Dendritic sodium spikelets and low-threshold calcium spikes in turtle olfactory bulb granule cells.

Active dendritic membrane properties were investigated by whole cell recordings from adult turtle olfactory bulb granule cells. The laminar structure of the olfactory bulb allowed differential polarization of the distal apical dendrites versus the somatic part of the cells by an external electric field. Dendritic depolarization evoked small (approximately 10 mV) all-or-none depolarizing events of approximately 10-ms duration. These spikelets often occurred in bursts at high frequency (< or = 250 Hz); they were present despite the application of synaptic and gap junction antagonists, but were abolished by TTX and intracellularly applied QX314. The spikelets were interpreted as attenuated sodium spikes initiated in different branches of the granule cells dendrites. They occurred spontaneously, but could also be evoked by excitatory postsynaptic potentials (EPSPs) to the distal dendrites. Spikelets initiated by distal excitation could function as prepotentials for full sodium spikes, in part depending on the level of proximal depolarization. Somatic depolarization by the electric field evoked full sodium spikes as well as low-threshold calcium spikes (LTSs). Calcium imaging revealed that the electrophysiologically identified LTS evoked from the soma was associated with calcium transients in the proximal and the distal dendrites. Our data suggest that the LTS in the soma/proximal dendrites plays a major role in boosting excitability, thus contributing to the initiation of sodium spiking in this compartment. The results furthermore suggest that the LTS and the sodium spikes may act independently or cooperatively to regulate dendritic calcium influx.

[1]  C. Nicholson,et al.  A model for the polarization of neurons by extrinsically applied electric fields. , 1986, Biophysical journal.

[2]  R. Nicoll,et al.  Dendrodendritic inhibition: demonstration with intracellular recording. , 1980, Science.

[3]  C. Nicholson,et al.  Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. , 1986, The Journal of physiology.

[4]  J. Midtgaard Processing of information from different sources: spatial synaptic integration in the dendrites of vertebrate CNS neurons , 1994, Trends in Neurosciences.

[5]  Jeffry S. Isaacson,et al.  Mechanisms governing dendritic γ-aminobutyric acid (GABA) release in the rat olfactory bulb , 2001 .

[6]  T. Powell,et al.  The synaptology of the granule cells of the olfactory bulb. , 1970, Journal of cell science.

[7]  C. Greer,et al.  Local information processing in dendritic trees: subsets of spines in granule cells of the mammalian olfactory bulb , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  C. Lingle,et al.  Pharmacological properties of T-type Ca2+ current in adult rat sensory neurons: effects of anticonvulsant and anesthetic agents. , 1998, Journal of neurophysiology.

[9]  Gordon M. Shepherd,et al.  The Olfactory Bulb , 1988 .

[10]  M. Moulins,et al.  Tetrodotoxin‐sensitive dendritic spiking and control of axonal firing in a lobster mechanoreceptor neurone. , 1993, The Journal of physiology.

[11]  G. Shepherd,et al.  Impulse activity in presynaptic dendrites: analysis of mitral cells in the isolated turtle olfactory bulb , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  D. Wellis,et al.  Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. , 1990, Journal of neurophysiology.

[13]  G. Westbrook,et al.  Regulation of synaptic timing in the olfactory bulb by an A-type potassium current , 1999, Nature Neuroscience.

[14]  K. Mori,et al.  An intracellular study of dendrodendritic inhibitory synapses on mitral cells in the rabbit olfactory bulb. , 1978, The Journal of physiology.

[15]  J. Midtgaard,et al.  Regulation of granule cell excitability by a low-threshold calcium spike in turtle olfactory bulb. , 2003, Journal of neurophysiology.

[16]  G. Stuart,et al.  Dependence of EPSP Efficacy on Synapse Location in Neocortical Pyramidal Neurons , 2002, Science.

[17]  Nace L. Golding,et al.  Dendritic Sodium Spikes Are Variable Triggers of Axonal Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1998, Neuron.

[18]  P. Lory,et al.  Specific contribution of human T-type calcium channel isotypes (alpha(1G), alpha(1H) and alpha(1I)) to neuronal excitability. , 2002, The Journal of physiology.

[19]  J. Magee,et al.  Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons , 2000, Nature Neuroscience.

[20]  Gongyu Y. Shen,et al.  Computational analysis of action potential initiation in mitral cell soma and dendrites based on dual patch recordings. , 1999, Journal of neurophysiology.

[21]  M. Vargas-Caballero,et al.  A slow fraction of Mg2+ unblock of NMDA receptors limits their contribution to spike generation in cortical pyramidal neurons. , 2003, Journal of neurophysiology.

[22]  G. Shepherd,et al.  Analysis of Relations between NMDA Receptors and GABA Release at Olfactory Bulb Reciprocal Synapses , 2000, Neuron.

[23]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[24]  G M Shepherd,et al.  Electrophysiological analysis of mitral cells in the isolated turtle olfactory bulb. , 1981, The Journal of physiology.

[25]  R. Meech,et al.  Ionic currents in giant motor axons of the jellyfish, Aglantha digitale. , 1993, Journal of neurophysiology.

[26]  Jung-Ha Lee,et al.  Distinct kinetics of cloned T‐type Ca2 +  channels lead to differential Ca2 +  entry and frequency‐dependence during mock action potentials , 1999, The European journal of neuroscience.

[27]  S. Nakanishi,et al.  Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Lubke,et al.  Olfactory bulb granule cell aggregates: morphological evidence for interperikaryal electrotonic coupling via gap junctions , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  K. Svoboda,et al.  Mechanisms of Lateral Inhibition in the Olfactory Bulb: Efficiency and Modulation of Spike-Evoked Calcium Influx into Granule Cells , 2003, The Journal of Neuroscience.

[30]  T. Kosaka,et al.  Neuronal gap junctions in the rat main olfactory bulb, with special reference to intraglomerular gap junctions , 2003, Neuroscience Research.

[31]  Alain Destexhe,et al.  Modelling corticothalamic feedback and the gating of the thalamus by the cerebral cortex , 2000, Journal of Physiology-Paris.

[32]  Gordon M Shepherd,et al.  Multiple modes of action potential initiation and propagation in mitral cell primary dendrite. , 2002, Journal of neurophysiology.

[33]  P. Lory,et al.  Specific contribution of human T‐type calcium channel isotypes (α1G, α1H and α1I) to neuronal excitability , 2002 .

[34]  J S Kauer,et al.  GABAergic and glutamatergic synaptic input to identified granule cells in salamander olfactory bulb. , 1994, The Journal of physiology.

[35]  B. Burrell,et al.  Action potential reflection and failure at axon branch points cause stepwise changes in EPSPs in a neuron essential for learning. , 2000, Journal of neurophysiology.

[36]  R. Traub,et al.  Axo-Axonal Coupling A Novel Mechanism for Ultrafast Neuronal Communication , 2001, Neuron.

[37]  K. Delaney,et al.  Contribution of a Calcium‐Activated Non‐Specific Conductance to NMDA Receptor‐Mediated Synaptic Potentials in Granule Cells of the Frog Olfactory Bulb , 2002, The Journal of physiology.

[38]  Minmin Luo,et al.  Response Correlation Maps of Neurons in the Mammalian Olfactory Bulb , 2001, Neuron.

[39]  K Kishi,et al.  Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory bulb , 1983, The Journal of comparative neurology.

[40]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[41]  N. Klugbauer,et al.  Low voltage activated calcium channels: from genes to function. , 2000, General physiology and biophysics.

[42]  G M Shepherd,et al.  Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells. , 1997, Science.

[43]  P. Jonas,et al.  Kinetics of Mg2+ unblock of NMDA receptors: implications for spike‐timing dependent synaptic plasticity , 2004, The Journal of physiology.

[44]  T. Powell,et al.  The morphology of the granule cells of the olfactory bulb. , 1970, Journal of cell science.

[45]  J. Midtgaard Spatial synaptic integration in Purkinje cell dendrites , 1995, Journal of Physiology-Paris.

[46]  V. Crunelli,et al.  Properties and origin of spikelets in thalamocortical neurones in vitro , 2002, Neuroscience.

[47]  G M Shepherd,et al.  Analysis of a long‐duration inhibitory potential in mitral cells in the isolated turtle olfactory bulb. , 1981, The Journal of physiology.