×

Firing properties of a stochastic PDE model of a rat sensory cortex layer 2/3 pyramidal cell. (English) Zbl 1038.92008

Summary: We have developed a nonlinear stochastic PDE (partial differential equation) model of a rat layer 2/3 somatosensory pyramidal neuron which approximates several of the dynamical properties of these cells. The model distinguishes telodendrites, a myelinated axon, initial segment, hillock, soma and a simplified dendritic tree. Distributions and properties of excitatory and inhibitory synapses were included, in accordance with recent anatomical and physiological findings. Using simulation methods, we aim to show that the spatial separation between regions of spatially distributed randomly activated excitatory and inhibitory synaptic inputs may be an important parameter which can influence neuronal firing properties.
Due to the complexity of the problem, with respect to configurations of spatially and temporally activated excitatory and inhibitory synaptic inputs, we consider two simple configurations in which the spatial region of activated excitatory and inhibitory synaptic inputs overlap and when they are far from each. In the first, denoted configuration \(\mathbf A\), activated excitatory and inhibitory synapses were located close to the soma. In the second, denoted configuration \(\mathbf B\), active inhibitory synapses were close to the soma, while active excitatory synapses were located on distal regions of the dendrite. For the first configuration, we find that increases in the mean rate of inhibition result in an increase in the width of the firing rate tuning curves, and that for particular mean input frequencies of excitation, increasing the mean input rate of inhibition does not always imply that the neuron fires at a slower rate.
Furthermore, we observed for mean input frequencies of excitation between 15 and 60 (Hz), that increasing the mean rate of inhibition resulted in the linearization of the firing rate over this interval. For configuration \(\mathbf B\), no increase in width nor a linearization effect via inhibition was observed. These differences indicate that the distance between regions of active excitatory and inhibitory synapses may be an important factor to consider in determining how the interaction between excitation and inhibition contributes to neuronal firing.

MSC:

92C20 Neural biology
60H15 Stochastic partial differential equations (aspects of stochastic analysis)
Full Text: DOI

References:

[1] Lu, X.; Lewis, E. R., Studies with spike initiators: linearization by noise allows continuous signal modulation in neural networks, IEEE Trans Biomed. Eng., 36, 36 (1989)
[2] Brunel, N.; Latham, P. E., Firing rate of the noisy quadratic integrate-and-fire neuron, Neural Computat., 15, 2281 (2003) · Zbl 1085.68617
[3] Stein, R. B., A theoretical analysis of neuronal variability, Biophys. J., 5, 173 (1965)
[4] Rall, W., Theoretical significance of dendritic trees for neuronal input-output relations, (Riess, R. F., Neural Theory and Modeling (1964), Stanford University), 73, (Chapter 4)
[5] Dodge, F. A.; Cooley, J. W., Action potential of the motoneuron, IBM J. Res. Devel., 17, 219 (1973)
[6] Mainen, Z. F.; Joerges, J.; Huguenard, J. R.; Sejnowski, T. J., A model of spike initiation in neocortical pyramidal cells, Neuron, 15, 1427 (1995)
[7] Holt, G. R.; Koch, C., Shunting inhibition does not have a divisive effect on firing rates, Neural Computat., 9, 1001 (1997)
[8] Tuckwell, H. C.; Wan, F. Y.M; Rospars, J.-P, A spatial stochastic neuronal model with Ornstein-Uhlenbeck input current, Biol. Cybernet., 86, 137 (2002) · Zbl 1066.92014
[9] Tuckwell, H. C.; Walsh, J. B., Random currents through nerve membranes i. uniform Poisson or white noise current in one dimensional cables, Biol. Cybernet., 49, 99 (1983) · Zbl 0536.92019
[10] Tuckwell, H. C.; Wan, F. Y.M, The response of a nerve cylinder to spatially distributed white noise inputs, J. Theor. Biol., 87, 275 (1980)
[11] Tuckwell, H. C.; Wan, F. Y.M; Wong, Y. S., The interspike interval of a cable model neuron with white noise input, Biol. Cybernet., 49, 155 (1984) · Zbl 0553.92010
[12] Destexhe, A., Simplified models of neocortical pyramidal cells preserving somatodendritic voltage attenuation, Neurocomputing, 38-40, 167 (2001)
[13] Feldmeyer, D.; Lubke, J.; Silver, R. A.; Sakmann, B., Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column, J. Physiol., 538, 3, 803 (2002)
[14] Markram, H.; Lubke, J.; Frotscher, M.; Roth, A.; Sakmann, B., Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex, J. Physiol., 500, 2, 409 (1997)
[15] Thomson, A. M.; Deuchars, J.; West, D. C., Relationships between morphology and physiology of pyramid-pyramid single axon connections in rat neocortex in vitro, J. Physiol., 478, 3, 423 (1994)
[16] Thomson, A. M.; Destexhe, A., Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices, Neuroscience, 92, 1193 (1999)
[17] Thomson, A. M.; West, D. C.; Wang, Y.; Bannister, A. P., Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro, Cereb. Cort., 12, 936 (2002)
[18] Larkman, A. L., Dendritic morphology of pyramidal neurones of the visual cortex of the rat: iii. spine distributions, J. Comparat. Neurol., 306, 332 (1991)
[19] DeFelipe, J.; Farinas, I., The pyramidal neuron of the cerebral cortex: morphology and chemical characteristics of the synaptic input, Prog. Neurobiol., 39, 563 (1992)
[20] Paré, D.; Shink, E.; Gaudreau, H.; Destexhe, A.; Lang, E. J., Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo, J. Neurophysiol., 79, 1450 (1998)
[21] Trevelyan, A. J.; Jack, J. J.B, Detailed passive cable models of layer 2/3 pyramidal cells in rat visual cortex at different temperatures, J. Physiol., 539, 2, 623 (2002)
[22] Huguenard, J. R.; Hamill, O. P.; Prince, D. A., Developmental changes in \(Na^+\) conductances in rat neocortical neurons: appearance of a slowly inactivating component, J. Neurophysiol., 59, 778 (1988)
[23] Hamill, O. P.; Huguenard, J. R.; Prince, D. A., Patch-clamp studies of voltage-gated currents in identified neurons in the rat cerebral cortex, Cereb. Cort., 1, 48 (1991)
[24] Mascagni, M. V.; Sherman, A. S., Methods in Neuronal modeling: From Ions to Networks (1999), MIT
[25] Tuckwell, H. C., Introduction to theoretical neurobiology, (Nonlinear and Stochastic Theories, vol. 2 (1988), Cambridge University: Cambridge University New York) · Zbl 0647.92009
[26] Paré, D.; Lang, E. J.; Destexhe, A., Inhibitory control of samotdendritic interactions underlying action potentials in neocortical pyramidal neurons in vivo: an intracellular and computational study, Neuroscience, 84, 377 (1998)
[27] Feerick, S.; Feng, J.; Brown, D., Inhibitory inputs increase a neurons’s firing rate, Neurocomputing, 38-40, 197 (2001)
[28] Monier, C.; Chavane, F.; Baudot, P.; Graham, L. J.; Frégnac, Y., Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning, Neuron, 37, 663 (2003)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.