Subdivisions of human parietal area 5 revealed by quantitative receptor autoradiography: a parietal region between motor, somatosensory, and cingulate cortical areas

Brodmann's area (BA) 5 of the human superior parietal cortex occupies a central anatomical position between the primary motor (BA 4), somatosensory (area 3b and BA 2), cingulate (area 23c), and superior parietal association cortex (BA 7). We studied the regional and laminar distributions of the binding sites of 12 different neurotransmitter receptors (glutamatergic: AMPA, kainate, NMDA; GABAergic: GABAA, GABAB; cholinergic: muscarinic M2, nicotinic; adrenergic: alpha1, alpha2; serotoninergic: 5-HT1A, 5-HT2; dopaminergic: D1) in human postmortem brains by means of quantitative receptor autoradiography, since the structural and functional aspects of human BA 5 are widely unknown, and previous observations have demonstrated characteristic differences in receptor distribution between motor and somatosensory areas. Binding site densities were measured in the cytoarchitectonically defined BA 5 and surrounding regions. Similarities and differences of receptor distribution between cortical areas were studied by cluster analysis of mean binding site densities averaged over all cortical layers, univariate and multivariate statistics, and by density profiles representing laminar receptor distribution patterns. Based on regional heterogeneities of binding site densities and of the cytoarchitecture within BA 5, we suggest a subdivision into three subareas: medial area 5M, lateral area 5L, and area 5Ci in the region around the cingulate sulcus. BA 5 is therefore a heterogeneous cortical region, comprising three subareas showing receptor expression patterns similar to the adjoining higher order somatosensory, multimodal parietal, or cingulate regions. These findings suggest that human BA 5 constitutes a higher order cortical area, clearly distinct from the primary somatosensory and motor cortex.

[1]  J. Mazziotta,et al.  Brain Mapping: The Methods , 2002 .

[2]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[3]  D L Rosene,et al.  Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents , 1987, The Journal of comparative neurology.

[4]  Francesco Lacquaniti,et al.  Multiple levels of representation of reaching in the parieto-frontal network. , 2003, Cerebral cortex.

[5]  Daniel G Stewart,et al.  Potential Noradrenergic Targets for Cognitive Enhancement in Schizophrenia , 2004, CNS Spectrums.

[6]  L. Limbird,et al.  Stimulation of Mitogen-activated Protein Kinase by G Protein-coupled α2-Adrenergic Receptors Does Not Require Agonist-elicited Endocytosis* , 1999, The Journal of Biological Chemistry.

[7]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[8]  Masahiro Sakamoto,et al.  Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus , 2004, Experimental Brain Research.

[9]  Elisabeth A. Murray,et al.  Supplementary Sensory Area The Medial Parietal Cortex in the Monkey , 1981 .

[10]  Philippe A. Chouinard,et al.  Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. , 2003, Journal of neurophysiology.

[11]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[12]  P S Goldman-Rakic,et al.  Quantitative autoradiographic mapping of serotonin 5‐HT1 and 5‐HT2 receptors and uptake sites in the neocortex of the rhesus monkey , 1989, The Journal of comparative neurology.

[13]  B. Merker Silver staining of cell bodies by means of physical development , 1983, Journal of Neuroscience Methods.

[14]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[15]  A. Schleicher,et al.  21 – Quantitative Analysis of Cyto- and Receptor Architecture of the Human Brain , 2002 .

[16]  J. Kaas The functional organization of somatosensory cortex in primates. , 1993, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[17]  [3H]RX 821002 in human dorsolateral prefrontal cortex: no changes in postmortem tissue from subjects with schizophrenia , 2003, Psychiatry Research.

[18]  F. Lacquaniti,et al.  Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. , 2001, Cerebral cortex.

[19]  A. Levey,et al.  Muscarinic Activation of Mitogen‐Activated Protein Kinase in PC12 Cells , 2000, Journal of neurochemistry.

[20]  C. Galletti,et al.  Role of the medial parieto-occipital cortex in the control of reaching and grasping movements , 2003, Experimental Brain Research.

[21]  Trevor Sharp,et al.  A review of central 5-HT receptors and their function , 1999, Neuropharmacology.

[22]  Guy Bouvier,et al.  Stimulation of human somatosensory cortex: tactile and body displacement perceptions in medial regions , 2004, Experimental Brain Research.

[23]  Lacquaniti,et al.  Visuo‐motor transformations for arm reaching , 1998, The European journal of neuroscience.

[24]  R. Nicoll,et al.  AMPA Receptor Trafficking at Excitatory Synapses , 2003, Neuron.

[25]  E Wyllie,et al.  Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. , 1994, Electroencephalography and clinical neurophysiology.

[26]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[27]  G. Paxinos,et al.  THE HUMAN NERVOUS SYSTEM , 1975 .

[28]  M. Inase,et al.  Two movement-related foci in the primate cingulate cortex observed in signal-triggered and self-paced forelimb movements. , 1991, Journal of neurophysiology.

[29]  A. Berts,et al.  Transcriptional Responses to Growth Factor and G Protein‐Coupled Receptors in PC12 Cells , 2000, Journal of neurochemistry.

[30]  Gary Aston-Jones,et al.  Behavioral functions of locus coeruleus derived from cellular attributes , 1985 .

[31]  P S Goldman-Rakic,et al.  Quantitative autoradiography of major neurotransmitter receptors in the monkey striate and extrastriate cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  K. Krnjević Synaptic mechanisms modulated by acetylcholine in cerebral cortex. , 2004, Progress in brain research.

[33]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[34]  Marco Iacoboni,et al.  Interhemispheric visuo-motor integration in humans: the role of the superior parietal cortex , 2004, Neuropsychologia.

[35]  L. Limbird Receptors linked to inhibition of adenylate cyclase: additional signaling mechanisms , 1988, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[36]  H. Burton,et al.  Differential effects of GABA and bicuculline on rapidly- and slowly-adapting neurons in primary somatosensory cortex of primates , 2004, Experimental Brain Research.

[37]  Karl Zilles,et al.  Architecture, Connectivity, and Transmitter Receptors of Human Extrastriate Visual Cortex , 1997 .

[38]  R. Summers,et al.  Role of adrenoceptor subtypes in memory consolidation , 2002, Progress in Neurobiology.

[39]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[40]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[41]  J. Bormann,et al.  The 'ABC' of GABA receptors. , 2000, Trends in pharmacological sciences.

[42]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[43]  K. Zilles,et al.  Hierarchical Processing of Tactile Shape in the Human Brain , 2001, Neuron.

[44]  M M Mesulam,et al.  Distribution of muscarinic receptor subtypes within architectonic subregions of the primate cerebral cortex , 1988, The Journal of comparative neurology.

[45]  J. Kalaska,et al.  Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics , 2004, Experimental Brain Research.

[46]  T Allison,et al.  Localization of functional regions of human mesial cortex by somatosensory evoked potential recording and by cortical stimulation. , 1996, Electroencephalography and clinical neurophysiology.

[47]  S P Wise,et al.  Neuronal responses in sensorimotor cortex to ramp displacements and maintained positions imposed on hindlimb of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[48]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[49]  P. Goldman-Rakic,et al.  D1 receptors in prefrontal cells and circuits , 2000, Brain Research Reviews.

[50]  R. H. Evans,et al.  Excitatory amino acid transmitters. , 1981, Annual review of pharmacology and toxicology.

[51]  A Carlsson,et al.  Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. , 2001, Annual review of pharmacology and toxicology.

[52]  L Krubitzer,et al.  Area 3a: topographic organization and cortical connections in marmoset monkeys. , 2001, Cerebral cortex.

[53]  N Palomero-Gallagher,et al.  Receptor autoradiographic mapping of the mesial motor and premotor cortex of the macaque monkey , 1998, The Journal of comparative neurology.

[54]  Mika Otsuki,et al.  Pure apraxic agraphia with abnormal writing stroke sequences: report of a Japanese patient with a left superior parietal haemorrhage , 1999, Journal of neurology, neurosurgery, and psychiatry.

[55]  Howard F. Solomon,et al.  Autoradiography and correlative imaging , 1995 .

[56]  Riitta Hari,et al.  Activation of human mesial cortex during somatosensory target detection task , 1996, Brain Research.

[57]  A. Schleicher,et al.  Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry , 2002, European Neuropsychopharmacology.

[58]  B. Vogt,et al.  Human cingulate cortex: Surface features, flat maps, and cytoarchitecture , 1995, The Journal of comparative neurology.

[59]  K. Zilles,et al.  Cyto-, Myelo-, and Receptor Architectonics of the Human Parietal Cortex , 2001, NeuroImage.

[60]  A. Galaburda,et al.  Inferior parietal lobule. Divergent architectonic asymmetries in the human brain. , 1984, Archives of neurology.

[61]  K Amunts,et al.  A stereological approach to human cortical architecture: identification and delineation of cortical areas , 2000, Journal of Chemical Neuroanatomy.

[62]  A. Schleicher,et al.  The Somatosensory Cortex of Human: Cytoarchitecture and Regional Distributions of Receptor-Binding Sites , 1997, NeuroImage.

[63]  C. Woolsey Multiple somatic areas , 1981 .

[64]  C. Economo,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen , 1925 .

[65]  P. B. Cipolloni,et al.  Cytoarchitecture and cortical connections of the posterior cingulate and adjacent somatosensory fields in the rhesus monkey , 2004, The Journal of comparative neurology.

[66]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[67]  A. Levey,et al.  Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. , 2004, Progress in brain research.

[68]  F. Lacquaniti,et al.  Representing spatial information for limb movement: role of area 5 in the monkey. , 1995, Cerebral cortex.

[69]  P. Morosan,et al.  Observer-Independent Method for Microstructural Parcellation of Cerebral Cortex: A Quantitative Approach to Cytoarchitectonics , 1999, NeuroImage.

[70]  P. Goldman-Rakic,et al.  Dopamine receptor-interacting proteins: the Ca(2+) connection in dopamine signaling. , 2003, Trends in pharmacological sciences.