Skip to main content
Log in

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

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agmon A and Connors BW (1992) Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex.J. Neurosci. 12:319–329.

    Google Scholar 

  • Agmon A and O'Dowd DK (1992) NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition.J. Neurophysiol. 68:345–349.

    Google Scholar 

  • Ahmed B, Anderson JC, Douglas RJ, Martin KAC, and Nelson JC (1994) Polyneuronal innervation of spiny stellate neurons in cat visual cortex.J. Comp. Neurology 341:39–49.

    Google Scholar 

  • Amitai Y, Friedman A, Connors BW, and Gutnick MJ (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex.Cerebral Cortex 3:26–38.

    Google Scholar 

  • Armstrong-James M, Welker E, and Callahan CA (1993) The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex.J. Neurosci. 13:2149–2160.

    Google Scholar 

  • Benshalom G (1989) Structural alterations of dendritic spines induced by neural degeneration of their presynaptic afferents.Synapse 4:210–222.

    Google Scholar 

  • Brown TH, Chang VC, Ganong AH, Keenan CL, and Kelso SR (1988) Biophysical properties of dendrites and spines that may control the induction and expression of long-term synaptic potentiation. In: PW Landfield and SA Deadwyler, eds. Long-Term Potentiation: From Biophysics to Behavior. Alan R. Liss New York, NY. pp. 201–264.

    Google Scholar 

  • Crick F (1982) Do dendritic spines twitch?Trends in Neurosci. 5:44–46.

    Google Scholar 

  • Fleshman JW, Segev I, and Burke RE (1988) Electrotonic architecture of type-identified α-motoneurons in the cat spinal cord.J. Neurophysiol. 60:60–85.

    Google Scholar 

  • Gold JI and Bear MF (1994) A model of dendritic spine Ca2+ concentration exploring possible basis for a sliding synaptic modification rule.Proc. Nat. Acad. Sci. 91:3941–3946.

    Google Scholar 

  • Harris KM and Stevens JK (1989) Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics.J. Neurosci. 9:2982–2997.

    Google Scholar 

  • Hillman D, Chen S, Aung TT, Cherksey B, Sugimori M, and Llinas R (1991) Localization of P-type calcium channels in the central nervous system.Proc. Nat. Acad. Sci. 88:7076–7080.

    Google Scholar 

  • Hines M (1989) A program for simulation of nerve equations with branching geometries.Int. J. Biomed., Comput. 24:55–68.

    Google Scholar 

  • Holmes WR (1990) Is the function of dendritic spines to concentrate calcium?Brain Research 519:338–342.

    Google Scholar 

  • Kawato M and Tsukahara N (1984) Electrical properties of dendritic spines with bulbous end terminals.Biophys. J. 46:155–166.

    Google Scholar 

  • Kim HG and Connors BW (1993) Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology.J. Neurosci 13:5301–5311.

    Google Scholar 

  • Koch C and Poggio T (1983) A theoretical analysis of electrical properties of spines.Proc. R. Soc. Lond. 218:455–477.

    Google Scholar 

  • Koch C and Zador A (1993) The function of dendritic spines: Devices subserving biochemical rather than electrical compartmentalization.J. Neurosci. 13 (2):413–422.

    Google Scholar 

  • Markram H and Sakmann B (1994) Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels.Proc. Nat. Acad. Sci. 91:5207–5211.

    Google Scholar 

  • Nitzan R, Segev I, and Yarom, Y (1990) Voltage behaviour along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig.J. Neurophys. 63:333–346.

    Google Scholar 

  • Rall W (1964) Theoretical significance of dendritic trees for neuronal input-output relations. In: R Reiss, ed. Neural Theory and Modeling. Stanford U. Press, Stanford, CA. pp. 73–97.

    Google Scholar 

  • Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input.J. Neurophysiol. 30:1138–1168.

    Google Scholar 

  • Rall, W (1974) Dendritic spines, synaptic potency and neuronal plasticity. In: CD Woody, KA Brown, TJ Crow, and JD Knispel, eds. Mechanisms Subserving Changes in Neuronal Activity. Brain Information Service Research Report Vol. 3, Los Angeles, CA. pp. 13–21.

  • Rall W and Rinzel J (1973) Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model.Biophys. J. 13:648–688.

    Google Scholar 

  • Rapp M, Segev I, and Yarom Y (1994) Physiology, morphology and detailed passive models of cerebellar Purkinje cells.J. Physiol. (London) 474:101–119.

    Google Scholar 

  • Regehr W, Kehoe JS, Ascher P, and Armstrong C (1993) Synaptically triggered action potentials in dendrites.Neuron 11:145–151.

    Google Scholar 

  • Reuveni I, Friedman A, Amitai Y, and Gutnick MJ (1993) Stepwise repolarization from Ca2+ plateaus in neocortical pyramidal cells: Evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites.J. Neurosci. 13:4609–4621.

    Google Scholar 

  • Rinzel J (1982) Neuronal plasticity (learning),Lect. Math. Life Sci. 15:7–25.

    Google Scholar 

  • Rinzel J and Rall W (1974) Transient response in a dendritic neuron model for current injected at one branch.Biophys. J. 14:759–790.

    Google Scholar 

  • Segev I, Fleshman JW, and Burke RE (1989) Compartmental models of complex neurons. In: C Koch and I Segev, eds. Methods in Neuronal Modeling: From Synapses to Networks. MIT Press, Boston, MA. pp. 63–96.

    Google Scholar 

  • Segev I, Fleshman JW, Miller JP, and Bunow B (1985) Modeling the electrical behavior of anatomically complex neurons using a network analysis program: passive membrane.Biol. Cybernetics 53:27–40.

    Google Scholar 

  • Segev I and Rall W (1988) Computational study of an excitable dendritic spine.J. Neurophysiol. 60:499–523.

    Google Scholar 

  • Segev I, White EL, and Gutnick MJ (1989) Detailed compartmental model of an em reconstructed spiny stellate cell in the mouse neocortex.Society for Neuroscience Abstracts 15:256.

    Google Scholar 

  • Stern P, Edwards FA, and Sakmann B (1992) Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex.J. Physiol. 449:247–278.

    Google Scholar 

  • Stratford AU, Mason A, Larkman AU, Major G, and Jack JJB (1989). The modeling of pyramidal neurons in the visual cortex. In: R Durbin, C Miall, and G Mitchison, eds. Addison Wesley, Worhengham, England, pp. 296–321.

    Google Scholar 

  • Stuart GJ and Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites.Nature 367:69–72.

    Google Scholar 

  • Swindale NV (1981) Dendritic spines only connect.Trends in Neurosci. 4:240–241.

    Google Scholar 

  • Thomson AM and West DC (1993a) Fluctuations in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recording in rat neocortex.Neurosci. 54:329–346.

    Google Scholar 

  • Thomson AM, Deuchars J, and West DC (1993b) Single axon excitatory post synaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation.Neurosci. 54:347–360.

    Google Scholar 

  • Turner DA (1984) Segmental cable evaluation of somatic transients in hippocampal neurons (CA1, CA3, and dentate).Biophys. J. 46:73–84.

    Google Scholar 

  • White EL (1989) Cortical Circuits. Synaptic Organization of the Cerebral Cortex; Structure, Function and Theory. Birkhauser Press, Boston.

    Google Scholar 

  • White EL and Rock MP (1980) Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections.J. Neurocytol. 9:615–636.

    Google Scholar 

  • Wilson CJ (1984) Passive cable properties of dendritic spines and spiny neurons.J. Neurosci. 4:281–297.

    Google Scholar 

  • Wilson CJ (1992) Dendritic morphology, inward rectification, and functional properties of neostriatal neurons. In: T McKenna, J Davis, and SF Zanetzer, eds. Single Neuron Computation. Academic Press, San Diego, CA. pp. 141–171.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Segev, I., Friedman, A., White, E.L. et al. Electrical consequences of spine dimensions in a model of a cortical spiny stellate cell completely reconstructed from serial thin sections. J Comput Neurosci 2, 117–130 (1995). https://doi.org/10.1007/BF00961883

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00961883

Keywords

Navigation