Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry

The postnatal establishment of cortical connectivity was studied by estimating the number (numerical density, synapse‐to‐neuron ratio, and total number) of the overall synaptic population and its distribution into gamma‐aminobutyric acid (GABA)‐immunopositive and GABA‐immunonegative synaptic contacts in the developing rat somatosensory cortex. These numerical data were obtained using the unbiased disector method in combination with GABA postembedding immunocytochemistry. The numerical density of both synaptic populations was low in the early postnatal period (postnatal days 5 and 10, P5, P10) after which it abruptly increased between P10 and P15 to approach adult values. However, since cortical volume continues to increase after this age, the number of synapses per neuron and the total number of synapses reached adult values only by P30. There was no evidence of overproduction of either GABA or non‐GABA synapses. Direct comparison between the two synaptic populations revealed a similar developmental pattern with the exception of the period around P20 when the production of GABA synapses slowed down. Thus, while the formation of non‐GABA synapses proceeded in a continuous manner throughout the first month of life, GABA synapse production was accomplished in two consecutive waves. We suggest that the second delayed wave of GABA synapse formation is related to the great developmental plasticity of the cortical inhibitory system. © 1996 Wiley‐Liss, Inc.

[1]  P. Somogyi,et al.  Targets and Quantitative Distribution of GABAergic Synapses in the Visual Cortex of the Cat , 1990, The European journal of neuroscience.

[2]  A. Sillito Functional Considerations of the Operation of GABAergic Inhibitory Processes in the Visual Cortex , 1984 .

[3]  L. Descarries,et al.  Regional and laminar density of the dopamine innervation in adult rat cerebral cortex , 1987, Neuroscience.

[4]  E. Weibel Practical methods for biological morphometry , 1979 .

[5]  M. Nicolelis,et al.  Development of direct GABAergic projections from the zona incerta to the somatosensory cortex of the rat , 1995, Neuroscience.

[6]  L. Descarries,et al.  Ultrastructural basis of monoamine and acetylcholine function in CNS , 1995 .

[7]  B. Connors,et al.  Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. , 1989, Journal of neurophysiology.

[8]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis , 1983, Journal of neurocytology.

[9]  A. Agmon,et al.  NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition. , 1992, Journal of neurophysiology.

[10]  P. Rakić,et al.  Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. , 1989, Brain research. Developmental brain research.

[11]  L. Benevento,et al.  The effects of dark-rearing on the electrophysiology of the rat visual cortex , 1992, Brain Research.

[12]  D. C. Sterio The unbiased estimation of number and sizes of arbitrary particles using the disector , 1984, Journal of microscopy.

[13]  A. Schousboe,et al.  Neurotransmitters as developmental signals , 1991, Neurochemistry International.

[14]  M. Colonnier,et al.  Postnatal changes in the number of neurons and synapses in the visual cortex (area 17) of the macaque monkey: A stereological analysis in normal and monocularly deprived animals , 1982, The Journal of comparative neurology.

[15]  E. G. Jones,et al.  Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  C. Beaulieu,et al.  Equivalent cell density in three areas of neonatal rat cerebral cortex , 1994, Neuroscience Letters.

[17]  M. Colonnier,et al.  A laminar analysis of the number of round‐asymmetrical and flat‐symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat , 1985, The Journal of comparative neurology.

[18]  F E Bloom,et al.  The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. , 1967, Brain research.

[19]  R. Dykes,et al.  Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition , 1983, Brain Research.

[20]  L. Descarries,et al.  Quantified regional and laminar distribution of the serotonin innervation in the anterior half of adult rat cerebral cortex. , 1989, Journal of chemical neuroanatomy.

[21]  James E. Vaughn,et al.  Review: Fine structure of synaptogenesis in the vertebrate central nervous system , 1989 .

[22]  J. Hablitz,et al.  Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. , 1993, Journal of neurophysiology.

[23]  C. Beaulieu,et al.  Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat , 1994, The Journal of comparative neurology.

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

[25]  W Wisden,et al.  The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  D. Winfield The postnatal development of synapses in the visual cortex of the cat and the effects of eyelid closure , 1981, Brain Research.

[27]  J. Barker,et al.  Differential and transient expression of GABAA receptor alpha-subunit mRNAs in the developing rat CNS , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D. Prince,et al.  Postnatal maturation of the GABAergic system in rat neocortex. , 1991, Journal of neurophysiology.

[30]  G. Rager,et al.  Synaptogenesis in the primary visual cortex of the tree shrew (Tupaia belangeri) , 1991, The Journal of comparative neurology.

[31]  Rafael Yuste,et al.  Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters , 1991, Neuron.

[32]  K. Micheva,et al.  Postnatal Development of GABA Neurons in the Rat Somatosensory Barrel Cortex: A Quantitative Study , 1995, The European journal of neuroscience.

[33]  D. Kristt Development of neocortical circuitry: Quantitative ultrastructural analysis of putative monoaminergic synapses , 1979, Brain Research.

[34]  J R Wolff,et al.  Pre‐ and postnatal development of the primary visual cortex of the common marmoset. II. Formation, remodelling, and elimination of synapses as overlapping processes , 1993, The Journal of comparative neurology.

[35]  Prof. Dr. Karl Zilles The Cortex of the Rat , 1985, Springer Berlin Heidelberg.

[36]  Kristina D. Micheva,et al.  An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[37]  L. Descarries,et al.  Quantified regional and laminar distribution of the noradrenaline innervation in the anterior half of the adult rat cerebral cortex , 1988, The Journal of comparative neurology.

[38]  T. Woolsey,et al.  Templates for locating the whisker area in fresh flattened mouse and rat cortex , 1987, Journal of Neuroscience Methods.

[39]  D. Simons,et al.  Early experience of tactile stimulation influences organization of somatic sensory cortex , 1987, Nature.

[40]  K. Micheva,et al.  Neonatal sensory deprivation induces selective changes in the quantitative distribution of GABA‐immunoreactive neurons in the rat barrel field cortex , 1995, The Journal of comparative neurology.

[41]  J. O’Kusky,et al.  Synapse elimination in the developing visual cortex: a morphometric analysis in normal and dark-reared cats. , 1985, Brain research.

[42]  M. Cynader,et al.  Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). , 1992, Cerebral cortex.

[43]  K. Fox,et al.  A critical period for experience-dependent synaptic plasticity in rat barrel cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  J. Wolff,et al.  Development of GABA-ergic system in rat visual cortex. , 1984, Advances in experimental medicine and biology.

[45]  Roger B. H. Tootell,et al.  Modified technique for cytochrome oxidase histochemistry: increased staining intensity and compatibility with 2-deoxyglucose autoradiography , 1987, Journal of Neuroscience Methods.

[46]  P S Goldman-Rakic,et al.  Synaptogenesis in the prefrontal cortex of rhesus monkeys. , 1994, Cerebral cortex.

[47]  G. Vrensen,et al.  Postnatal development of neurons and synapses in the visual and motor cortex of rabbits: A quantitative light and electron microscopic study , 1977, Brain Research Bulletin.

[48]  B. Schlaggar,et al.  Early development of the somatotopic map and barrel patterning in rat somatosensory cortex , 1994, The Journal of comparative neurology.

[49]  D. Prince,et al.  Cellular and synaptic physiology and epileptogenesis of developing rat neocortical neurons in vitro. , 1987, Brain research.

[50]  W. Welker Analysis of Sniffing of the Albino Rat 1) , 1964 .

[51]  P. Somogyi,et al.  Antisera to gamma-aminobutyric acid. II. Immunocytochemical application to the central nervous system. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[52]  Y. Ben-Ari,et al.  GABA: an excitatory transmitter in early postnatal life , 1991, Trends in Neurosciences.

[53]  E. G. Jones,et al.  Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17 , 1986, Nature.