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Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Essence of Prefrontal Function: Regulation of Behavior by Representational Knowledge
1.1 Subdivisions of Prefrontal Cortex
1.2 Global Nature of Prefrontal Syndrome in Humans
1.3 Animal Model for Prefrontal Function in Humans
1.4 Delayed‐Response Tests and Varying Interpretations of Their Functional Significance
1.5 Distractability and Perseveration: Secondary Consequences of Basic Defect in Representational Memory
1.6 Representational Memory in Wisconsin Card Sort and Other Diagnostic Tests of Prefrontal Function in Humans
1.7 Localization of Delayed‐Response Function: Principal Sulcus
1.8 Circuit Basis of Visuospatial Functions
2 Accessing and “On‐Line” Processing of Representations in Visuospatial Domain: Parietal‐Prefrontal Connections
2.1 Visuospatial Representational Memory in Humans
2.2 Spatial‐Mnemonic Nature of Delayed‐Response Deficit: Domain‐Specific Memory Loss
2.3 Topography of Representational Memory in Prefrontal Cortex
2.4 Electrophysiological Evidence of Spatial‐Mnemonic Processes in Principal Sulcus
2.5 Parietal‐Prefrontal Connectivity
2.6 Columnar and Laminar Framework for Feedforward and Feedback Mechanisms
2.7 Functional Significance of Parietal‐Prefrontal Collaboration
3 Long‐Term Memory and “Off‐Line” Processing: Prefrontal‐Limbic Connections
3.1 Role of Hippocampus in Spatial Memory
3.2 Multiple Connections Between Principal Sulcus and Hippocampal Formation
3.3 Quadripartite Neural Network: Parietal‐Temporal‐Cingulate‐Prefrontal Circuit
3.4 Limbic Contribution to Spatial Memory
4 Response Initiation and Inhibition: Projections to Striatum, Tectum, Thalamus, and Premotor Cortex
4.1 Motor‐Control Functions of Prefrontal Cortex
4.2 Cortical‐Striatal Pathway and Related Feedback Loops
4.3 Cortical‐Tectal Pathway
4.4 Thalamic‐Cortical Systems
4.5 Prefrontal‐Premotor Connections: Anterior Supplementary Motor Cortex Relays
4.6 Functional Speculations
5 Modulatory Mechanisms: Brain Stem Catecholamine Projections
5.1 Activation of Cognitive Machinery
5.2 Concentration and Synthesis of Catecholamines in Primate Cortex
5.3 Brain Stem Innervation of Prefrontal Cortex
5.4 Delayed‐Response Deficits and Recovery Produced by Catecholamine Loss and Replacement in Prefrontal Cortex
5.5 Circuit Basis for Neuromodulation in Principal Sulcus
6 Multiple Subsystems of Prefrontal Cortex: Unity or Diversity of Function
6.1 Unity or Diversity of Prefrontal Function
6.2 Frontal Eye Fields
6.3 Inferior Convexity
6.4 Orbital Prefrontal Cortices
6.5 Problem of Integration
7 Diseases Affecting Prefrontal Cortex
7.1 Schizophrenia: Loss of Corticocortical Processing and Regulation of Behavior by Representational Knowledge
7.2 Wernicke‐Korsakoff Syndrome: Loss of Thalamocortical and Brain Stem Modulatory Mechanisms
7.3 Huntington's Chorea and Parkinson's Disease: Loss of Prefrontal‐Striatal Mechanisms and Initiation or Inhibition of Motor Response
7.4 Overview of Neurobiology of Disease
8 Summary
Figure 1. Figure 1.

Lateral view of human and monkey cerebral cortex. Human prefrontal divisions based on Brodmann's (1929) cytoarchitectonic map; macaque prefrontal divisions based on Walker's (1940) cytoarchitectonic map. Stippling, area 46.

Figure 2. Figure 2.

Three components of spatial delayed‐response trial. Top, monkey sees experimenter bait one food well (cue) before both wells are covered. Middle, opaque screen is lowered for one or more seconds (delay). Bottom, screen is raised and monkey chooses one well by displacing its cover.

Figure 3. Figure 3.

Results from 3 monkeys tested on delayed eye‐movement task. Correct‐performance percentage is shown along axes drawn through central fixation point; 8 positions of target stimuli are located at constant distance (13°) from fixation point. Thick line, performance at shortest delay (usually 0.5–1.5 s); thin line, performance at 3‐s delay; dashed line, performance at 6‐s delay. A, B: monkey with sequential lesions of middle third of principal sulcus. A: monkey exhibits marked deficit in lower left visual field and milder deficit in lower right visual field at all delays. B: lower right‐field deficit is much more severe after animal was subjected to prefrontal lesion of middle principal sulcus in left hemisphere. C: monkey with unilateral lesion of entire principal sulcus showed loss in ability to remember targets in both upper and lower contralateral fields at 6‐s delay, though performance was accurate at shorter delays. D: monkey with lesion confined to posterior portion of principal sulcus and anterior bank of arcuate sulcus showed severe deficit in contralateral upper visual field at all delays. All 3 monkeys performed without difficulty in all locations within visual field as long as visual target was present at time of response.

Figure 4. Figure 4.

Neuronal activity of cell recorded near principal sulcus during multiple trials of delayed‐response eye‐movement task. Unit activity rasters are aligned to cue, delay, and response periods of task. A: when target was presented 13° right of fixation, cell was activated during delay; B: when target was presented 13° left of fixation, cell did not increase base‐line firing rate during delay. Firing rate did increase slightly after eyes moved left. FP, fixation point.

Figure 5. Figure 5.

Subarea‐to‐subarea interconnections of parietal and prefrontal cortex that may be essential for spatial memory. Medial parietal cortex (7m) is interconnected with dorsal bank and rim of caudal principal sulcus (PS); area 7a is interconnected with fundus and lower portion of each bank; area 7b is interconnected with upper portion and rim of ventral bank of PS; area 7ip in caudal bank of intraparietal sulcus (IpS) is connected with anterior bank of the arcuate sulcus (ArcS).

Figure 6. Figure 6.

Simplified circuit diagram of terminal fields of parietal associational fibers (light stipple) and callosal fibers (dark stipple) in layers I and IV of adjacent columns in principal sulcus. Callosal (dark triangles) and associational (light triangles) projection neurons send axons to contralateral prefrontal cortex and to ipsilateral parietal cortex, respectively. Callosal neurons are more concentrated in columns defined by callosal afferents, and associational neurons are more concentrated in columns receiving dense association‐fiber input. Layer III contains ∼80% of callosal and associational projection neurons; 20% are distributed in layers V and VI.

Data from Schwartz and Goldman‐Rakic
Figure 7. Figure 7.

Prefrontal connections with parahippocampal gyrus (areas TH and TF), entorhinal cortex (area 28), presubiculum (PSUB), and caudomedial lobule (CML) based on cases in which principal sulcus was implanted with horseradish peroxidase gel that labels both efferents and afferents to injected area. B, C: coronal sections cut through two levels (b, c in A) showing terminal fields of anterogradely transported label from injection site (stippled); reciprocal projections revealed by retrograde transport studies are not shown but arise from (roughly) same areas. CA, Ammon's horn; CC, corpus callosum; CING, cingulate gyrus; CS, collateral sulcus; DG, dentate gyrus; OTS, occipitotemporal sulcus; PS, principal sulcus; RS, retrosplenial cortex.

Adapted from Goldman‐Rakic et al.
Figure 8. Figure 8.

Diagram of third‐party connections of posterior parietal and caudal principal sulcus based on double‐label studies in which one anterograde tracer was injected into prefrontal cortex and another into parietal cortex of same animal. Superimposition of adjacent sections shows these areas projecting to different layers of the same column or to adjacent columns in designated target areas (see insert). Major targets of prefrontal and parietal projections are limbic areas on medial surface and opercular and superior temporal cortices on lateral surface. Stippling, intraparietal sulcus (IPS) and principal sulcus (PS).

Figure 9. Figure 9.

Major motor‐control efferent pathways. A, corticocortical pathway: principal sulcus (PS) to supplementary motor cortex (SMA); B, cortical‐striatal pathway: PS to caudate nucleus (Cd); C, cortical‐tectal pathway: PS to intermediate and deep layers of superior colliculus (SC).

Data from Goldman and Nauta , Selemon and Goldman‐Rakic ; M. L. Jouandet and P. S. Goldman‐Rakic, unpublished observations
Figure 10. Figure 10.

Topographical relationships between ventral anterior nucleus, mediodorsal nucleus, and medial pulvinar nucleus and selected cytoarchitectonic subdivisions of prefrontal cortex. Each subdivision projects to only one cytoarchitectonic area of cortex; each cortical area receives unique multiple thalamic input.

From Goldman‐Rakic and Porrino
Figure 11. Figure 11.

Prefrontal interconnections with several brain stem monoaminergic cell groups thought to be involved in activational processes. BC, brachium conjunctivum; CS, central superior nucleus; DR, dorsal raphe; LC, locus coeruleus; nST, solitary tract nucleus; PS, principal sulcus; PY, pyramids.

Data from Arnsten and Goldman‐Rakic and Porrino and Goldman‐Rakic
Figure 12. Figure 12.

Walker's cytoarchitectonic map of monkey prefrontal cortex. Lateral and ventral views show approximate locations of frontal eye fields (areas 8A, 45), inferior prefrontal convexity (area 12), and posterior orbital prefrontal cortex (areas 13, 14). AS, arcuate sulcus; CS, central sulcus; OT, optic tract; PS, principal sulcus.



Figure 1.

Lateral view of human and monkey cerebral cortex. Human prefrontal divisions based on Brodmann's (1929) cytoarchitectonic map; macaque prefrontal divisions based on Walker's (1940) cytoarchitectonic map. Stippling, area 46.



Figure 2.

Three components of spatial delayed‐response trial. Top, monkey sees experimenter bait one food well (cue) before both wells are covered. Middle, opaque screen is lowered for one or more seconds (delay). Bottom, screen is raised and monkey chooses one well by displacing its cover.



Figure 3.

Results from 3 monkeys tested on delayed eye‐movement task. Correct‐performance percentage is shown along axes drawn through central fixation point; 8 positions of target stimuli are located at constant distance (13°) from fixation point. Thick line, performance at shortest delay (usually 0.5–1.5 s); thin line, performance at 3‐s delay; dashed line, performance at 6‐s delay. A, B: monkey with sequential lesions of middle third of principal sulcus. A: monkey exhibits marked deficit in lower left visual field and milder deficit in lower right visual field at all delays. B: lower right‐field deficit is much more severe after animal was subjected to prefrontal lesion of middle principal sulcus in left hemisphere. C: monkey with unilateral lesion of entire principal sulcus showed loss in ability to remember targets in both upper and lower contralateral fields at 6‐s delay, though performance was accurate at shorter delays. D: monkey with lesion confined to posterior portion of principal sulcus and anterior bank of arcuate sulcus showed severe deficit in contralateral upper visual field at all delays. All 3 monkeys performed without difficulty in all locations within visual field as long as visual target was present at time of response.



Figure 4.

Neuronal activity of cell recorded near principal sulcus during multiple trials of delayed‐response eye‐movement task. Unit activity rasters are aligned to cue, delay, and response periods of task. A: when target was presented 13° right of fixation, cell was activated during delay; B: when target was presented 13° left of fixation, cell did not increase base‐line firing rate during delay. Firing rate did increase slightly after eyes moved left. FP, fixation point.



Figure 5.

Subarea‐to‐subarea interconnections of parietal and prefrontal cortex that may be essential for spatial memory. Medial parietal cortex (7m) is interconnected with dorsal bank and rim of caudal principal sulcus (PS); area 7a is interconnected with fundus and lower portion of each bank; area 7b is interconnected with upper portion and rim of ventral bank of PS; area 7ip in caudal bank of intraparietal sulcus (IpS) is connected with anterior bank of the arcuate sulcus (ArcS).



Figure 6.

Simplified circuit diagram of terminal fields of parietal associational fibers (light stipple) and callosal fibers (dark stipple) in layers I and IV of adjacent columns in principal sulcus. Callosal (dark triangles) and associational (light triangles) projection neurons send axons to contralateral prefrontal cortex and to ipsilateral parietal cortex, respectively. Callosal neurons are more concentrated in columns defined by callosal afferents, and associational neurons are more concentrated in columns receiving dense association‐fiber input. Layer III contains ∼80% of callosal and associational projection neurons; 20% are distributed in layers V and VI.

Data from Schwartz and Goldman‐Rakic


Figure 7.

Prefrontal connections with parahippocampal gyrus (areas TH and TF), entorhinal cortex (area 28), presubiculum (PSUB), and caudomedial lobule (CML) based on cases in which principal sulcus was implanted with horseradish peroxidase gel that labels both efferents and afferents to injected area. B, C: coronal sections cut through two levels (b, c in A) showing terminal fields of anterogradely transported label from injection site (stippled); reciprocal projections revealed by retrograde transport studies are not shown but arise from (roughly) same areas. CA, Ammon's horn; CC, corpus callosum; CING, cingulate gyrus; CS, collateral sulcus; DG, dentate gyrus; OTS, occipitotemporal sulcus; PS, principal sulcus; RS, retrosplenial cortex.

Adapted from Goldman‐Rakic et al.


Figure 8.

Diagram of third‐party connections of posterior parietal and caudal principal sulcus based on double‐label studies in which one anterograde tracer was injected into prefrontal cortex and another into parietal cortex of same animal. Superimposition of adjacent sections shows these areas projecting to different layers of the same column or to adjacent columns in designated target areas (see insert). Major targets of prefrontal and parietal projections are limbic areas on medial surface and opercular and superior temporal cortices on lateral surface. Stippling, intraparietal sulcus (IPS) and principal sulcus (PS).



Figure 9.

Major motor‐control efferent pathways. A, corticocortical pathway: principal sulcus (PS) to supplementary motor cortex (SMA); B, cortical‐striatal pathway: PS to caudate nucleus (Cd); C, cortical‐tectal pathway: PS to intermediate and deep layers of superior colliculus (SC).

Data from Goldman and Nauta , Selemon and Goldman‐Rakic ; M. L. Jouandet and P. S. Goldman‐Rakic, unpublished observations


Figure 10.

Topographical relationships between ventral anterior nucleus, mediodorsal nucleus, and medial pulvinar nucleus and selected cytoarchitectonic subdivisions of prefrontal cortex. Each subdivision projects to only one cytoarchitectonic area of cortex; each cortical area receives unique multiple thalamic input.

From Goldman‐Rakic and Porrino


Figure 11.

Prefrontal interconnections with several brain stem monoaminergic cell groups thought to be involved in activational processes. BC, brachium conjunctivum; CS, central superior nucleus; DR, dorsal raphe; LC, locus coeruleus; nST, solitary tract nucleus; PS, principal sulcus; PY, pyramids.

Data from Arnsten and Goldman‐Rakic and Porrino and Goldman‐Rakic


Figure 12.

Walker's cytoarchitectonic map of monkey prefrontal cortex. Lateral and ventral views show approximate locations of frontal eye fields (areas 8A, 45), inferior prefrontal convexity (area 12), and posterior orbital prefrontal cortex (areas 13, 14). AS, arcuate sulcus; CS, central sulcus; OT, optic tract; PS, principal sulcus.

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Patricia S. Goldman‐Rakic. Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory. Compr Physiol 2011, Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain: 373-417. First published in print 1987. doi: 10.1002/cphy.cp010509