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Advances in Anatomy
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Vol. 174
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Springer-Verlag Berlin Heidelberg GmbH
S. Geyer
The Microstructural Border
Between the Motor
and the Cognitive Domain
in the Human Cerebral Cortex
With 25Figures and 3Tables
Springer
Dr. Stefan Geyer
C. & O. Vogt Brain Research Institute
University of Diisseldorf
Universitătsstr. 1
40225 Diisseldorf
Germany
e-mail: [email protected]
ISSN 0301-5556
ISBN 978-3-540-40228-2
Library of Congress Cataloging-in-Publication Data
Geyer, Stefan, 1963-
The microstructural border between the motor and the cognitive domain in the
human cerebral cortex I Stefan Geyer.
p. cm. - (Advances in anatomy, embryoloy, and cell biology; v. 174)
Includes bibliographical references and index.
ISBN 978-3-540-40228-2 ISBN 978-3-642-18910-4 (eBook)
DOI 10.1007/978-3-642-18910-4
1. Motor cortex-Cytology. 2. Cerebral cortex-Cytology. 3. Cytoarchitectonics.
I. Tide. II. Series.
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Contents
1 Prologue:Toward the Concept
ofa Cortical ControlofVoluntaryMovements.....
1.1 Jackson and the ConceptofaMotor Cortex........
1.2 ExperimentalConfirmation ofthe Motor Cortex
in LaboratoryAnimals............................ 1
1.3 Maps ofthe Motor Cortex in Humans ............. 2
1.4 Differences in Function BetweenMotor
and PremotorCortex ............................. 3
1.5 Cytoarchitectonic Analysis ofthe Motor
and Premotor Cortex ............................. 4
1.6 Lashleyand Clark's Criticism
ofCytoarchitectonic Maps ........................ 5
1.7 Observer-Independent Cytoarchitectonic
Analysis and ProbabilisticMicrostructural-
FunctionalCorrelation-Two Responses
to Lashleyand Clark's Criticism................... 7
1.8 Goalofthis Study ................................ 8
2 Materialsand Methods ........................... 9
2.1 HistologicalProcessing ofPostmortem Brains ..... 10
2.2 Observer-Independent Cytoarchitectonic Analysis. 10
2.3 Three-Dimensional Reconstructionand Spatial
Normalization ofthe HistologicalVolumes ........ 12
3 Results........................................... 15
3.1 CytoarchitectonicFeatures
and Observer-IndependentAnalysis
ofthe BorderBetweenArea6and
the Prefrontal Cortex .,........................... 15
3.2 Cytoarchitectonic Features
and Observer-Independent Analysisofthe
Border BetweenArea6and the Primary
Motor Cortex..................................... 23
3.3 Reconstruction ofthe Histological Volumes
in 3-D,Spatial Normalization,and Generation
ofthe Population Map ofArea6................... 24
VII
4 Discussion....................................... 27
4.1 Observer-Independent Delineation ofArea6 ...... 27
4.2 Spatial NormalizationofArea 6................... 29
4.3 The Isocortical MotorSystem in Macaques........ 30
4.3.1 The Structural Framework:Microanatomical
Subdivisionofthe Agranular Frontal Isocortex .... 31
4.3.2 The Organizational Principle: Parieto-Frontal
Circuits.......................................... 33
4.3.3 The Isocortical MotorSystem in Macaques........ 34
4.3.3.1 PrimaryMotorCortex (Area Fl).................. 34
4.3.3.2 SupplementaryMotor Areas"SMAProper"
and "Pre-SMA" (Areas F3and F6)................. 40
4.3.3.3 Dorsolateral PremotorCortex
(PMd;AreasF2and F7) .......................... 48
4.3.3.4 Ventrolateral Premotor Cortex
(PMv;Areas F4and F5) .......................... 53
4.4 The IsocorticalMotorSystem in Humans ......... 61
4.4.1 StructuralOrganization .......................... 63
4.4.1.1 PrimaryMotorCortex............................ 63
4.4.1.2 SupplementaryMotor Areas "SMAProper"
and "Pre-SMA"................................... 65
4.4.1.3 Dorsolateraland Ventrolateral PremotorCortex ... 66
4.4.2 FunctionalOrganization.......................... 67
4.4.2.1 PrimaryMotorCortex............................ 70
4.4.2.2 SupplementaryMotorAreas "SMAProper"
and "Pre-SMA" ................................... 71
4.4.2.3 DorsolateralPremotorCortex..................... 73
4.4.2.4 Ventrolateral PremotorCortex.................... 74
5 Epilogue......................................... 75
References .............................................. 77
SubjectIndex ........................................... 91
VIII
1 Prologue: Toward the Concept of a Cortical Control
of Voluntary Movements
1.1
Jacksonand the Concept of a MotorCortex
In 1863John Hughlings Jackson wrote about unilateral epileptic seizures caused by
syphilis: "In very many cases of epilepsy, and especially in syphilitic epilepsy, the
convulsions are limited to one side of the body; and, as autopsies of patients who
have died after syphilitic epilepsy appear to show,the cause is obvious organic dis
ease on the side of the brain, opposite to the side of the body convulsed, frequently
onthe surface ofthehemisphere" (cited from Finger 1994;Jackson 1863).Inthe mid
dle of the nineteenth century the concept of a cortical control of voluntary move
ments that is fullyaccepted today was hotly debated. It waswidelybelieved that the
corpus striatumwasthe uppermost center ofmotorcontrol and the origin ofthe de
scending motor tracts. Jackson, on the other hand, was intrigued by the spread of
seizures over specific body parts, e.g., from the hand to the arm to the face on one
side of the body or from the hip to the legto the foot and toes. Most frequently af
fected were the muscles ofthe face,hand, and foot. Only in severe cases did the sei
zure cross the midline and involve the entire body, usually followedby loss of con
sciousness. In hemiplegic patients Jackson observed that unilateral seizures were
most likelyto affectthose parts ofthe body that werealso most affected in hemiple
gia. It appeared to him as if epilepsy were the "mobile counterpart of hemiplegia".
Based on these observations, Jackson proposed a sector of the cerebral cortex with
motor functions and topographically organized representations of muscles. In this
motor cortex, those body parts most frequently affected by epileptic seizures (i.e.,
face,hand, and foot) were assumed to have larger spatial representations than body
parts lessfrequently affected.
1.2
Experimental Confirmation of the MotorCortex in LaboratoryAnimals
Jackson's concept wasbased on clinical observations and brilliant conclusions.How
ever,he could not confirm experimentally the existence ofsuch a motor cortex, nor
could hedefine itsprecise topography.This succeeded afewyears later.Severaltimes
during the nineteenth century, scientists had attempted to induce body movements
byelectrically stimulating the cortex oflaboratoryanimals. Theexperiments,howev-
er, were not successful or provided conflicting results. In 1870,Gustav Fritsch and
Eduard Hitzig stimulated the cortex ofdogs-not in a laboratory, but on a dressing
table in a bedroom of Hitzig's house in Berlin. They found discrete regions of the
cortex that gavemuscular responses in the forepaw,hindpaw, face, and neck on the
opposite side. A unilateral lesion of the forepaw area with a scalpel handle signifi
cantly impaired motor performance but did not cause sensory deficits (Fritsch and
Hitzig 1870).Fritsch and Hitzig interpreted these findings as evidence for a discrete
motor cortex with a somatotopic (i.e.,topographicallycorrect) representation ofthe
body.
Several years later David Ferrier replicated the findings of Fritsch and Hitzig in
primates. Bystimulating the cortex rostral to the central sulcus with faradic current
he obtained a broad spectrum of movements. Amonkey with a small motor cortex
lesion developed paralysis restricted to the opposite hand and forearm but no defi
cits intouch and pain sensation.Another with alesion that encompassed large parts
ofthe leftfrontal,parietal,and temporallobe displayed aright hemiplegia. When the
brain was examined histologically, Ferrier found a degeneration of the pyramidal
tract extending as far as the lumbar spinal cord (Ferrier 1876,1886;Ferrier and Yeo
1885).In 1881,he eventook a monkey with aunilaterallesion ofthe left motor cor
tex to the Seventh International MedicalCongress in London. When the hemiplegic
animal, operated upon seven months earlier, limped into the demonstration room,
Jean-Martin Charcot remarked:"It is a patient!" (cited from Finger 1994). Basedon
the observation that patients with cortical lesions showed deficits predominantly in
voluntary movements whereas involuntary and "automatic" movements wereless af
fected,Jackson had already hypothesized that the cerebral cortex wasresponsible for
voluntary actions whereas subcortical centers played a role in more "automatic" ac
tivities. Ferrier confirmedthese conclusionswith observationsinlaboratoryanimals.
Primateswith amore elaborate cortex rely,when interactingwith their environment,
more onvoluntary movements than do animals loweron the phylogenetic scale,e.g.,
reptiles or amphibians. In other words, the higher an animal's levelon the phyloge
netic scale, the more its voluntary movements are affected by damage to the motor
cortex. The findings further supported the conceptthat voluntary movements, being
phylogenetically more "modern:' are represented mainlyon acortical level.
Around the turn of the twentieth century, Sidney Griinbaum and Charles Sher
rington supplemented Ferrier's studies with stimulation and lesion experiments in
apes. In accordance with Ferrier's findings, they reported that stimuli that evoked
motor responsesfrom the precentralgyrus wereineffectivewhen applied inthe post
central gyrus. Likewise,ablationsofthe precentralgyrus resulted in paralysis,where
as lesions in the postcentral gyrus did not (Grimbaum and Sherrington 1902,1903).
Grunbaum and Sherrington's carefully conducted experiments and meticulously
published data remainedseminal throughoutthe twentieth century.
1.3
Maps of the MotorCortex in Humans
The first comprehensive map ofthe human motor cortex is usually attributed to the
Canadian neurosurgeon Wilder Penfield.The sketch ofits somatotopic organization
(Penfield and Rasmussen 1952)-betterknown as the "motor homunculus"-can be
2
