
2.2 Synthesis: Role of Brain Stem, Hypothalamic, and Basal Forebrain Diffuse Cortical Projection Systems in Cortical Function
Figure 1. Figure 1.

Types and sizes of neurons in different layers of mouse somatic sensory cortex in Nissl stain (far left, layers I‐VIb) and Golgi preparation (1–17). Far right, typical appearance and distribution of “specific” cortical afferents (a, b), “unspecific or pluriareal” afferents (c, d), and corticortical association fibers (e, f) in the same material.

From Lorente de Nó .
Figure 2. Figure 2.

Distribution of retrogradely labeled neurons in cat thalamic intralaminar nuclei after injection of fast blue dye into pericruciate sensorimotor cortex (Δ in a, b, c) and nuclear yellow dye into cingulate gyrus (Δ in d, e). Retrogradely labeled neurons are shown by corresponding symbols in thalamic sections on left; double‐labeled neurons are indicated by *. Note that few intralaminar neurons in this experiment projected to both cortical fields. CeM, centre median nucleus; CL, centrolateral nucleus; CM, centromedial nucleus; fr, fasciculus retroflexus; Hb, habenular nuclei; LD, laterodorsal nucleus; LP, lateroposterior nucleus; MD, mediodorsal nucleus; Pc, paracentral nucleus; Pf, parafascicular nucleus; VB, ventrobasal nucleus; VL, ventrolateral nucleus; VM, ventromedial nucleus.

From Macchi and Bentivoglio .
Figure 3. Figure 3.

Series of oscilloscope sweeps during 7‐impulse/s electrical stimulation of cat centromedial thalamic nucleus. Stimulus is shown by dots under intracellular recordings in AD. E: recruiting response evoked in motor cortex EEG. Stimulation was not associated with any detectable change in firing of pyramidal tract neurons at some time points (A), but at other times, despite similar back‐ground firing frequency, stimulation resulted in grouping of long‐latency discharges (B). During periods of relatively low background activity, the effect of centromedial thalamic stimulation was variable (C, D) and sometimes resulted in excitatory postsynaptic potentials without neuronal discharge (D).

From Purpura et al. .
Figure 4. Figure 4.

Effect of nonspecific afferents on cortical neurons in the model of Oshima . A: distribution of neurons with excitatory (E, open columns), inhibitory (I, filled columns), disfacilitatory (DF, hatched columns), and disinhibitory (DI, stippled columns) responses plotted at varying cortical depths. B: cascade model for excitatory (open circles) and inhibitory (filled circles) neurons and synapses, relaying nonspecific afferent inputs down through cerebral cortex. C: distribution of excitatory (open circles) and inhibitory (filled circles) terminals from nonspecific afferent fibers. Arrows in B and C indicate direction of information flow.

From Oshima . In: Motor Control Mechanisms in Health and Disease, © 1983, Raven Press, New York.
Figure 5. Figure 5.

Distribution of retrogradely labeled neurons in cat claustrum after injections of nuclear yellow dye (NY) into pericruciate cortex (a, b) and fast blue dye (FB) into occipital cortex (c, d). Singly and doubly retrogradely labeled neurons are shown on figure. Note anteroposterior topographical ordering of neurons projecting to these cortical areas and that only one cell was labeled from both injection sites.

From Macchi et al. .
Figure 6. Figure 6.

A, B: peristimulus firing‐rate histograms from 2 different pyramidal tract neurons during single‐shock (130 μA, 0.2 ms) stimulation of claustrum at times marked by arrows. Note that neuron in A was inhibited but that neuron in B showed brief excitation prior to inhibitory interval. C: location of stimulating electrode is shown by the lesion in claustrum.

From Salerno et al. .
Figure 7. Figure 7.

Proposed organization of projection from magnocellular basal nucleus to human cerebral cortex. Neurons in the medial septal (MS) and diagonal band (DB) nuclei and in the medial part of the nucleus basalis (NB) give rise to a medial pathway. One branch of this pathway runs through the fornix to innervate the hippocampal formation (HIP), whereas the other courses over genu of corpus callosum to enter the cingulate bundle, from which it distributes to innervate medial cortical areas. A lateral pathway originates in lateral parts of the nucleus basalis and runs laterally into the external capsule from which it distributes to lateral cortical areas.

Figure 8. Figure 8.

Integrated firing rates for visual cortical neuron in cat exposed to optimally oriented bar of light moving across its visual field at 10°/s (left) or 20°/s (right) before (upper histograms) or during (lower histograms) iontophoretic application of acetylcholine. Note that directional selectivity is enhanced (relative heights of peak firing rate in 2 directions is more unequal) by application of acetylcholine while background firing rate is suppressed.

From Sillito and Kemp .
Figure 9. Figure 9.

Organization of the hypothalamic projection to rat cerebral cortex. Size of box from which each projection arises is roughly proportional to the number of neurons participating in the projection. The tuberal lateral hypothalamus (LHAt, upper left) projects to the entire ipsilateral cortex but shows little evidence of topographical organization. The posterior lateral hypothalamus (LHAp, lower left) also innervates the entire ipsilateral cortical mantle. The latter projection arises in a topographical manner, with medial cortical areas receiving input from the medial part of the cell group and lateral cortical areas receiving afferents from the lateral part. The total number of lateral hypothalamic neurons contributing to these two cortical projections is ∼20% greater than the number in the magnocellular basal nucleus. By contrast, relatively few cortical projection neurons are found in fields of Forel (FF) and the tuber‐omammillary nucleus (TMN). The former is topographically organized in medial‐to‐lateral axis and innervates a rather restricted region, primarily confined to frontal cortex. The latter cell group, on each side of the brain, innervates entire cortex of both hemispheres but does not appear to arise in a topographical manner. Relatively minor crossed projections from lateral hypothalamic cell groups have been omitted for clarity.

From Saper .
Figure 10. Figure 10.

Origins and terminal distribution of mesocortical projection system. Three pools of neurons organized in medial‐to‐lateral topographical order primarily innervate different cortical fields. Most medially located group of cells innervates pregenual (pg), supragenual (sg), and posterior cingulate (pc) areas; the intermediate group projects to prefrontal (pf) and suprarhinal (insular) and perirhinal (sr/p) areas; and the lateral group innervates entorhinal (er) cortex. Laminar and areal distribution of dopaminergic terminals in glyoxylic acid histofluorescence preparations is diagrammatically shown at left.

From Loughlin and Fallon , © 1984, with permission from Pergamon Press, Ltd.
Figure 11. Figure 11.

Interaction of thalamic and ventral tegmental stimulation on the activity of frontal cortical neurons. A, B: top, 10 superimposed oscilloscope sweeps; bottom, dot raster display of consecutive trials. Stimulation of the mediodorsal thalamic nucleus at 10 Hz (A) produces excitatory responses with fixed latency but inhibits intertrial firing of the cortical neuron. Stimulation of the ventral tegmental area (B) at 1 impulse/s causes prolonged period of inhibition. C, D: dot raster displays generated by stimulating the mediodorsal thalamic nucleus (StMD) at indicated time after stimulation of the ventral tegmental area (StVMT). In normal rat (left), stimulation of the ventral tegmental area within 10 ms prior to mediodorsal thalamic stimulus prevents excitatory effect of the latter. In 6‐hydroxydopamine treated animal (right), in which mesocortical dopaminergic innervation has been destroyed, this inhibitory interaction is not seen.

From Ferron et al. .
Figure 12. Figure 12.

Trajectory of noradrenergic fibers in rat from locus coeruleus to neocortex. Fibers innervating medial cortical areas (M) pass through the septum, over the genu of the corpus callosum, and either run forward into the medial frontal lobe or caudally in the cingulate bundle. Fibers projecting to lateral cortical areas (L) run laterally from the substantia innominata into the external capsule underlying the insular cortex and then run caudally through the external capsule to innervate other lateral cortical areas.

From Morrison et al. . Copyright 1979 by the American Association for the Advancement of Science.
Figure 13. Figure 13.

Appearance of dopamine β‐hydroxylase immunoreactive fibers in rat somatic sensory cortex. Right, scale indicates distance in microns from the pial surface. Roman numerals refer to cortical laminae. A: higher magnification of upper four layers in B. Note predominantly horizontal orientation of fibers in deep part of layer VI and in layer I, almost random orientation in layers IV, V, and superficial layer VI, and radial orientation in layers II and III. Varicose nature of fibers and abrupt changes in orientation at borders of layers I and II and layers III and IV are apparent at higher magnification.

From Morrison et al. .
Figure 14. Figure 14.

Three‐epoch series from polygraph recording of the firing of locus coeruleus neuron during different stages of the wake‐sleep cycle. First epoch, firing of locus coeruleus neuron slows as animal passes from waking (low‐amplitude, high‐frequency EEG) to slow‐wave sleep (high‐amplitude, periodic, low‐frequency EEG). Second epoch, as animal passes from slow‐wave sleep to desynchronized sleep (low‐amplitude, high‐frequency EEG; nearly absent EMG activity) at up arrow, locus coeruleus unit becomes silent. Third epoch, unit begins firing coincident with onset of waking EEG (down arrow) but prior to return of waking EMG activity (*). Upper panels show analog discharge traces from the unit during one transition of waking to slow‐wave sleep (W & SWS) and one period of desynchronized sleep (PS). The dots indicate that the spike met the waveform discriminator criteria and would have been included in integrated activity in lower recordings.

From Aston‐Jones and Bloom .
Figure 15. Figure 15.

Series of integrated discharge‐rate histograms from a neuron in cat visual cortex obtained during movement of bar of light of preferred orientation across peripheral field of unit in preferred (forward) and reverse (backward) directions. During iontophoretic application of norepinephrine (second row), stimulus‐specific firing of unit is reduced, but background firing rate is almost zero. Net result is an increase in signal‐to‐noise ratio. In third row, recovery from suppressing effect of norepinephrine was incomplete.

From Kasamatsu and Heggelund .
Figure 16. Figure 16.

Differences in laminar pattern of innervation of primary visual cortex of squirrel monkey and cynomolgus monkey by serotonergic (5‐HT) fibers and noradrenergic (NA) fibers. Note that although overall pattern is similar, density of fibers and sublaminar variation is greater in cynomolgus monkey.

From Morrison et al. .
Figure 17. Figure 17.

Series of oscilloscope tracings recorded intracellulary from neurons in locus coeruleus, mesencephalic trigeminal nucleus (mes V), and dorsal raphe nucleus. In upper trace, locus coeruleus neuron fires burst of action potentials when the animal's toe is pinched (arrows); this is followed by a period of hyperpolarization in which there is suppression of firing lasting 3 s. In middle trace, mesencephalic trigeminal neuron fires a burst of action potentials during displacement of mandible (arrows) but shows no afterhyper‐polarization. In lower trace, dorsal raphe neuron shows slow, regular, spontaneous firing pattern. Each action potential is followed by afterhyperpolarization, then gradual interspike depolarization, which constitutes “pacemaker” potential and may account for slow, regular firing rates of dorsal raphe neurons.

From Aghajanian and VanderMaelen .
Figure 18. Figure 18.

Section through rat pons illustrating distribution of choline acetyltransferase immunoreactive neurons in peduculopontine (PPT) and laterodorsal tegmental (LDT) nuclei in rat brain. Note that 2 groups, which consist of similar‐appearing neurons and which project to many of the same terminal fields, are continuous along the ventrolateral margin of central gray matter (CG). CUN, cuneiform nucleus; DR, dorsal raphe nucleus; INC, inferior colliculus; SCP, superior cerebellar peduncle; SCR, superior central raphe nucleus; VTN, ventral tegmental nucleus.

Adapted from Armstrong et al. .
Figure 19. Figure 19.

Series of sections from 2 rat brains illustrating reciprocity of parabrachial projection to cerebral cortex. In experiment R21 (left), an injection of wheat germ agglutinin‐conjugated horseradish peroxidase, a retrograde tracer, was placed into the parabrachial nucleus (F). In experiment LC1 (right), an injection of tritiated amino acids, used as anterograde tracer, was made into the same area. Distribution of retrogradely labeled cells (triangles in R21, AF) and anterogradely labeled fibers (small dots in LC1, GL) in these 2 experiments was nearly identical: both were densest in layer V of insular, posteroventral infralimbic, and lateral frontal areas.

From Saper .


Figure 1.

Types and sizes of neurons in different layers of mouse somatic sensory cortex in Nissl stain (far left, layers I‐VIb) and Golgi preparation (1–17). Far right, typical appearance and distribution of “specific” cortical afferents (a, b), “unspecific or pluriareal” afferents (c, d), and corticortical association fibers (e, f) in the same material.

From Lorente de Nó .


Figure 2.

Distribution of retrogradely labeled neurons in cat thalamic intralaminar nuclei after injection of fast blue dye into pericruciate sensorimotor cortex (Δ in a, b, c) and nuclear yellow dye into cingulate gyrus (Δ in d, e). Retrogradely labeled neurons are shown by corresponding symbols in thalamic sections on left; double‐labeled neurons are indicated by *. Note that few intralaminar neurons in this experiment projected to both cortical fields. CeM, centre median nucleus; CL, centrolateral nucleus; CM, centromedial nucleus; fr, fasciculus retroflexus; Hb, habenular nuclei; LD, laterodorsal nucleus; LP, lateroposterior nucleus; MD, mediodorsal nucleus; Pc, paracentral nucleus; Pf, parafascicular nucleus; VB, ventrobasal nucleus; VL, ventrolateral nucleus; VM, ventromedial nucleus.

From Macchi and Bentivoglio .


Figure 3.

Series of oscilloscope sweeps during 7‐impulse/s electrical stimulation of cat centromedial thalamic nucleus. Stimulus is shown by dots under intracellular recordings in AD. E: recruiting response evoked in motor cortex EEG. Stimulation was not associated with any detectable change in firing of pyramidal tract neurons at some time points (A), but at other times, despite similar back‐ground firing frequency, stimulation resulted in grouping of long‐latency discharges (B). During periods of relatively low background activity, the effect of centromedial thalamic stimulation was variable (C, D) and sometimes resulted in excitatory postsynaptic potentials without neuronal discharge (D).

From Purpura et al. .


Figure 4.

Effect of nonspecific afferents on cortical neurons in the model of Oshima . A: distribution of neurons with excitatory (E, open columns), inhibitory (I, filled columns), disfacilitatory (DF, hatched columns), and disinhibitory (DI, stippled columns) responses plotted at varying cortical depths. B: cascade model for excitatory (open circles) and inhibitory (filled circles) neurons and synapses, relaying nonspecific afferent inputs down through cerebral cortex. C: distribution of excitatory (open circles) and inhibitory (filled circles) terminals from nonspecific afferent fibers. Arrows in B and C indicate direction of information flow.

From Oshima . In: Motor Control Mechanisms in Health and Disease, © 1983, Raven Press, New York.


Figure 5.

Distribution of retrogradely labeled neurons in cat claustrum after injections of nuclear yellow dye (NY) into pericruciate cortex (a, b) and fast blue dye (FB) into occipital cortex (c, d). Singly and doubly retrogradely labeled neurons are shown on figure. Note anteroposterior topographical ordering of neurons projecting to these cortical areas and that only one cell was labeled from both injection sites.

From Macchi et al. .


Figure 6.

A, B: peristimulus firing‐rate histograms from 2 different pyramidal tract neurons during single‐shock (130 μA, 0.2 ms) stimulation of claustrum at times marked by arrows. Note that neuron in A was inhibited but that neuron in B showed brief excitation prior to inhibitory interval. C: location of stimulating electrode is shown by the lesion in claustrum.

From Salerno et al. .


Figure 7.

Proposed organization of projection from magnocellular basal nucleus to human cerebral cortex. Neurons in the medial septal (MS) and diagonal band (DB) nuclei and in the medial part of the nucleus basalis (NB) give rise to a medial pathway. One branch of this pathway runs through the fornix to innervate the hippocampal formation (HIP), whereas the other courses over genu of corpus callosum to enter the cingulate bundle, from which it distributes to innervate medial cortical areas. A lateral pathway originates in lateral parts of the nucleus basalis and runs laterally into the external capsule from which it distributes to lateral cortical areas.



Figure 8.

Integrated firing rates for visual cortical neuron in cat exposed to optimally oriented bar of light moving across its visual field at 10°/s (left) or 20°/s (right) before (upper histograms) or during (lower histograms) iontophoretic application of acetylcholine. Note that directional selectivity is enhanced (relative heights of peak firing rate in 2 directions is more unequal) by application of acetylcholine while background firing rate is suppressed.

From Sillito and Kemp .


Figure 9.

Organization of the hypothalamic projection to rat cerebral cortex. Size of box from which each projection arises is roughly proportional to the number of neurons participating in the projection. The tuberal lateral hypothalamus (LHAt, upper left) projects to the entire ipsilateral cortex but shows little evidence of topographical organization. The posterior lateral hypothalamus (LHAp, lower left) also innervates the entire ipsilateral cortical mantle. The latter projection arises in a topographical manner, with medial cortical areas receiving input from the medial part of the cell group and lateral cortical areas receiving afferents from the lateral part. The total number of lateral hypothalamic neurons contributing to these two cortical projections is ∼20% greater than the number in the magnocellular basal nucleus. By contrast, relatively few cortical projection neurons are found in fields of Forel (FF) and the tuber‐omammillary nucleus (TMN). The former is topographically organized in medial‐to‐lateral axis and innervates a rather restricted region, primarily confined to frontal cortex. The latter cell group, on each side of the brain, innervates entire cortex of both hemispheres but does not appear to arise in a topographical manner. Relatively minor crossed projections from lateral hypothalamic cell groups have been omitted for clarity.

From Saper .


Figure 10.

Origins and terminal distribution of mesocortical projection system. Three pools of neurons organized in medial‐to‐lateral topographical order primarily innervate different cortical fields. Most medially located group of cells innervates pregenual (pg), supragenual (sg), and posterior cingulate (pc) areas; the intermediate group projects to prefrontal (pf) and suprarhinal (insular) and perirhinal (sr/p) areas; and the lateral group innervates entorhinal (er) cortex. Laminar and areal distribution of dopaminergic terminals in glyoxylic acid histofluorescence preparations is diagrammatically shown at left.

From Loughlin and Fallon , © 1984, with permission from Pergamon Press, Ltd.


Figure 11.

Interaction of thalamic and ventral tegmental stimulation on the activity of frontal cortical neurons. A, B: top, 10 superimposed oscilloscope sweeps; bottom, dot raster display of consecutive trials. Stimulation of the mediodorsal thalamic nucleus at 10 Hz (A) produces excitatory responses with fixed latency but inhibits intertrial firing of the cortical neuron. Stimulation of the ventral tegmental area (B) at 1 impulse/s causes prolonged period of inhibition. C, D: dot raster displays generated by stimulating the mediodorsal thalamic nucleus (StMD) at indicated time after stimulation of the ventral tegmental area (StVMT). In normal rat (left), stimulation of the ventral tegmental area within 10 ms prior to mediodorsal thalamic stimulus prevents excitatory effect of the latter. In 6‐hydroxydopamine treated animal (right), in which mesocortical dopaminergic innervation has been destroyed, this inhibitory interaction is not seen.

From Ferron et al. .


Figure 12.

Trajectory of noradrenergic fibers in rat from locus coeruleus to neocortex. Fibers innervating medial cortical areas (M) pass through the septum, over the genu of the corpus callosum, and either run forward into the medial frontal lobe or caudally in the cingulate bundle. Fibers projecting to lateral cortical areas (L) run laterally from the substantia innominata into the external capsule underlying the insular cortex and then run caudally through the external capsule to innervate other lateral cortical areas.

From Morrison et al. . Copyright 1979 by the American Association for the Advancement of Science.


Figure 13.

Appearance of dopamine β‐hydroxylase immunoreactive fibers in rat somatic sensory cortex. Right, scale indicates distance in microns from the pial surface. Roman numerals refer to cortical laminae. A: higher magnification of upper four layers in B. Note predominantly horizontal orientation of fibers in deep part of layer VI and in layer I, almost random orientation in layers IV, V, and superficial layer VI, and radial orientation in layers II and III. Varicose nature of fibers and abrupt changes in orientation at borders of layers I and II and layers III and IV are apparent at higher magnification.

From Morrison et al. .


Figure 14.

Three‐epoch series from polygraph recording of the firing of locus coeruleus neuron during different stages of the wake‐sleep cycle. First epoch, firing of locus coeruleus neuron slows as animal passes from waking (low‐amplitude, high‐frequency EEG) to slow‐wave sleep (high‐amplitude, periodic, low‐frequency EEG). Second epoch, as animal passes from slow‐wave sleep to desynchronized sleep (low‐amplitude, high‐frequency EEG; nearly absent EMG activity) at up arrow, locus coeruleus unit becomes silent. Third epoch, unit begins firing coincident with onset of waking EEG (down arrow) but prior to return of waking EMG activity (*). Upper panels show analog discharge traces from the unit during one transition of waking to slow‐wave sleep (W & SWS) and one period of desynchronized sleep (PS). The dots indicate that the spike met the waveform discriminator criteria and would have been included in integrated activity in lower recordings.

From Aston‐Jones and Bloom .


Figure 15.

Series of integrated discharge‐rate histograms from a neuron in cat visual cortex obtained during movement of bar of light of preferred orientation across peripheral field of unit in preferred (forward) and reverse (backward) directions. During iontophoretic application of norepinephrine (second row), stimulus‐specific firing of unit is reduced, but background firing rate is almost zero. Net result is an increase in signal‐to‐noise ratio. In third row, recovery from suppressing effect of norepinephrine was incomplete.

From Kasamatsu and Heggelund .


Figure 16.

Differences in laminar pattern of innervation of primary visual cortex of squirrel monkey and cynomolgus monkey by serotonergic (5‐HT) fibers and noradrenergic (NA) fibers. Note that although overall pattern is similar, density of fibers and sublaminar variation is greater in cynomolgus monkey.

From Morrison et al. .


Figure 17.

Series of oscilloscope tracings recorded intracellulary from neurons in locus coeruleus, mesencephalic trigeminal nucleus (mes V), and dorsal raphe nucleus. In upper trace, locus coeruleus neuron fires burst of action potentials when the animal's toe is pinched (arrows); this is followed by a period of hyperpolarization in which there is suppression of firing lasting 3 s. In middle trace, mesencephalic trigeminal neuron fires a burst of action potentials during displacement of mandible (arrows) but shows no afterhyper‐polarization. In lower trace, dorsal raphe neuron shows slow, regular, spontaneous firing pattern. Each action potential is followed by afterhyperpolarization, then gradual interspike depolarization, which constitutes “pacemaker” potential and may account for slow, regular firing rates of dorsal raphe neurons.

From Aghajanian and VanderMaelen .


Figure 18.

Section through rat pons illustrating distribution of choline acetyltransferase immunoreactive neurons in peduculopontine (PPT) and laterodorsal tegmental (LDT) nuclei in rat brain. Note that 2 groups, which consist of similar‐appearing neurons and which project to many of the same terminal fields, are continuous along the ventrolateral margin of central gray matter (CG). CUN, cuneiform nucleus; DR, dorsal raphe nucleus; INC, inferior colliculus; SCP, superior cerebellar peduncle; SCR, superior central raphe nucleus; VTN, ventral tegmental nucleus.

Adapted from Armstrong et al. .


Figure 19.

Series of sections from 2 rat brains illustrating reciprocity of parabrachial projection to cerebral cortex. In experiment R21 (left), an injection of wheat germ agglutinin‐conjugated horseradish peroxidase, a retrograde tracer, was placed into the parabrachial nucleus (F). In experiment LC1 (right), an injection of tritiated amino acids, used as anterograde tracer, was made into the same area. Distribution of retrogradely labeled cells (triangles in R21, AF) and anterogradely labeled fibers (small dots in LC1, GL) in these 2 experiments was nearly identical: both were densest in layer V of insular, posteroventral infralimbic, and lateral frontal areas.

From Saper .
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Clifford B. Saper. Diffuse Cortical Projection Systems: Anatomical Organization and Role in Cortical Function. Compr Physiol 2011, Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain: 169-210. First published in print 1987. doi: 10.1002/cphy.cp010506