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Three-dimensional cytoarchitectonic analysis of the posterior bank of the human precentral sulcus

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Abstract

Studies employing functional magnetic resonance imaging have identified the human frontal eye field as being in the anterior and partly in the posterior wall, as well as at the base of the precentral sulcus. Moreover, it is known that the frontal eye field extends rostrally to the superior frontal sulcus. According to Brodmann’s cytoarchitectonic map, this region belongs to the dysgranular Brodmann area 6 of the premotor cortex. However, the frontal eye field in non-human primates has been located within the arcuate sulcus in Brodmann area 8, generating considerable debate about where to locate exactly the frontal eye field in humans. Functional studies of the primate frontal eye field have revealed a principal homology of voluntary saccadic control systems in human and old-world monkeys, especially the macaque. But these homologies seem to be contradicted by the reported topographic localization at the cytoarchitectonic level. Therefore, we studied the cytoarchitectonic structure of the posterior bank of the precentral sulcus of a human brain, employing newly developed spatial mapping techniques to provide data about whether or not this region should be considered cytoarchitecturally homogeneous or heterogeneous. We used functional magnetic resonance imaging results, as an initial guide in localizing a region which is activated by saccadic tasks. A maximum of activation was detected around the junction of the superior frontal sulcus and the precentral sulcus extending 1.5 cm along the precentral sulcus in direction of the lateral sulcus. Here, one human brain has been analyzed to obtain preliminary data about the cytoarchitectonical changes of a part of area 6. Statistical analysis of the three-dimensional architectonic data from this region allowed us to identify a zone at the posterior bank, which in other studies has been associated with a functional region that controls pursuit eye movements and performs sensory-to-motor transformations. We found two significant sectors along the ventral part of the posterior bank of the precentral sulcus. The caudal transition region coincides partly with a region that integrates retinal and eye position signals for target location, arm, and axial movements. The second more ventrally located region is attributed to process oral-facial movements. The caudal transition region coincides with our functional magnetic resonance imaging investigation. It was revealed that this region lies at the inferior frontal eye field, where a pronounced activation over a larger region can be stimulated. Currently, more studies are needed to combine functional magnetic resonance imaging data of maximal activation with data from whole histologic brain sections of more individuals and to quantify the variability of this region and its sub-regions by means of a standardized brain atlas.

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Abbreviations

3D:

three-dimensional

BA:

Brodmann’s area

BOLD:

blood oxygen level dependent

CS:

central sulcus

EPI:

echo planar imaging

FEF:

frontal eye field

FOV:

field of view

iFEF:

inferior frontal eye field

fMRI:

functional magnetic resonance imaging

L:

layer, lamina

LIP:

lateral intraparietal area

MNI:

Montreal Neurologic Institute

MRI:

magnetic resonance imaging

NeuN:

neuronal nuclear protein

PET:

positron emission tomography

PCS:

precentral sulcus

PMd:

dorsal superior premotor cortex

PMd-caudal:

caudal part of the dorsal premotor cortex

PMd-rostral:

rostral part of the dorsal premotor cortex

PMv:

ventral inferior premotor cortex

PMv-caudal:

caudal part of the ventral premotor cortex

PMv-rostral:

rostral part of the ventral premotor cortex

Pocg:

postcentral gyrus

ROI:

region of interest

Prcg:

precentral gyrus

SEF:

supplementary eye field

sFEF:

superior frontal eye field

SWM:

spatial working memory task

T1:

longitudinal relaxation time

TE:

echo time

TR:

repetition time

VOI:

volume of interest

References

  • Amunts K, Weiss PH, Mohlberg H, Pieperhoff P, Eickhoff S, Gurd JM, Marshall JC, Shah NJ, Fink GR, Zilles K (2004) Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space–the roles of Brodmann areas 44 and 45. Neuroimage 22:42–56

    Article  PubMed  Google Scholar 

  • Andersen RA, Essick GK, Siegel RM (1985) Encoding of spatial location by posterior parietal neurons. Science 230:456–458

    Article  PubMed  CAS  Google Scholar 

  • Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L (1990) Eye position effects on visual, memory and saccade related activity in areas LIP and 7A of macaque. J Neurosci 10:1176–1196

    PubMed  CAS  Google Scholar 

  • Anderson TJ, Jenkins IH, Brooks DJ, Hawken MB, Frackowiak RS, Kennard C (1994) Cortical control of saccades and fixation in man. A PET study. Brain 117:1073–1084

    Google Scholar 

  • Bailey P, von Bonin G (1951) The isocortex of man. University of Illinois Press, Urbana, IL

    Google Scholar 

  • Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 286:211–228

    Article  Google Scholar 

  • Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375

    Article  PubMed  CAS  Google Scholar 

  • Berman RA, Colby CL, Genovese CR, Voyvodic JT, Luna B, Thulborn KR, Sweeney JA (1999) Cortical networks subserving pursuit and saccadic eye movements in humans: an fMRI study. Hum Brain Mapp 8:209–225

    Article  PubMed  CAS  Google Scholar 

  • Blanke O, Seeck M (2003) Direction of saccadic and smooth eye movements induced by electrical stimulation of the human frontal eye field: effect of orbital position. Exp Brain Res 150:174–183

    PubMed  Google Scholar 

  • von Bonin G, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana, IL

    Google Scholar 

  • Boussaoud D, Bremmer F (1999) Gaze effects in the cerebral cortex: reference frames for space coding and action. Exp Brain Res 128:170–180

    Article  PubMed  CAS  Google Scholar 

  • Braak H (1980) Architectonics of the human telencephalic cortex. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Brauer K, Schober W (1970) Catalogue of Mammalian Brains. VEB Gustav Fischer Verlag, Jena

    Google Scholar 

  • Bremmer F, Ilg UJ, Thiele A, Distler C, Hoffmann K-P (1997a) Eye position effects in monkey cortex. I. Visual and pursuit related activity in extrastriate areas MT and MST. J Neurophysiol 77:944–961

    PubMed  CAS  Google Scholar 

  • Bremmer F, Distler C, Hoffmann K-P (1997b) Eye position effects in monkey cortex. I. Pursuit- and fixation-related activity in posterior parietal areas LIP and 7A. J Neurophysiol 77:962–977

    PubMed  CAS  Google Scholar 

  • Bremmer F, Pouget A, Hoffmann K-P (1998) Eye position encoding in the macaque posterior parietal cortex. Eur J Neurosci 10:153–160

    Article  PubMed  CAS  Google Scholar 

  • Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Barth, Leipzig

    Google Scholar 

  • Chalupa LM, Werner JS (eds) (2004) The visual neuroscience. MIT Press, Cambridge

  • Courtney SM, Petit L, Maisog JM, Ungerleider LG, Haxby JV (1998) An area specialized for spatial working memory in human frontal cortex. Science 279:1347–1351

    Article  PubMed  CAS  Google Scholar 

  • Crammond DJ, Kalaska JF (1996) Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task. Exp Brain Res 108:45–61

    Article  PubMed  CAS  Google Scholar 

  • Duke-Elder S, Wybar KC (1961) The anatomy of the visual system. Henry Kimpton, London

    Google Scholar 

  • Duvernoy HM (1999) The human brain surface, blood supply, and three-dimensional sectional anatomy. Springer, Wien

    Google Scholar 

  • von Economo C, Koskinas GN (1925) Die Zytoarchitektonik der Hirnrinde des erwachsenen Menschen. Springer, Wien

    Google Scholar 

  • Fadiga L, Fogassi L, Gallese V, Rizzolatti G (2000) Visuomotor neurons: ambiguity of the discharge or ‘motor’ perception? Int J Psychophysiol 35:165–177

    Article  PubMed  CAS  Google Scholar 

  • Ferrier D (1875) Experiments on the brains of monkeys. Proc R Soc Lond 23:409–432

    Google Scholar 

  • Foerster O (1931) The cerebral cortex in man. Lancet 2:309–312

    Google Scholar 

  • Fogassi L, Raos V, Franchi G, Gallese V, Luppino G, Matelli M (1999) Visual responses in the dorsal premotor area F2 of the macaque monkey. Exp Brain Res 128:194–199

    Article  PubMed  CAS  Google Scholar 

  • Fox PT, Fox JM, Raichle ME, Burde RM (1985) The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. J Neurophysiol 54:348–369

    PubMed  CAS  Google Scholar 

  • Gabernet L, Meskenaite V, Hepp-Reymond MC (1999) Parcellation of the lateral premotor cortex of the macaque monkey based on staining with the neurofilament antibody SMI-32. Exp Brain Res 128:188–193

    Article  PubMed  CAS  Google Scholar 

  • Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G (1988) Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements. Exp Brain Res 71:475–490

    Article  PubMed  CAS  Google Scholar 

  • Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G (1989) Somatotopic representation in inferior area 6 of the macaque monkey. Brain Behav Evol 33:118–121

    PubMed  CAS  Google Scholar 

  • Geyer S, Matelli M, Luppino G, Zilles K (2000) Functional neuroanatomy of the primate isocortical motor system. Anat Embryol 202:443–474

    Article  PubMed  CAS  Google Scholar 

  • Godoy J, Luders H, Dinner DS, Morris HH, Wyllie E (1990) Versive eye movements elicited by cortical stimulation of the human brain. Neurology 40:296–299

    PubMed  CAS  Google Scholar 

  • Heide W, Binkofski F, Seitz JR, Posse S, Nitschke MF, Freund H-J, Kömpf D (2001) Activation of frontoparietal cortices during memorized triple-step sequences of saccadic eye movements: an fMRI study. Eur J Neurosci 13:1177–1189

    Article  PubMed  CAS  Google Scholar 

  • Hepp-Reymond MC, Husler EJ, Maier MA, Ql HX (1994) Force-related neuronal activity in two regions of the primate ventral premotor cortex. Can J Physiol Pharmacol 72:571–579

    PubMed  CAS  Google Scholar 

  • Lobel E, Kahane P, Leonards U, Grosbras M, Lehericy S, Le Bihan D, Berthoz A (2001) Localization of human frontal eye fields: anatomical and functional findings of functional magnetic resonance imaging and intracerebral electrical stimulation. J Neurosurg 95:804–815

    Article  PubMed  CAS  Google Scholar 

  • Luna B, Thulborn KR, Strojwas MH, McCurtain BJ, Berman RA, Genovese CR, Sweeney JA (1998) Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study. Cereb Cortex 8:40–47

    Article  PubMed  CAS  Google Scholar 

  • Matelli M, Luppino G (1996) Thalamic input to mesial and superior area 6 in the macaque monkey. J Comp Neurol 372:59–87

    Article  PubMed  CAS  Google Scholar 

  • Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav Brain Res 18:125–136

    Article  PubMed  CAS  Google Scholar 

  • Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311:445–462

    Article  PubMed  CAS  Google Scholar 

  • Modersitzki J (2004) Numerical methods for image registration. Oxford University Press, Oxford

    Google Scholar 

  • Muri RM, Heid O, Nirkko AC, Ozdoba C, Felblinger J, Schroth G, Hess CW (1998) Functional organization of saccades and antisaccades in the frontal lobe in humans: a study with echo planar functional magnetic resonance imaging. J Neurol Neurosurg Psychiatry 65:374–377

    PubMed  CAS  Google Scholar 

  • Ngowyang G (1934) Die Cytoarchitektonik des menschlichen Stirnhirns. Monogr Nat Res Inst Psychol Acad Sin 7:1–69

    Google Scholar 

  • O’Driscoll GA, Wolff AL, Benkelfat C, Florencio PS, Lal S, Evans AC (2000) Functional neuroanatomy of smooth pursuit and predictive saccades. Neuroreport 11:1335–1340

    Article  PubMed  CAS  Google Scholar 

  • Ono M, Kubik S, Abernathey CD (1990) Atlas of the cerebral sulci. Thieme, Stuttgart

    Google Scholar 

  • Paus T (1996) Location and function of the human frontal eye-field: a selective review. Neuropsychologia 34:475–483

    Article  PubMed  CAS  Google Scholar 

  • Penfield W, Jasper H (1954) Epilepsy and the functional anatomy of the human brain. Little Brown and Co, Boston

    Google Scholar 

  • Petit L, Haxby JV (1999) Functional anatomy of pursuit eye movements in humans as revealed by fMRI. J Neurophysiol 82:463–471

    PubMed  CAS  Google Scholar 

  • Petit L, Orssaud C, Tzourio N, Salamon G, Mazoyer B, Berthoz A (1993) PET study of voluntary saccadic eye movements in humans: basal ganglia-thalamocortical system and cingulate cortex involvement. J Neurophysiol 69:1009–10017

    PubMed  CAS  Google Scholar 

  • Petit L, Orssaud C, Tzourio N, Crivello F, Berthoz A, Mazoyer B (1996) Functional anatomy of a prelearned sequence of horizontal saccades in humans. J Neurosci 16:3714–3726

    PubMed  CAS  Google Scholar 

  • Picard N, Strick PL (2001) Imaging the premotor areas. Curr Opin Neurobiol 11:663–672

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen T, Penfield W (1948) Movement of head and eyes from stimulation of human frontal cortex. Res Publ Assoc Res Nerv Ment Dis 27:346–361

    PubMed  Google Scholar 

  • Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res 71:491–507

    Article  PubMed  CAS  Google Scholar 

  • Rizzolatti G, Gentilucci M, Camarda RM, Gallese V, Luppino G, Matelli M, Fogassi L (1990) Neurons related to reaching-grasping arm movements in the rostral part of area 6 (area 6a beta). Exp Brain Res 82:337–350

    Article  PubMed  CAS  Google Scholar 

  • Rizzolatti G, Fogassi L, Gallese V (2002) Motor and cognitive functions of the ventral premotor cortex. Curr Opin Neurobiol 12:149–154

    Article  PubMed  CAS  Google Scholar 

  • Rosano C, Krisky CM, Welling JS, Eddy WF, Luna B, Thulborn KR, Sweeney JA (2002) Pursuit and saccadic eye movement subregions in human frontal eye field: a high-resolution fMRI investigation. Cereb Cortex 12:107–115

    Article  PubMed  Google Scholar 

  • Rosano C, Sweeney JA, Melchitzky DS, Lewis DA (2003) The human precentral sulcus: chemoarchitecture of a region corresponding to the frontal eye fields. Brain Res 972:16–30

    Article  PubMed  CAS  Google Scholar 

  • Sanides F (1962) Die Architektonik des menschlichen Stirnhirns Monographien aus dem Gesamtgebiete der Neurologie und Psychiatrie: 98. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Sarkissov SA, Filimonoff IN, Kononowa EP, Preobraschenskaja IS, Kukuew LA (1955) Atlas of the cytoarchitectonics of the human cerebral cortex. Medgiz, Moscow

    Google Scholar 

  • Schall JD (1997) Visuomotor areas of the frontal lobe. In: Rockland K, Peters A, Kaas J (eds) Extrastriate cortex of primates, vol 12, Cerebral cortex. Plenum Press, New York, pp 527–638

  • Schieber MH (1999) Somatotopic gradients in the distributed organization of the human primary motor cortex hand area: evidence from small infarcts. Exp Brain Res 128:139–148

    Article  PubMed  CAS  Google Scholar 

  • Schmitt O, Böhme M (2002) A robust transcortical profile scanner for generating 2D-traverses in histological sections of rich curved cortical courses. Neuroimage 16:1103–1119

    Article  PubMed  CAS  Google Scholar 

  • Schmitt O, Hömke L, Dümbgen L (2003) Detection of cortical transition regions utilizing statistical analysis of excess masses. Neuroimage 19:42–63

    PubMed  Google Scholar 

  • Schmitt O, Pakura M, Aach T, Hömke L, Böhme M, Bock S, Preuße S (2004a) Analysis of nerve fibers and their distribution in histologic sections of the human brain. Microsc Res Tech 63:220–243

    Article  PubMed  CAS  Google Scholar 

  • Schmitt O, Preuße S, Haas SJP (2004b) Comparison of contrast, sensitivity and efficiency of signal amplified and nonamplified immunohistochemical reactions suitable for videomicroscopy based quantification and neuroimaging. Brain Res Methods 12:157–171

    Google Scholar 

  • Shen L, Alexander GE (1997) Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. J Neurophysiol 77:1195–1212

    PubMed  CAS  Google Scholar 

  • Somogyi P, Takagi H (1982) A note on the use of picric acid and paraformaldehyde glutaraldehyde fixative for correlated light and electron mircoscopic immuno-cytochemistry. Neuroscience 7:1779–1783

    Article  PubMed  CAS  Google Scholar 

  • Stanton GB, Deng SY, Goldberg ME, McMullen NT (1989) Cytoarchitectural characteristics of the frontal eye fields in macaque monkeys. J Comp Neurol 282:415–427

    Article  PubMed  CAS  Google Scholar 

  • Stanton GB, Bruce CJ, Goldberg ME (1993) Topography of projections to the frontal lobe from the macaque frontal eye fields. J Comp Neurol 330:286–301

    Article  PubMed  CAS  Google Scholar 

  • Stanton GB, Bruce CJ, Goldberg ME (1995) Topography of projections to posterior cortical areas from the macaque frontal eye fields. J Comp Neurol 353:291–305

    Article  PubMed  CAS  Google Scholar 

  • Strasburger E (1937) Die myeloarchitektonische Gliederung des Stirnhirns beim Menschen und Schimpansen. J Psychol Neurol 47:461–491

    Google Scholar 

  • Sweeney JA, Mintun MA, Kwee S, Wiseman MB, Brown DL, Rosenberg DR, Carl JR (1996) Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J Neurophysiol 75:454–468

    PubMed  CAS  Google Scholar 

  • Talairach J, Tournoux P (1993) Referentially orientated cerebral MRI anatomy. Thieme Medical publishers Inc, New York

    Google Scholar 

  • Tehovnik EJ, Sommer MA, Chou IH, Slocum WM, Schiller PH (2000) Eye fields in the frontal lobes of primates. Brain Res Brain Res Rev 32:413–448

    Article  PubMed  CAS  Google Scholar 

  • Vogt O (1910) Die myeloarchitektonische Felderung des menschlichen Stirnhirns. J Psychol Neurol 15:221–238

    Google Scholar 

  • Vogt O (1926) Die vergleichend-architektonische und die vergleichend-reizphysiologische Felderung der Großhirnrinde unter besonderer Berücksichtigung der menschlichen. Naturwissenschaften 14:1190–1194

    Article  Google Scholar 

  • Vogt C, Vogt O (1919) Allgemeine Ergebnisse unserer Hirnforschung. J Psychol Neurol 25:279–461

    Google Scholar 

  • Zipser D, Andersen RA (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–684

    Article  PubMed  CAS  Google Scholar 

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Acknowledgement

We thank U. Almert and P. Lau of the Institute of Anatomy (University of Lübeck) for excellent histologic preparations. Dr. F. Binkofski and Dr. M. Nagel were of great help, as they provided the activation maxima of saccadic experiments. We also thank S. Haas for support and M. Westlund for editing of the manuscript.

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Schmitt, O., Modersitzki, J., Heldmann, S. et al. Three-dimensional cytoarchitectonic analysis of the posterior bank of the human precentral sulcus. Anat Embryol 210, 387–400 (2005). https://doi.org/10.1007/s00429-005-0030-8

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