Elsevier

Neurocomputing

Volumes 52–54, June 2003, Pages 45-52
Neurocomputing

Structural and biophysical mechanisms underlying dynamic sensitivity of primary sensory interneurons in the cricket cercal sensory system

https://doi.org/10.1016/S0925-2312(02)00786-5Get rights and content

Abstract

We constructed probabilistic models of afferent inputs and compartmental models of interneurons in the cricket cercal system to examine the effects of dendritic morphology, distribution of synaptic inputs, and membrane properties on interneuron directional tuning properties. The mean directional tuning of afferent inputs to an interneuron was an excellent predictor of its directional tuning. Location of the synapses on the interneurons’ dendrites was not essential to determining tuning characteristics, but had a substantial effect on sensitivity. Thus, we conclude that both sampling of the afferent population, and anatomical distribution of synaptic inputs are important determinants of an interneuron's directional response.

Introduction

The response properties of a neuron to complex patterns of synaptic inputs are controlled by a combination of factors including: (1) the electroanatomy of the cell, (2) its biophysical properties and (3) the distribution and activation pattern of synaptic inputs. We used electrophysiological experiments, statistical and compartmental modeling techniques to (1) calculate detailed, quantitative predictions of a variety of ensemble afferent activity patterns elicited by air current stimuli, (2) define simulated synaptic input patterns onto the dendrites of compartmental interneuron models, and (3) examine the roles of dendritic morphology, distribution of synaptic inputs and membrane properties on the directional tuning properties of the neurons.

Primary sensory interneurons in the cercal system are sensitive to the direction and dynamics of air currents [6], [11], [18]. The interneurons receive excitatory input from an ensemble of sensory receptor afferents which form a neural map of air current direction in the central nervous system [8]. Interneurons extract and encode information about stimulus direction based on the shape and position of their dendrites within the afferent map [9]. Three independent factors could contribute to the directional sensitivity of each interneuron IN: (a) the position of its dendrites within the afferent map, (b) its selective connectivity with subclasses of afferents having specific directional sensitivities, and (c) the membrane properties of the cell.

Section snippets

Methods

Anatomical reconstructions and physiological data were used to create biophysically based compartmental models of three identified sensory interneurons. Values for Ri and Cm were set to experimentally established values. Rm was initially assumed to be uniform throughout the cell, and was set to yield the measured steady-state input resistance and complex input impedance recorded in real neurons [17]. Next, parameter domains for voltage-dependent conductances and synaptic inputs were determined

Results

The directional tuning of model interneurons in response to air currents from different directions was calculated using the methods described above. In all cases, the directional tuning curves measured from the model cells were very similar to those recorded previously in physiological experiments on these same identified cells [6], [11]. Fig. 1 shows a comparison of a directional tuning curve recorded from identified IN 10-3 and a simulation of the same experiment. The histogram of the number

Discussion

The results of simulations reported here suggest that the directional tuning properties of primary sensory INs in the cricket cercal system are determined largely by the anatomical structure of the INs, the directional tuning properties of those afferents that provide excitatory input and the spatial distribution of those inputs to different dendritic branches. Interneurons with different dendritic structures receive different sets of excitatory inputs and thus are tuned to specific air current

Acknowledgements

This work was supported by National Science Foundation grants IBN 0090966 to GAJ and SMC and MRI 9871191 to JPM. Special thanks to Zane Aldworth for providing physiology data.

References (18)

  • J.B. Bacon et al.

    A silver intensification method for cobalt filled neurons in whole mount preparations

    Brain Res.

    (1977)
  • B.J. Claiborne et al.

    Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus

    J. Comput. Neurol.

    (1990)
  • G.I. Cummins, Compartmental models and genetic algorithms provide insight into structure-function relationships in the...
  • G.W. Davis et al.

    A role for postsynaptic neurons in determining presynaptic release properties in the cricket CNSevidence for retrograde control of facilitation

    J. Neurosci.

    (1993)
  • M. Horner et al.

    Voltage-activated currents in identified giant INs isolated from adult crickets gryllus bimaculatus

    J. Exp. Biol.

    (1998)
  • G.A. Jacobs et al.

    Cellular mechanisms underlying directional sensitivity of an identified sensory IN

    J. Neurosci.

    (1986)
  • G.A. Jacobs et al.

    Predicting emergent properties of neuronal ensembles using a database of individual neurons

  • G.A. Jacobs et al.

    Functional organization of a neural map in the cricket cercal sensory system

    J. Neurosci.

    (1996)
  • G.A. Jacobs et al.

    Extraction of sensory parameters from a neural map by primary sensory INs

    J. Neurosci.

    (2000)
There are more references available in the full text version of this article.

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