Broca's region: Cytoarchitectonic asymmetry and developmental changes

Functional imaging and clinical studies in children and adults have provided evidence of developmental changes in the hemispheric specialization for language. Whereas cytoarchitectonic asymmetry has been demonstrated in Broca's region of adults, the anatomical correlates of developmental changes in language dominance are largely unknown. In the present postmortem study of 34 human brains (ages ranging from 3.5 months to 85 years), the cytoarchitecture of areas 44 and 45 as the putative anatomical correlates of Broca's region, their developmental changes, and interhemispheric asymmetry were analyzed. Asymmetry as estimated by Euclidean distances between feature vectors of cytoarchitectonic profiles of left and right areas 44 and 45 was already found in 1‐year‐old infants. Asymmetry tended to increase with age, which was significant in area 45, but not in area 44. An adult‐like, left‐larger‐than‐right asymmetry in the volume fraction of cell bodies [gray level index (GLI)] was reached at approximately 5 years in area 45 and 11 years in area 44. These time points indicate a delayed development of the cytoarchitectonic asymmetry in Broca's region in comparison with that of the primary motor cortex. It may be hypothesized that the delayed maturation is the microstructural basis of the development of language abilities and the influence of language practice on cytoarchitecture during childhood. Interhemispheric asymmetry in the cytoarchitecture of areas 44 and 45 continues to change throughout life. We conclude that the cytoarchitectonic asymmetry of areas 44 and 45 is a result of microstructural plasticity that endures throughout almost the whole lifespan. J. Comp. Neurol. 465:72–89, 2003. © 2003 Wiley‐Liss, Inc.

[1]  H. Kretschmann,et al.  Different volume changes of cerebral cortex and white matter during histological preparation. , 1982, Microscopica acta.

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

[3]  O Schmitt,et al.  Systematic investigations of the contrast results of histochemical stainings of neurons and glial cells in the human brain by means of image analysis. , 1997, Micron.

[4]  E. Ringelstein,et al.  Language lateralization in healthy right-handers. , 2000, Brain : a journal of neurology.

[5]  P. Morosan,et al.  Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System , 2001, NeuroImage.

[6]  M. Koenderink,et al.  Postnatal maturation of the layer III pyramidal neurons in the human prefrontal cortex: a quantitative Golgi analysis , 1994, Brain Research.

[7]  A M Galaburda,et al.  Anatomical asymmetries in the adult and developing brain and their implications for function. , 1981, Advances in pediatrics.

[8]  F. Aboitiz,et al.  The evolutionary origin of the language areas in the human brain. A neuroanatomical perspective , 1997, Brain Research Reviews.

[9]  K. Zilles,et al.  Neurobiological bases of behavioral development in the first year. , 1997, Neuropediatrics.

[10]  K. Amunts,et al.  Broca’s language area from a neuroanatomical and developmental perspective , 2000 .

[11]  K. Skullerud.  Variations in the size of the human brain. Influence of age, sex, body length, body mass index, alcoholism, Alzheimer changes, and cerebral atherosclerosis. , 1985, Acta neurologica Scandinavica. Supplementum.

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

[13]  Arnold B. Scheibel,et al.  The postnatal development of the motor speech area: A preliminary study , 1989, Brain and Language.

[14]  B Milner,et al.  THE ROLE OF EARLY LEFT‐BRAIN INJURY IN DETERMINING LATERALIZATION OF CEREBRAL SPEECH FUNCTIONS , 1977, Annals of the New York Academy of Sciences.

[15]  B. Anderson,et al.  Age and hemisphere effects on dendritic structure. , 1996, Brain : a journal of neurology.

[16]  N. Geschwind,et al.  Developmental dyslexia: Four consecutive patients with cortical anomalies , 1985, Annals of neurology.

[17]  L. Katz,et al.  Brain morphology in normal and dyslexic children: The influence of sex and age , 1994, Annals of neurology.

[18]  K Zilles,et al.  A quantitative approach to cytoarchitectonics: Analysis of structural inhomogeneities in nervous tissue using an image analyser , 1990, Journal of microscopy.

[19]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[20]  H. Haug.  The Aging Human Cerebral Cortex: Morphometry of Areal Differences and Their Functional Meaning , 1989 .

[21]  A. Schleicher,et al.  The yakovlev collection A pilot study of its suitability for the morphometric documentation of the human brain , 1979, Journal of the Neurological Sciences.

[22]  G. Humphrey,et al.  Sex differences in infant reaching , 1987, Neuropsychologia.

[23]  R. A. Dtavidoff,et al.  Prolonged post-tetanic depolarization of frog dorsal root fibers , 1983, Neuroscience.

[24]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[25]  I. T. Draper.  Human Neuropsychology , 1979 .

[26]  M. Botez,et al.  Expressive aphasia and amusia following right frontal lesion in a right-handed man. , 1959, Brain : a journal of neurology.

[27]  V H Denenberg,et al.  A developmental study of sex and age interactions in the human corpus callosum. , 1992, Brain research. Developmental brain research.

[28]  R. Kraft,et al.  Longitudinal Change of Ear Advantage for Receptive Language Function in 2½ - to 9-Year-Old Children , 1994, Perceptual and motor skills.

[29]  P. Morosan,et al.  Probabilistic Mapping and Volume Measurement of Human Primary Auditory Cortex , 2001, NeuroImage.

[30]  S. Carey,et al.  Language deficits after apparent clinical recovery from childhood aphasia , 1979, Annals of neurology.

[31]  Marcel Kinsbourne,et al.  Phylogeny and ontogeny of cerebral lateralization. , 1995 .

[32]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[33]  E. Grober,et al.  Age, sex, and aphasia type. Evidence for a regional cerebral growth process underlying lateralization. , 1983, The Journal of nervous and mental disease.

[34]  L S Illis,et al.  Neurotrauma , 1998, Spinal Cord.

[35]  D. B. Tower,et al.  THE ACTIVITIES OF BUTYRYLCHOLINESTERASE AND CARBONIC ANHYDRASE, THE RATE OF ANAEROBIC GLYCOLYSTS, AND THE QUESTION OF A CONSTANT DENSITY OF GLIAL CELLS IN CEREBRAL CORTICES OF VARIOUS MAMMALIAN SPECIES FROM MOUSE TO WHALE , 1973, Journal of neurochemistry.

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

[37]  de Brabander,et al.  Layer‐specific dendritic regression of pyramidal cells with ageing in the human prefrontal cortex , 1998, The European journal of neuroscience.

[38]  V. Schmithorst,et al.  Normal fMRI Brain Activation Patterns in Children Performing a Verb Generation Task , 2001, NeuroImage.

[39]  K. Amunts,et al.  Advances in cytoarchitectonic mapping of the human cerebral cortex. , 2001, Neuroimaging clinics of North America.

[40]  E. Plante,et al.  ELEVATED ANDROGEN, BRAIN DEVELOPMENT AND LANGUAGE/LEARNING DISABILITIES IN CHILDREN WITH CONGENITAL ADRENAL HYPERPLASIA , 1996, Developmental medicine and child neurology.

[41]  M. Marín‐Padilla,et al.  Prenatal and early postnatal ontogenesis of the human motor cortex: a golgi study. I. The sequential development of the cortical layers. , 1970, Brain research.

[42]  A. Schleicher,et al.  Structural Asymmetries in the Human Forebrain and the Forebrain of Non-human Primates and Rats , 1996, Neuroscience & Biobehavioral Reviews.

[43]  M. Mishkin,et al.  Onset of speech after left hemispherectomy in a nine-year-old boy. , 1997, Brain : a journal of neurology.

[44]  E. J. Field,et al.  Das zentralnervensystem in Zahlen und Tabellen , 1970 .

[45]  S. F. Witelson,et al.  Left hemisphere specialization for language in the newborn. Neuroanatomical evidence of asymmetry. , 1973, Brain : a journal of neurology.

[46]  Neurobiological bases of behavioral development in the second year. , 1999, Neuropediatrics.

[47]  W R Shankle,et al.  Approximate Doubling of Numbers of Neurons in Postnatal Human Cerebral Cortex and in 35 Specific Cytoarchitectural Areas from Birth to 72 Months , 1999, Pediatric and developmental pathology : the official journal of the Society for Pediatric Pathology and the Paediatric Pathology Society.

[48]  G. Yeni-Komshian,et al.  Discrimination and identification of voicing and place contrasts in aphasic patients. , 1982, Canadian journal of psychology.

[49]  P. Simos,et al.  Behavioral and Electrophysiological Indices of Voicing-Cue Discrimination: Laterality Patterns and Development , 1997, Brain and Language.

[50]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

[51]  P. Coleman,et al.  Dendritic growth in the aged human brain and failure of growth in senile dementia. , 1979, Science.

[52]  A. Kertesz,et al.  The epidemiology of aphasic and cognitive impairment in stroke: age, sex, aphasia type and laterality differences. , 1981, Brain : a journal of neurology.

[53]  E. Haacke,et al.  Hemispheric Language Dominance in Children Demonstrated by Functional Magnetic Resonance Imaging , 1999, Journal of child neurology.

[54]  R E Carson,et al.  Altered patterns of cerebral activity during speech and language production in developmental stuttering. An H2(15)O positron emission tomography study. , 1997, Brain : a journal of neurology.

[55]  Karl Zilles,et al.  Estimation of volume fractions in nervous tissue with an image analyzer , 1982, Journal of Neuroscience Methods.

[56]  A. Scheibel,et al.  A quantitative dendritic analysis of wernicke's area in humans. I. Lifespan changes , 1993, The Journal of comparative neurology.

[57]  T. Rasmussen,et al.  INTRACAROTID INJECTION OF SODIUM AMYTAL FOR THE LATERALIZATION OF CEREBRAL SPEECH DOMINANCE EXPERIMENTAL AND CLINICAL OBSERVATIONS , 1960 .

[58]  P. Kuhl,et al.  Cross-language analysis of phonetic units in language addressed to infants. , 1997, Science.

[59]  D. Ingvar,et al.  Disturbances of speech prosody following right hemisphere infarcts , 1991, Acta neurologica Scandinavica.

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

[61]  P. Broca.  Remarques sur le siège de la faculté du langage articulé, suivies d'une observation d'aphémie (perte de la parole) , 1861 .

[62]  David A. Ziegler,et al.  Abnormal asymmetry in language association cortex in autism , 2002, Annals of neurology.

[63]  Y. Grodzinsky.  The neurology of syntax: Language use without Broca's area , 2000, Behavioral and Brain Sciences.

[64]  Karl Zilles,et al.  Postnatal development of interhemispheric asymmetry in the cytoarchitecture of human area 4 , 1997, Anatomy and Embryology.

[65]  Alfonso Caramazza,et al.  The perception and production of Voice-Onset Time in aphasia , 1977, Neuropsychologia.

[66]  K Amunts,et al.  Quantitative analysis of sulci in the human cerebral cortex: Development, regional heterogeneity, gender difference, asymmetry, intersubject variability and cortical architecture , 1997, Human brain mapping.

[67]  Karl Zilles,et al.  Ontogenesis of the laminar structure in areas 17 and 18 of the human visual cortex , 2004, Anatomy and Embryology.

[68]  T. Rasmussen,et al.  INTRACAROTID SODIUM AMYTAL FOR THE LATERALIZATION OF CEREBRAL SPEECH DOMINANCE; OBSERVATIONS IN 123 PATIENTS. , 1964, Journal of neurosurgery.

[69]  H. Uylings,et al.  Postnatal maturation of layer V pyramidal neurons in the human prefrontal cortex. A quantitative Golgi analysis , 1995, Brain Research.

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

[71]  R. Müller,et al.  Language organization in patients with early and lateleft-hemisphere lesion: a pet study , 1999, Neuropsychologia.

[72]  Paul D. Coleman,et al.  Quantitative evidence for selective dendritic growth in normal human aging but not in senile dementia , 1981, Brain Research.

[73]  W R Shankle,et al.  The development of structure and function in the postnatal human cerebral cortex from birth to 72 months: changes in thickness of layers II and III co-relate to the onset of new age-specific behaviors. , 2002, Pediatric pathology & molecular medicine.

[74]  D. Molfese.  Predicting Dyslexia at 8 Years of Age Using Neonatal Brain Responses , 2000, Brain and Language.

[75]  R. Ingham,et al.  A PET study of the neural systems of stuttering , 1996, Nature.

[76]  A. Basso,et al.  Traumatic Aphasia in Children and Adults: A Comparison of Clinical Features and Evolution , 1990, Cortex.

[77]  G M Innocenti,et al.  Forms and measures of adult and developing human corpus callosum: Is there sexual dimorphism? , 1989, The Journal of comparative neurology.

[78]  C. Leonard,et al.  Anomalous cerebral structure in dyslexia revealed with magnetic resonance imaging. , 1993, Archives of neurology.

[79]  J. Piven,et al.  Structural and functional magnetic resonance imaging of autism , 2002, International Journal of Developmental Neuroscience.

[80]  P. Huttenlocher.  Morphometric study of human cerebral cortex development , 1990, Neuropsychologia.

[81]  Otto Muzik,et al.  Impairment of dentato-thalamo-cortical pathway in autistic men: language activation data from positron emission tomography , 1998, Neuroscience Letters.

[82]  P. Pietrini,et al.  Where the brain appreciates the moral of a story. , 1995, Neuroreport.

[83]  William D Gaillard,et al.  A functional magnetic resonance imaging study of left hemisphere language dominance in children. , 2002, Archives of neurology.

[84]  W. Meier-Ruge,et al.  Age‐Related White Matter Atrophy in the Human Brain , 1992, Annals of the New York Academy of Sciences.

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

[86]  Donna B. Pincus,et al.  Distinguishing Lies from Jokes: Theory of Mind Deficits and Discourse Interpretation in Right Hemisphere Brain-Damaged Patients , 1998, Brain and Language.

[87]  E. Capitani,et al.  Factors Influencing Type and Severity of Aphasia , 1980, Cortex.

[88]  Y. Joanette,et al.  Age-related evolution of the contribution of the right hemisphere to language: absence of evidence. , 1999, The International journal of neuroscience.

[89]  Robert Minahan,et al.  Language recovery after left hemispherectomy in children with late‐onset seizures , 1999, Annals of neurology.

[90]  D. Le Bihan,et al.  Noninvasive assessment of language dominance in children and adolescents with functional MRI , 1997, Neurology.

[91]  P. Coleman,et al.  Dendritic proliferation in the aging brain as a compensatory repair mechanism. , 1986, Progress in brain research.

[92]  A. Schleicher,et al.  Asymmetry in the Human Motor Cortex and Handedness , 1996, NeuroImage.

[93]  Paul D. Coleman,et al.  Neuron numbers and dendritic extent in normal aging and Alzheimer's disease , 1987, Neurobiology of Aging.

[94]  L. Jäncke,et al.  Normal intrasylvian anatomical asymmetry in children with developmental language disorder , 1998, Neuropsychologia.

[95]  J A Wada,et al.  Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adults and 100 infant brains. , 1975, Archives of neurology.

[96]  P. Jusczyk,et al.  Infants' memory for spoken words. , 1997, Science.