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Organization of Secondary Motor Areas of Cerebral Cortex

Mario Wiesendanger

10.1002/cphy.cp010224

Source: Supplement 2: Handbook of Physiology, The Nervous System, Motor Control

Originally published: 1981

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Scope of Chapter
2 Methodological Approach in Historical Perspective
3 Primary and Secondary Motor Areas: Cytoarchitectonic Maps and Terminology
4 Premotor Area
4.1 Structure and General Considerations
4.2 Lesions of Premotor Cortex
4.3 Electrical Stimulation of Premotor Cortex
4.4 Electrical Activity Recorded in Premotor Cortex of Unconscious Animals
4.5 Single‐Unit Recordings in Premotor Cortex of Conscious Monkeys
4.6 Synthesis
5 Supplementary Motor Area
5.1 Definition and Historical Note
5.2 Structural Relationship of Supplementary Motor Area
5.3 Effects of Electrical Stimulation of Supplementary Motor Area and Epilepsy
5.4 Deficits Following Supplementary Motor Area Lesions
5.5 Electrophysiology of Supplementary Motor Area
5.6 Studies on Activation of Supplementary Motor Area in Human Beings
5.7 Synthesis
6 Somatosensory Cortical Areas SI And SII
6.1 Critical Review of Evidence for Motor Features of Areas SI and SII
6.2 Concept of Corticofugal Control of Somatosensory Transmission
6.3 Synthesis
7 Parietal Association Cortex Viewed as A Motor Area (A Short Introduction)
7.1 Lesions of Parietal Association Cortex and Electrical Stimulation
7.2 Structural Relationships With Motor Areas
7.3 Command Functions of Parietal Lobe
7.4 Synthesis
8 Addendum
Figure 1. Figure 1.

Motor areas in relation to classic cytoarchitectonic maps of monkey cortex. Areas 4 and FA (maps at right) correspond to motor cortex proper. Note variations of anterior border in the three maps. Brodmann's area 6 (left maps) is subdivided into a posterior portion 6aα and 6b by Vogt and Vogt or FB and FBA by von Bonin and Bailey and into an anterior portion 6aβ (Vogt and Vogt) or FC and FCB (von Bonin and Bailey). Reasons are given in the text to suggest that only the rostral portion of area 6 be considered as the premotor cortex. The posterior portion is likely to belong to the primary motor cortex representing proximal and axial muscles.

Adapted from von Bonin and Bailey 15, Brodmann 21, and Vogt and Vogt 159
Figure 2. Figure 2.

Structure of monkey's motor cortex. A: a parasagittal Nissl section through the hand motor control area with the approximate caudal boundary of area 4 adjoining area 3a and with approximate rostral boundary of area 4 adjoining area 6aα. B: A large injection of the enzyme horseradish peroxidase into the cervical cord (not shown) labeled many corticospinal cells in the fifth layer. Note high density of labeled cells in area 4. Scattered cells are also present throughout postcentral cortex and in posterior area 6 (area 6aα). C: outline of monkey brain with indication of sections shown in B. D: a nest of 3 labeled pyramidal tract cells, greatly magnified.

From M. Wiesendanger, B. Sessle, and R. Wiesendanger, unpublished data
Figure 3. Figure 3.

Major corticocortical connections of the premotor cortex (area 6aβ). A: origins of the afferent pathways, arrows to the premotor cortex. B: efferent projections, arrows from the premotor cortex.

From Humphrey 72
Figure 4. Figure 4.

Motor areas as elaborated by means of repetitive electrical stimulation of mesial surface of monkey's cerebral cortex. A: representation of muscular movements in the human brain. Note similar arrangement on mesial surface as in semiusculus representation (i.e., representation of the monkey's body parts) in D by Woolsey. B: motor areas on mesial surface. In front of leg area of primary motor field are the secondary field (tonic raising of arm) and the tertiary field (adversive movements of trunk and head). C: areas indicating predominant effects obtained in the human brain. D: semiusculus representation of Woolsey. All four areas have motor, M, and somatosensory, S, attributes, the first letter indicating the dominant effect.

A: adapted from Schäfer 181; B: adapted from Vogt and Vogt 160; C: adapted from Penfield and Welch 125; D: from Woolsey 173
Figure 5. Figure 5.

Major corticocortical connections of supplementary motor area. A: origins of afferent pathways, arrows to the supplementary motor area. B: efferent projections, arrows from the supplementary motor area.

From Humphrey 72
Figure 6. Figure 6.

Motor threshold for intracortical cathodal stimulation in anesthetized Cebus monkey; EMG response was recorded when stimulating tungsten microelectrode was at best depth. Left: threshold response of interosseus muscle when stimulating at point marked by star (penetration in precentral hand control area). Right: note increase of threshold intensity (in mA) as penetrations were made nearer to the supplementary motor area. Cebus monkey; anesthesia, N2O and Surital.

From Wiesendanger et al. 168
Figure 7. Figure 7.

Patterns of movements (figurine representation) elicited by repetitive cathodal stimulation (1‐ms pulses at 50 Hz) at various points of mesial surface. Left precentral cortex had a large, chronic lesion (sparing some of motor cortex at depth of central fissure). Note scarcity of forelimb movements upon stimulation of left supplementary motor area as compared to effects obtained from the right, intact cortex. Cebus monkey; anesthesia, N2O and Surital.

From Wiesendanger et al. 168
Figure 8. Figure 8.

Firing pattern of supplementary motor area neuron of monkey during execution of precision grip. Top left: 3 examples of original recording of unit activity and of force exerted between thumb and forefinger. Animals were trained to maintain a constant pressure (determined by a force window) for 1 s. Top, middle and right: force traces and associated rasters of unit activity aligned about force plateau. Top middle: required force for reinforcement, 3.6 N; top right: force, 2.3 N. Bottom: histograms of cellular activity constructed from the rasters. FON: histogram aligned with force onset; TON‐TOF: histogram aligned with force plateau. Note that discharge frequency starts to increase before pressure onset and that firing frequency was higher when force level increased. This cell had both dynamic and static characteristics.

From Smith 143
Figure 9. Figure 9.

Somatotopic organization of supplementary motor area as evidenced from unit recordings in an awake monkey. A section of opening of headpiece is shown overlying medial edge of hemisphere. Each symbol represents an electrode penetration. Filled circles, tracks that contained neurons related to distal movements of upper extremity; open circles, to proximal movements; crosses, to body or leg movements. V, visual neurons; small dots, tracks without responsive neurons. In spite of a considerable overlap, these experiments provide supporting evidence for a somatotopic arrangement similar to that found in electrical stimulation experiments by Vogt and Vogt 160 and by Woolsey 173. See also Fig. 5.

From Brinkman and Porter 17
Figure 10. Figure 10.

Changes of regional cerebral blood flow (rCBF) in supplementary motor area (SMA) of man. Vertex and lateral view of left hemisphere. Top, during repetitive fast flexion of the contralateral index finger. Bottom, internal programming of a motor sequence test (not accompanied by any electromyogram activity); opposition of thumb and forefingers in nontrivial sequence was imagined but not actually performed. The first task strongly increased rCBF in opposite Rolandic region, but not in SMA. Inversely, internal programming appears to activate contralateral as well as ipsilateral (not shown) SMA, but not Rolandic region. Right, color code for percentage of increase in rCBF.

Adapted from Roland et al. 133
Figure 11. Figure 11.

Differential projection from subdivisions of peri‐Rolandic hand area to cervical spinal cord. Stippled areas in spinal gray matter indicate terminal labeling (silver grains in autoradiographs) following injections ([3H]leucine and

3H]proline) of individual cytoarchitectonic areas. Schematic diagram summarizing results obtained from 6 different monkeys (Macaca fascicularis). Note concentration of labeling in dorsal horn following postcentral injections and in intermediate zone following injections in area 3a and area 4. The relatively sparse projection to the ventral horn (probably reflecting the corticomotoneuronal system) appears to originate from area 3a as defined by Coulter and Jones. [From Coulter and Jones 33
Figure 12. Figure 12.

The corticopontine projection from peri‐Rolandic cortex and adjoining areas in monkey. A: topological relationship between cortical, α, and pontine areas; b, c, d, caudal, mid‐pontine, and rostral coronal sections of pons, with outlines of pontine nuclei. Note concentration of frontal projection to midline areas of pontine nuclei. Parietal association cortex projects more laterally. B: gradients in density of corticopontine projection. By far the heaviest projection was found to originate from the pre‐ and postcentral cortex. Further sources of contributions are in following order; supplementary motor area, area 5, SII, area 6 on lateral hemisphere, area 8, area 7, and prefrontal association cortex (areas 9 and 10). Cortical area with a stippled outline (Aa) was not investigated in this study. See also Brodal, ref. 20.

From Wiesendanger et al. 169


Figure 1.

Motor areas in relation to classic cytoarchitectonic maps of monkey cortex. Areas 4 and FA (maps at right) correspond to motor cortex proper. Note variations of anterior border in the three maps. Brodmann's area 6 (left maps) is subdivided into a posterior portion 6aα and 6b by Vogt and Vogt or FB and FBA by von Bonin and Bailey and into an anterior portion 6aβ (Vogt and Vogt) or FC and FCB (von Bonin and Bailey). Reasons are given in the text to suggest that only the rostral portion of area 6 be considered as the premotor cortex. The posterior portion is likely to belong to the primary motor cortex representing proximal and axial muscles.

Adapted from von Bonin and Bailey 15, Brodmann 21, and Vogt and Vogt 159


Figure 2.

Structure of monkey's motor cortex. A: a parasagittal Nissl section through the hand motor control area with the approximate caudal boundary of area 4 adjoining area 3a and with approximate rostral boundary of area 4 adjoining area 6aα. B: A large injection of the enzyme horseradish peroxidase into the cervical cord (not shown) labeled many corticospinal cells in the fifth layer. Note high density of labeled cells in area 4. Scattered cells are also present throughout postcentral cortex and in posterior area 6 (area 6aα). C: outline of monkey brain with indication of sections shown in B. D: a nest of 3 labeled pyramidal tract cells, greatly magnified.

From M. Wiesendanger, B. Sessle, and R. Wiesendanger, unpublished data


Figure 3.

Major corticocortical connections of the premotor cortex (area 6aβ). A: origins of the afferent pathways, arrows to the premotor cortex. B: efferent projections, arrows from the premotor cortex.

From Humphrey 72


Figure 4.

Motor areas as elaborated by means of repetitive electrical stimulation of mesial surface of monkey's cerebral cortex. A: representation of muscular movements in the human brain. Note similar arrangement on mesial surface as in semiusculus representation (i.e., representation of the monkey's body parts) in D by Woolsey. B: motor areas on mesial surface. In front of leg area of primary motor field are the secondary field (tonic raising of arm) and the tertiary field (adversive movements of trunk and head). C: areas indicating predominant effects obtained in the human brain. D: semiusculus representation of Woolsey. All four areas have motor, M, and somatosensory, S, attributes, the first letter indicating the dominant effect.

A: adapted from Schäfer 181; B: adapted from Vogt and Vogt 160; C: adapted from Penfield and Welch 125; D: from Woolsey 173


Figure 5.

Major corticocortical connections of supplementary motor area. A: origins of afferent pathways, arrows to the supplementary motor area. B: efferent projections, arrows from the supplementary motor area.

From Humphrey 72


Figure 6.

Motor threshold for intracortical cathodal stimulation in anesthetized Cebus monkey; EMG response was recorded when stimulating tungsten microelectrode was at best depth. Left: threshold response of interosseus muscle when stimulating at point marked by star (penetration in precentral hand control area). Right: note increase of threshold intensity (in mA) as penetrations were made nearer to the supplementary motor area. Cebus monkey; anesthesia, N2O and Surital.

From Wiesendanger et al. 168


Figure 7.

Patterns of movements (figurine representation) elicited by repetitive cathodal stimulation (1‐ms pulses at 50 Hz) at various points of mesial surface. Left precentral cortex had a large, chronic lesion (sparing some of motor cortex at depth of central fissure). Note scarcity of forelimb movements upon stimulation of left supplementary motor area as compared to effects obtained from the right, intact cortex. Cebus monkey; anesthesia, N2O and Surital.

From Wiesendanger et al. 168


Figure 8.

Firing pattern of supplementary motor area neuron of monkey during execution of precision grip. Top left: 3 examples of original recording of unit activity and of force exerted between thumb and forefinger. Animals were trained to maintain a constant pressure (determined by a force window) for 1 s. Top, middle and right: force traces and associated rasters of unit activity aligned about force plateau. Top middle: required force for reinforcement, 3.6 N; top right: force, 2.3 N. Bottom: histograms of cellular activity constructed from the rasters. FON: histogram aligned with force onset; TON‐TOF: histogram aligned with force plateau. Note that discharge frequency starts to increase before pressure onset and that firing frequency was higher when force level increased. This cell had both dynamic and static characteristics.

From Smith 143


Figure 9.

Somatotopic organization of supplementary motor area as evidenced from unit recordings in an awake monkey. A section of opening of headpiece is shown overlying medial edge of hemisphere. Each symbol represents an electrode penetration. Filled circles, tracks that contained neurons related to distal movements of upper extremity; open circles, to proximal movements; crosses, to body or leg movements. V, visual neurons; small dots, tracks without responsive neurons. In spite of a considerable overlap, these experiments provide supporting evidence for a somatotopic arrangement similar to that found in electrical stimulation experiments by Vogt and Vogt 160 and by Woolsey 173. See also Fig. 5.

From Brinkman and Porter 17


Figure 10.

Changes of regional cerebral blood flow (rCBF) in supplementary motor area (SMA) of man. Vertex and lateral view of left hemisphere. Top, during repetitive fast flexion of the contralateral index finger. Bottom, internal programming of a motor sequence test (not accompanied by any electromyogram activity); opposition of thumb and forefingers in nontrivial sequence was imagined but not actually performed. The first task strongly increased rCBF in opposite Rolandic region, but not in SMA. Inversely, internal programming appears to activate contralateral as well as ipsilateral (not shown) SMA, but not Rolandic region. Right, color code for percentage of increase in rCBF.

Adapted from Roland et al. 133


Figure 11.

Differential projection from subdivisions of peri‐Rolandic hand area to cervical spinal cord. Stippled areas in spinal gray matter indicate terminal labeling (silver grains in autoradiographs) following injections ([3H]leucine and

3H]proline) of individual cytoarchitectonic areas. Schematic diagram summarizing results obtained from 6 different monkeys (Macaca fascicularis). Note concentration of labeling in dorsal horn following postcentral injections and in intermediate zone following injections in area 3a and area 4. The relatively sparse projection to the ventral horn (probably reflecting the corticomotoneuronal system) appears to originate from area 3a as defined by Coulter and Jones. [From Coulter and Jones 33


Figure 12.

The corticopontine projection from peri‐Rolandic cortex and adjoining areas in monkey. A: topological relationship between cortical, α, and pontine areas; b, c, d, caudal, mid‐pontine, and rostral coronal sections of pons, with outlines of pontine nuclei. Note concentration of frontal projection to midline areas of pontine nuclei. Parietal association cortex projects more laterally. B: gradients in density of corticopontine projection. By far the heaviest projection was found to originate from the pre‐ and postcentral cortex. Further sources of contributions are in following order; supplementary motor area, area 5, SII, area 6 on lateral hemisphere, area 8, area 7, and prefrontal association cortex (areas 9 and 10). Cortical area with a stippled outline (Aa) was not investigated in this study. See also Brodal, ref. 20.

From Wiesendanger et al. 169
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Article Title: Organization of Secondary Motor Areas of Cerebral Cortex
 

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Mario Wiesendanger. Organization of Secondary Motor Areas of Cerebral Cortex. Compr Physiol 2011, Supplement 2: Handbook of Physiology, The Nervous System, Motor Control: 1121-1147. First published in print 1981. doi: 10.1002/cphy.cp010224