Glial hypertrophy is associated with synaptogenesis following motor‐skill learning, but not with angiogenesis following exercise

Rats reared from weaning in a complex environment have an increase in (1) glial surface area, (2) capillary volume, and (3) the number of synapses, per neuron. In that paradigm it has not been possible to determine whether the glial increase more closely correlates with the increase in synaptic numbers or with angiogenesis. More recently we have found that rats that exercised had an increase in the density of capillaries without an increase in the synaptic numbers, whereas rats that learned new motor skills had a greater number of synapses per neuron without an increase in the density of capillaries. Those findings provided the opportunity to investigate whether changes in glial volume in the cerebellum correspond to changes in the number of synapses or in capillary volume. Glial area fraction estimates were obtained using point counts on electron micrographs from the previous studies. The skill learning group had a greater volume of molecular layer per Purkinje cell, and also a greater volume of glia per Purkinje cell, than rats in either an inactive group or rats in two exercise groups. No significant differences were found in glial volume per synapse and glial volume per capillary across groups, although there was a tendency for glial volume per capillary to be lower in the exercise groups. The data indicate that glial volume correlates with synaptic numbers and not with capillary density. © 1994 Wiley‐Liss, Inc.

[1]  R. Herndon,et al.  Astrocytes play a role in regulation of synaptic density , 1987, Brain Research.

[2]  S. Palay,et al.  Cerebellar Cortex: Cytology and Organization , 1974 .

[3]  H. J. G. GUNDERSEN,et al.  Some new, simple and efficient stereological methods and their use in pathological research and diagnosis , 1988, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[4]  J. Grosche,et al.  NMDA-activated currents in Bergmann glial cells. , 1993, Neuroreport.

[5]  W. Greenough,et al.  Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron , 1985, Brain Research.

[6]  H. S. Bennett,et al.  Morphological classifications of vertebrate blood capillaries. , 1959, The American journal of physiology.

[7]  Stephen J. Smith,et al.  The excitatory neurotransmitter glutamate causes filopodia formation in cultured hippocampal astrocytes , 1990, Glia.

[8]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[9]  J. Turner,et al.  Morphology of astroglial cells is controlled by beta-adrenergic receptors , 1987, The Journal of cell biology.

[10]  W. Greenough,et al.  Exercise and the Brain: Angiogenesis in the Adult Rat Cerebellum after Vigorous Physical Activity and Motor Skill Learning , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[11]  C. Tweedle,et al.  Magnocellular neuropeptidergic neurons in hypothalamus: Increases in membrane apposition and number of specialized synapses from pregnancy to lactation , 1982, Brain Research Bulletin.

[12]  Stephen J. Smith,et al.  Neuronal activity triggers calcium waves in hippocampal astrocyte networks , 1992, Neuron.

[13]  J. Sutin,et al.  Expression of adrenergic receptors in individual astrocytes and motor neurons isolated from the adult rat brain , 1992, Glia.

[14]  Cavanagh Jb,et al.  The proliferation of astrocytes around a needle wound in the rat brain. , 1970 .

[15]  S. Murphy,et al.  The role of polyphosphoinositides in agonist-evoked release of vasoactive factors from astrocytes. , 1992, Progress in brain research.

[16]  A. Beaudet,et al.  Autoradiographic localization of specific kainic acid binding sites in pigeon and rat cerebellum , 1981, Brain Research.

[17]  W. Greenough,et al.  Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites, and capillaries , 1987, Brain Research.

[18]  W. Greenough,et al.  Astrocytic and synaptic response to kindling in hippocampal subfield CA1. I. Synaptogenesis in response to kindling in vitro , 1993, Brain Research.

[19]  H. Kimelberg,et al.  Excitatory amino acids directly depolarize rat brain astrocytes in primary culture , 1984, Nature.

[20]  M. Norenberg,et al.  Microvessels Isolated from Rat Brain: Localization of Astrocyte Processes by Immunohistochemical Techniques , 1981, Journal of neurochemistry.

[21]  C. Müller,et al.  Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes , 1989, Nature.

[22]  C. Meshul,et al.  Transplanted astrocytes reduce synaptic density in the neuropil of cerebellar cultures , 1988, Brain Research.

[23]  E. Rubel,et al.  Rapid and reversible astrocytic reaction to afferent activity blockade in chick cochlear nucleus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  M. Leon,et al.  Elaboration of glial cell processes in the rat olfactory bulb associated with early learning , 1993, Brain Research.

[25]  H. J. G. Gundersen,et al.  The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis , 1988, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[26]  B. Cragg,et al.  Estimation of the number of synapses in a volume of nervous tissue from counts in thin sections by electron microscopy , 1974, Journal of neurocytology.

[27]  W. Greenough,et al.  Plasticity of GFAP-immunoreactive astrocyte size and number in visual cortex of rats reared in complex environments , 1991, Brain Research.

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

[29]  M. Krug,et al.  The influence of long-term potentiation on the spatial relationship between astrocyte processes and potentiated synapses in the dentate gyrus neuropil of rat brain , 1991, Brain Research.

[30]  P. Somogyi,et al.  Subcellular localization of a putative kainate receptor in Bergmann glial cells using a monoclonal antibody in the chick and fish cerebellar cortex , 1990, Neuroscience.

[31]  W. Greenough,et al.  Astrocytic and synaptic response to kindling in hippocampal subfield CA1. II. Synaptogenesis and astrocytic process increases to in vivo kindling , 1993, Brain Research.

[32]  E. Weibel Stereological Methods. Practical methods for biological morphometry , 1979 .

[33]  P. Rakić,et al.  Neuron‐glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electonmicroscopic study in Macacus rhesus , 1971, The Journal of comparative neurology.

[34]  F. Eckenstein,et al.  Induction of dendritic spine proliferation by an astrocyte secreted factor , 1992, Experimental Neurology.

[35]  A. Schousboe,et al.  Regulatory role of astrocytes for neuronal biosynthesis and homeostasis of glutamate and GABA. , 1992, Progress in brain research.

[36]  W. Greenough,et al.  Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[37]  T. Berger,et al.  Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells. , 1992, Science.

[38]  David Krech,et al.  Increases in cortical depth and glia numbers in rats subjected to enriched environment , 1966, The Journal of comparative neurology.