Regional Dendritic Variation in Neonatal Human Cortex: A Quantitative Golgi Study

The present study quantitatively compared the basilar dendritic/spine systems of lamina V pyramidal neurons across four hierarchically arranged regions of neonatal human neocortex. Tissue blocks were removed from four Brodmann’s areas (BAs) in the left hemisphere of four neurologically normal neonates (mean age = 41 ± 40 days): primary (BA4 and BA3-1-2), unimodal (BA18), and supramodal cortices (BA10). Tissue was stained with a modified rapid Golgi technique. Ten cells per region (N = 160) were quantified. Despite the small sample size, significant differences in dendritic/spine extent obtained across cortical regions. Most apparent were substantial differences between BA4 and BA10: total dendritic length was 52% greater in BA4 than BA10, and dendritic spine number was 67% greater in BA4 than BA10. Neonatal patterns were compared to adult patterns, revealing that the relative regional pattern of dendritic complexity in the neonate was roughly the inverse of that established in the adult, with BA10 rather than BA4 being the most complex area in the adult. Overall, regional dendritic patterns suggest that the developmental time course of basilar dendritic systems is heterochronous and is more protracted for supramodal BA10 than for primary or unimodal regions (BA4, BA3-1-2, BA18).

[1]  J. Schadé,et al.  Quantitative Analysis of Neuronal Parameters in the Maturing Cerebral Cortex , 1964 .

[2]  L. Becker,et al.  Morphology of the Developing Visual Cortex of the Human Infant: A Quantitative and Qualitative Golgi Study , 1980, Journal of neuropathology and experimental neurology.

[3]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[4]  H. Lange,et al.  Qualitative and quantitative development of the visual cortex in man , 1983 .

[5]  G. Schroth,et al.  Brain development (sulci and gyri) as assessed by early postnatal MR imaging in preterm and term newborn infants. , 2001, Neuropediatrics.

[6]  M. L. Pucak,et al.  Synaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cortex , 1998, The Journal of comparative neurology.

[7]  I. Akiguchi,et al.  Age-related changes of pyramidal cell basal dendrites in layers III and V of human motor cortex: A quantitative Golgi study , 2004, Acta Neuropathologica.

[8]  G. Elston,et al.  Pyramidal Cells, Patches, and Cortical Columns: a Comparative Study of Infragranular Neurons in TEO, TE, and the Superior Temporal Polysensory Area of the Macaque Monkey , 2000, The Journal of Neuroscience.

[9]  G. Elston,et al.  Complex dendritic fields of pyramidal cells in the frontal eye field of the macaque monkey: comparison with parietal areas 7a and LIP , 1998, Neuroreport.

[10]  M. Segal,et al.  Morphological plasticity in dendritic spines of cultured hippocampal neurons , 1996, Neuroscience.

[11]  Garey Lj,et al.  The development of dendritic spines in the human visual cortex. , 1984 .

[12]  D F Benson.  Prefrontal abilities. , 1993, Behavioural neurology.

[13]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[14]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.

[15]  L. Becker,et al.  Dendritic development in human occipital cortical neurons. , 1984, Brain research.

[16]  M. E. Cordero,et al.  Dendritic development in neocortex of infants with early postnatal life undernutrition. , 1993, Pediatric neurology.

[17]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

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

[19]  D. Benson,et al.  The neurology of thinking , 1994 .

[20]  A. Scheibel,et al.  Chapter 4 – The Methods of Golgi , 1978 .

[21]  G. Elston.  Pyramidal Cells of the Frontal Lobe: All the More Spinous to Think With , 2000, The Journal of Neuroscience.

[22]  J. Stone,et al.  Major glutamatergic projection from subplate into visual cortex during development , 1998, The Journal of comparative neurology.

[23]  M G Rosa,et al.  Comparison of dendritic fields of layer III pyramidal neurons in striate and extrastriate visual areas of the marmoset: a Lucifer yellow intracellular injection. , 1996, Cerebral cortex.

[24]  A. Larkman,et al.  Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions , 1991, The Journal of comparative neurology.

[25]  H. Uylings,et al.  Morphometric dendritic field analysis of pyramidal neurons in the human prefrontal cortex: relation to section thickness , 1996, Journal of Neuroscience Methods.

[26]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[27]  M. Phelps,et al.  Developmental changes in brain metabolism in sedated rhesus macaques and vervet monkeys revealed by positron emission tomography. , 1995, Cerebral cortex.

[28]  Features of the ensemble organization of the human cerebral cortex from birth to 20 years of age , 1990, Neuroscience and Behavioral Physiology.

[29]  A. Scheibel,et al.  A quantitative dendritic analysis of wernicke's area in humans. II. Gender, hemispheric, and environmental factors , 1993, The Journal of comparative neurology.

[30]  J. Morrison,et al.  Quantitative analysis of the dendritic morphology of corticocortical projection neurons in the macaque monkey association cortex , 2002, Neuroscience.

[31]  J P SCHADE,et al.  Structural organization of the human cerebral cortex. 1. Maturation of the middle frontal gyrus. , 1961, Acta anatomica.

[32]  J. D. E. Gabrieli,et al.  Integration of diverse information in working memory within the frontal lobe , 2000, Nature Neuroscience.

[33]  G. Elston,et al.  Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. , 1998, Cerebral cortex.

[34]  I. Kostović,et al.  Prenatal development of neurons in the human prefrontal cortex. II. A quantitative Golgi study , 1992, The Journal of comparative neurology.

[35]  Bob Jacobs,et al.  Regional Dendritic Variation in Primate Cortical Pyramidal Cells , 2002 .

[36]  H. Uylings,et al.  Neuronal development in human prefrontal cortex in prenatal and postnatal stages. , 1990, Progress in brain research.

[37]  Adele Diamond,et al.  Frontal lobe involvement in cognitive changes during the first year of life. , 1991 .

[38]  John Q. Trojanowski,et al.  Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents , 1977, Brain Research.

[39]  D. Purpura,et al.  Quantitative analysis of the spatial distribution of axonal and dendritic terminals of hippocampal pyramidal neurons in immature human brain , 1979, Experimental Neurology.

[40]  Christopher S. Monk,et al.  Mechanisms of Postnatal Neurobiological Development: Implications for Human Development , 2001, Developmental neuropsychology.

[41]  P. Huttenlocher.  Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[42]  V. Mountcastle.  The evolution of ideas concerning the function of the neocortex. , 1995, Cerebral cortex.

[43]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

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

[45]  L. Garey,et al.  The development of dendritic spines in the human visual cortex. , 1984, Human neurobiology.

[46]  C. Shatz,et al.  Subplate pioneers and the formation of descending connections from cerebral cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  G. Micheletti.  The Prefrontal Cortex. Anatomy, Physiology and Neuropsychology of the Frontal Lobe, Fuster J.M.. Raven Press, New York (1989) , 1989 .

[48]  I. Kostović,et al.  Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study , 1988, The Journal of comparative neurology.

[49]  P. Goldman-Rakic,et al.  Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate Galago, with comparative comments on anthropoid primates , 1991, The Journal of comparative neurology.

[50]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[51]  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.

[52]  P. E. Roland,et al.  Metabolic measurements of the working frontal cortex in man , 1984, Trends in Neurosciences.

[53]  J. Fuster.  Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[54]  L. L. Porter,et al.  Morphological Characterization of a Cortico-cortical relay in the cat sensorimotor cortex. , 1997, Cerebral cortex.

[55]  G. Elston,et al.  Cortical integration in the visual system of the macaque monkey: large-scale morphological differences in the pyramidal neurons in the occipital, parietal and temporal lobes , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[57]  G. Elston.  Pyramidal cell heterogeneity in the visual cortex of the nocturnal new world owl monkey (aotus trivirgatus) , 2003, Neuroscience.

[58]  O. Andreassen,et al.  Mice Deficient in Cellular Glutathione Peroxidase Show Increased Vulnerability to Malonate, 3-Nitropropionic Acid, and 1-Methyl-4-Phenyl-1,2,5,6-Tetrahydropyridine , 2000, The Journal of Neuroscience.

[59]  Koichii Tanaka,et al.  Recruitment order and dendritic morphology of rat phrenic motoneurons , 1996, The Journal of comparative neurology.

[60]  P S Goldman-Rakic,et al.  Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain , 1983, The Journal of comparative neurology.

[61]  T. Wiesel,et al.  Targets of horizontal connections in macaque primary visual cortex , 1991, The Journal of comparative neurology.

[62]  B. Jacobs,et al.  Life‐span dendritic and spine changes in areas 10 and 18 of human cortex: A quantitative golgi study , 1997, The Journal of comparative neurology.

[63]  G. Elston,et al.  The Pyramidal Cell in Cognition: A Comparative Study in Human and Monkey , 2001, The Journal of Neuroscience.

[64]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[65]  R. S. Williams,et al.  THE GOLGI RAPID METHOD IN CLINICAL NEUROPATHOLOGY: THE MORPHOLOGIC CONSEQUENCES OF SUBOPTIMAL FIXATION , 1978, Journal of neuropathology and experimental neurology.

[66]  C. Horner,et al.  Methods of estimation of spine density--are spines evenly distributed throughout the dendritic field? , 1991, Journal of anatomy.

[67]  Kathleen R. Gibson,et al.  Myelination and behavioral development: A comparative perspective on questions of neoteny, altriciality and intelligence. , 1991 .

[68]  D. Lewis,et al.  Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. , 2000, Cerebral cortex.

[69]  P. Huttenlocher,et al.  The development of synapses in striate cortex of man. , 1987, Human neurobiology.

[70]  J. Fuster.  Cortical dynamics of memory. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[71]  G. Elston.  Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. , 2003, Cerebral cortex.

[72]  C. M. Lee.  Growth and Development of Children , 1959 .

[73]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[74]  K. Rockland,et al.  The pyramidal cell of the sensorimotor cortex of the macaque monkey: phenotypic variation. , 2002, Cerebral cortex.

[75]  J. D. Ruiter.  The influence of post-mortem fixation delay on the reliability of the Golgi silver impregnation , 1983, Brain Research.

[76]  GUY N. ELSTO,et al.  Cortical heterogeneity : Implications for visual processing and polysensory integration , 2022 .

[77]  J. Trojanowski,et al.  Prefrontal granular cortex of the rhesus monkey. II. Interhemispheric cortical afferents , 1977, Brain Research.

[78]  M. Phelps,et al.  Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. , 1986, Science.

[79]  C. Shatz,et al.  Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons , 1987, Nature.

[80]  G. Elston,et al.  The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. , 1997, Cerebral cortex.

[81]  M Marín-Padilla,et al.  Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: A unifying theory , 1992, The Journal of comparative neurology.