Developmental Regulation of Basket/Stellate Cell→Purkinje Cell Synapses in the Cerebellum

We used paired recordings to study the development of synaptic transmission between inhibitory interneurons of the molecular layer and Purkinje cells in the cerebellar cortex of the rat. The electrophysiological data were combined with a morphological study of the recorded cells using biocytin or Lucifer yellow staining. Thirty-one interneuron–Purkinje cell pairs were obtained, and 11 of them were recovered morphologically. The age of the rats ranged from 11 to 31 d after birth. During this period synaptic maturation resulted in an 11-fold decrease in the average current evoked in a Purkinje cell by a spike in a presynaptic interneuron. Unitary IPSCs in younger animals exhibited paired-pulse depression, whereas paired-pulse facilitation was found in more mature animals. These data suggest that reduction in transmitter release probability contributed to the developmental decrease of unitary IPSCs. However, additional mechanisms at both presynaptic and postsynaptic loci should also be considered. The decrease of the average synaptic current evoked in a Purkinje cell by an action potential in a single interneuron suggests that as development proceeds interneuron activities must be coordinated to inhibit efficiently Purkinje cells.

[1]  B. Katz,et al.  Quantal components of the end‐plate potential , 1954, The Journal of physiology.

[2]  M. Kuno Quantal components of excitatory synaptic potentials in spinal motoneurones , 1964, The Journal of physiology.

[3]  A. R. Martin,et al.  Quantal Nature of Synaptic Transmission , 1966 .

[4]  R Llinás,et al.  The action of antidromic impulses on the cerebellar Purkinje cells , 1966, The Journal of physiology.

[5]  A Mallart,et al.  The relation between quantum content and facilitation at the neuromuscular junction of the frog , 1968, The Journal of physiology.

[6]  J. Altman,et al.  Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer , 1972, The Journal of comparative neurology.

[7]  M. Berry,et al.  The growth of the dendritic trees of Purkinje cells in the cerebellum of the rat , 1976, Brain Research.

[8]  B. Sakmann,et al.  Change in synaptic channel gating during neuromuscular development , 1978, Nature.

[9]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis , 1983, Journal of neurocytology.

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

[11]  R K Wong,et al.  Unitary inhibitory synaptic potentials in the guinea‐pig hippocampus in vitro. , 1984, The Journal of physiology.

[12]  Idan Segev,et al.  Space-Clamp Problems When Voltage Clamping Branched Neurons With Intracellular Microelectrodes , 1985 .

[13]  M. Miller,et al.  Maturation of rat visual cortex. III. Postnatal morphogenesis and synaptogenesis of local circuit neurons. , 1986, Brain research.

[14]  Michael W. Miller Research reportMaturation of rat visual cortex. III. Postnatal morphogenesis and synaptogenesis of local circuit neurons , 1986 .

[15]  JW Propst,et al.  Correlations between active zone ultrastructure and synaptic function studied with freeze-fracture of physiologically identified neuromuscular junctions , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[17]  Y. Ben-Ari,et al.  Giant synaptic potentials in immature rat CA3 hippocampal neurones. , 1989, The Journal of physiology.

[18]  J. Clements A statistical test for demonstrating a presynaptic site of action for a modulator of synaptic amplitude , 1990, Journal of Neuroscience Methods.

[19]  Prof. Dr. Valentino Braitenberg,et al.  Anatomy of the Cortex , 1991, Studies of Brain Function.

[20]  K. Stratford,et al.  Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  T. M. Mayhew,et al.  Anatomy of the Cortex: Statistics and Geometry. , 1991 .

[22]  A. Konnerth,et al.  Synaptic‐ and agonist‐induced excitatory currents of Purkinje cells in rat cerebellar slices. , 1991, The Journal of physiology.

[23]  Shaul Hestrin,et al.  Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse , 1992, Nature.

[24]  J Midtgaard,et al.  Stellate cell inhibition of Purkinje cells in the turtle cerebellum in vitro. , 1992, The Journal of physiology.

[25]  J. Garthwaite,et al.  GABAB Receptors in the Parallel Fibre Pathway of Rat Cerebellum , 1992, The European journal of neuroscience.

[26]  J. Midtgaard Membrane properties and synaptic responses of Golgi cells and stellate cells in the turtle cerebellum in vitro. , 1992, The Journal of physiology.

[27]  Arne Møller,et al.  Total numbers of various cell types in rat cerebellar cortex estimated using an unbiased stereological method , 1993, Brain Research.

[28]  J J Jack,et al.  Solutions for transients in arbitrarily branching cables: II. Voltage clamp theory. , 1993, Biophysical journal.

[29]  H. Gerschenfeld,et al.  Inhibitory synaptic currents in stellate cells of rat cerebellar slices. , 1993, The Journal of physiology.

[30]  A. Thomson,et al.  Fluctuations in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex , 1993, Neuroscience.

[31]  G. Major,et al.  Solutions for transients in arbitrarily branching cables: III. Voltage clamp problems. , 1993, Biophysical journal.

[32]  R. Nicoll,et al.  Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. , 1993, Journal of neurophysiology.

[33]  B. Barbour Synaptic currents evoked in purkinje cells by stimulating individual granule cells , 1993, Neuron.

[34]  J. Walrond,et al.  Two structural adaptations for regulating transmitter release at lobster neuromuscular synapses , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Daniel Johnston,et al.  Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties , 1994, Trends in Neurosciences.

[36]  Peter Somogyi,et al.  Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites , 1994, Nature.

[37]  B. Walmsley,et al.  Counting quanta: Direct measurements of transmitter release at a central synapse , 1995, Neuron.

[38]  S. Siegelbaum,et al.  Regulation of hippocampal transmitter release during development and long-term potentiation. , 1995, Science.

[39]  I. Forsythe,et al.  Pre‐ and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. , 1995, The Journal of physiology.

[40]  Naiphinich Kotchabhakdi,et al.  Developmental Changes of Inhibitory Synaptic Currents in Cerebellar Granule Neurons: Role of GABAA Receptor α6 Subunit , 1996, The Journal of Neuroscience.

[41]  Lei Zhang,et al.  Generation of Cerebellar Interneurons from Dividing Progenitors in White Matter , 1996, Neuron.

[42]  S. Cull-Candy,et al.  Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. , 1996, The Journal of physiology.

[43]  A. Kriegstein,et al.  Excitatory GABA Responses in Embryonic and Neonatal Cortical Slices Demonstrated by Gramicidin Perforated-Patch Recordings and Calcium Imaging , 1996, The Journal of Neuroscience.

[44]  J. Altman,et al.  Development of the Cerebellar System: In Relation to Its Evolution, Structure, and Functions , 1996 .

[45]  A. Marty,et al.  Fluctuations of inhibitory postsynaptic currents in Purkinje cells from rat cerebellar slices. , 1996, The Journal of physiology.

[46]  C. Govind,et al.  Structural features of crayfish phasic and tonic neuromuscular terminals , 1996, The Journal of comparative neurology.

[47]  Mnh,et al.  Histologie du Système Nerveux de Lʼhomme et des Vertébrés , 1998 .