Electrical consequences of spine dimensions in a model of a cortical spiny stellate cell completely reconstructed from serial thin sections

We built a passive compartmental model of a cortical spiny stellate cell from the barrel cortex of the mouse that had been reconstructed in its entirety from electron microscopic analysis of serial thin sections (White and Rock, 1980). Morphological data included dimensions of soma and all five dendrites, neck lengths and head diameters of all 380 spines (a uniform neck diameter of 0.1 μm was assumed), locations of all symmetrical and asymmetrical (axo-spinous) synapses, and locations of all 43 thalamocortical (TC) synapses (as identified from the consequences of a prior thalamic lesion). In the model, unitary excitatory synaptic inputs had a peak conductance change of 0.5 nS at 0.2 msec; conclusions were robust over a wide range of assumed passive-membrane parameters. When recorded at the soma, all unitary EPSPs, which were initiated at the spine heads, were relatively iso-efficient; each produced about 1 mV somatic depolarization regardless of spine location or geometry. However, in the spine heads there was a twentyfold variation in EPSP amplitudes, largely reflecting the variation in spine neck lengths. Synchronous activation of the TC synapses produced a somatic depolarization probably sufficient to fire the neuron; doubling or halving the TC spine neck diameters had only minimal effect on the amplitude of the composite TC-EPSP. As have others, we also conclude that from a somato-centric viewpoint, changes in spine geometry would have relatively little direct influence on amplitudes of EPSPs recorded at the soma, especially for a distributed, synchronously activated input such as the TC pathway. However, consideration of the detailed morphology of an entire neuron indicates that, from a dendro-centric point of view, changes in spine dimension can have a very significant electrical impact on local processing near the sites of input.

[1]  H. Markram,et al.  Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M Hines,et al.  A program for simulation of nerve equations with branching geometries. , 1989, International journal of bio-medical computing.

[3]  Y Yarom,et al.  Physiology, morphology and detailed passive models of guinea‐pig cerebellar Purkinje cells. , 1994, The Journal of physiology.

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

[5]  William R. Holmes,et al.  Is the function of dendritic spines to concentrate calcium? , 1990, Brain Research.

[6]  C. Koch,et al.  The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  E. White,et al.  Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections , 1980, Journal of neurocytology.

[8]  J. C. Anderson,et al.  Polyneuronal innervation of spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[9]  B. Sakmann,et al.  Active propagation of somatic action potentials into neocortical pyramidal cell dendrites , 1994, Nature.

[10]  J I Gold,et al.  A model of dendritic spine Ca2+ concentration exploring possible bases for a sliding synaptic modification threshold. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  B. Sakmann,et al.  Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. , 1992, The Journal of physiology.

[12]  M Kawato,et al.  Electrical properties of dendritic spines with bulbous end terminals. , 1984, Biophysical journal.

[13]  F. Crick Do dendritic spines twitch? , 1982, Trends in Neurosciences.

[14]  A. Friedman,et al.  Stepwise repolarization from Ca2+ plateaus in neocortical pyramidal cells: evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  J Rinzel,et al.  Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. , 1973, Biophysical journal.

[16]  W. Rall Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. , 1967, Journal of neurophysiology.

[17]  E. Welker,et al.  The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  R. Llinás,et al.  Localization of P-type calcium channels in the central nervous system. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[19]  KM Harris,et al.  Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. Deuchars,et al.  Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation , 1993, Neuroscience.

[21]  B. Connors,et al.  Regenerative activity in apical dendrites of pyramidal cells in neocortex. , 1993, Cerebral cortex.

[22]  J. P. Miller,et al.  Modeling the electrical behavior of anatomically complex neurons using a network analysis program: Passive membrane , 1985, Biological Cybernetics.

[23]  N. V. Swindale,et al.  Dendritic spines only connect , 1981, Trends in Neurosciences.

[24]  B. Connors,et al.  Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[26]  C. Wilson,et al.  Passive cable properties of dendritic spines and spiny neurons , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  I Segev,et al.  Electrotonic architecture of type-identified alpha-motoneurons in the cat spinal cord. , 1988, Journal of neurophysiology.

[28]  T. Poggio,et al.  A theoretical analysis of electrical properties of spines , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[29]  Charles J. Wilson Dendritic morphology, inward rectification, and the functional properties of neostriatal neurons , 1992 .

[30]  John Rinzel,et al.  Neuronal plasticity (learning) , 1982 .

[31]  Idan Segev,et al.  Compartmental models of complex neurons , 1989 .

[32]  G. Benshalom,et al.  Structural alterations of dendritic spines induced by neural degeneration of their presynaptic afferents , 1989, Synapse.

[33]  J Rinzel,et al.  Transient response in a dendritic neuron model for current injected at one branch. , 1974, Biophysical journal.

[34]  Clay Armstrong,et al.  Synaptically triggered action potentials in dendrites , 1993, Neuron.

[35]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  E. White Cortical Circuits: Synaptic Organization of the Cerebral Cortex , 1989 .

[37]  D A Turner,et al.  Segmental cable evaluation of somatic transients in hippocampal neurons (CA1, CA3, and dentate). , 1984, Biophysical journal.

[38]  W Rall,et al.  Computational study of an excitable dendritic spine. , 1988, Journal of neurophysiology.

[39]  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.

[40]  Y Yarom,et al.  Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig. , 1990, Journal of neurophysiology.