Dendritic Integration in Olfactory Sensory Neurons: A Steady-State Analysis of How the Neuron Structure and Neuron Environment Influence the Coding of Odor Intensity

Response properties of the receptor potential at steady state were analyzed in a biophysical model of an olfactory sensory neuron embedded in a multicell environment. The neuron structure was described as a set of several identical dendrites (or cilia) bearing the transduction mechanisms, joined to a nonsensory part—dendritic knob, soma, and axon. The different ionic compositions of the media surrounding the neuron sensory and nonsensory parts and the extraneuronal voltage sources, which both result from the presence of auxiliary cells, were also taken into account. Analytical solutions were found to describe how the receptor potential at the nonsensory part responds to a uniform change in the odorant-dependent conductance resulting from odorant stimulation of the sensory dendrites. We investigated the influence of various geometrical and electrical parameters on the receptor-potential response in the classical model neuron within a homogeneous environment and in the model neuron surrounded with auxiliary cells. First, it was found that the maximum amplitude of the receptor potential is independent of the neuron structure in the absence of auxiliary cells but not in their presence. In the latter case, the amplitude decreases with the length and number of sensory dendrites and with the input resistance of the nonsensory part. Second, the sensitivity (as measured by the increase in membrane conductance at half-maximum response) of the neuron model in the absence of auxiliary cells is higher, but its dynamic range is narrower than in their presence. The dynamic range is wide and the sensitivity low when the input resistance of the nonsensory part is small and the sensory dendrite is unbranched. Both sensitivity and dynamic range are higher for a longer dendrite. These results help understand the morphology of insect olfactory sensilla and can be generalized to other neuron types.

[1]  W. Gnatzy,et al.  Pheromone receptors in Bombyx mori and Antheraea pernyi , 2004, Cell and Tissue Research.

[2]  J. Rospars,et al.  Intensity Coding in an Olfactory Sensory Neuron , 1997 .

[3]  A. Grinnell,et al.  Introduction to Nervous Systems , 1978 .

[4]  J. Rospars,et al.  Coding of stimulus intensity in an olfactory receptor neuron: role of neuron spatial extent and passive dendritic backpropagation of action potentials. , 1996, Bulletin of mathematical biology.

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

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

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

[8]  W. Rall.  Membrane potential transients and membrane time constant of motoneurons. , 1960, Experimental neurology.

[9]  Alexander Borst,et al.  Amplification of high-frequency synaptic inputs by active dendritic membrane processes , 1996, Nature.

[10]  J. Thorson,et al.  Insect Olfactory Sensilla: Structural, Chemical and Electrical Aspects of the Functional Organisation , 1980 .

[11]  G M Shepherd,et al.  Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. , 1991, Journal of neurophysiology.

[12]  Konrad Colbow,et al.  R. H. Wright Lectures on Insect Olfaction , 1987 .

[13]  G. Ringham.  Origin of nerve impulse in slowly adapting stretch receptor of crayfish. , 1971, Journal of neurophysiology.

[14]  K. Kaissling.  Sensory Transduction in Insect Olfactory Receptors , 1974 .

[15]  J. Bower,et al.  Simulated responses of cerebellar Purkinje cells are independent of the dendritic location of granule cell synaptic inputs. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[16]  N T Carnevale,et al.  Electrophysiological characterization of remote chemical synapses. , 1982, Journal of neurophysiology.

[17]  A simple analytical method for determining the steady-state potential in models of geometrically complex neurons , 1998, Journal of Neuroscience Methods.

[18]  W. Rall.  Cable theory for dendritic neurons , 1989 .

[19]  A. Holley,et al.  [Transduction and coding of olfactory information]. , 1977, Journal de physiologie.

[20]  U. Thurm,et al.  EPITHELIAL PHYSIOLOGY OF INSECT SENSILLA , 1980 .

[21]  K. Ernst.  Die Feinstruktur von Riechsensillen auf der Antenne des Aaskäfers Necrophorus (Coleoptera) , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[22]  T. Poggio,et al.  Retinal ganglion cells: a functional interpretation of dendritic morphology. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  T. Getchell.  Functional properties of vertebrate olfactory receptor neurons. , 1986, Physiological reviews.

[24]  J. D. Kramer.  The electrical circuitry of an olfactory sensillum in Antheraea polyphemus , 1985 .

[25]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. , 1980, The Journal of physiology.

[26]  J. Rospars,et al.  Coding of odour intensity in a sensory neuron. , 1997, Bio Systems.

[27]  K. Kaissling,et al.  Passive electrical properties of insect sensilla may produce the biphasic shape of spikes , 1984 .

[28]  H. Breer,et al.  Peripheral processes in insect olfaction. , 1992, Annual review of physiology.

[29]  P Lánský,et al.  Coding of odor intensity. , 1993, Bio Systems.

[30]  K. Kaissling,et al.  Effects of temperature on silkmoth olfactory responses to pheromone can be simulated by modulation of resting cell membrane resistances , 1996, Journal of Comparative Physiology A.

[31]  U. Thurm.  Basics of the Generation of Receptor Potentials in Epidermal Mechanoreceptors of Insects , 1974 .

[32]  F. Zufall,et al.  Dual activation of a sex pheromone-dependent ion channel from insect olfactory dendrites by protein kinase C activators and cyclic GMP. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[33]  D. Perkel,et al.  Quantitative methods for predicting neuronal behavior , 1981, Neuroscience.

[34]  W. Grampp,et al.  The impulse activity in different parts of the slowly adapting stretch receptor neuron of the lobster. , 1966, Acta physiologica Scandinavica. Supplementum.

[35]  T. Keil,et al.  Reconstruction and morphometry of silkmoth olfactory hairs: A comparative study of sensilla trichodea on the antennae of male Antheraea polyphemus and Antheraea pernyi (Insecta, Lepidoptera) , 1984, Zoomorphology.

[36]  W. Gnatzy,et al.  Pheromone receptors in Bombyx mori and Antheraea pernyi , 2004, Cell and Tissue Research.

[37]  K. Kaissling,et al.  Kinetics of olfactory receptor potentials , 1969 .

[38]  K. Kaissling,et al.  Chemo-electrical transduction in insect olfactory receptors. , 1986, Annual review of neuroscience.

[39]  Henry C. Tuckwell,et al.  Coding of odor intensity in a steady-state deterministic model of an olfactory receptor neuron , 1996, Journal of Computational Neuroscience.

[40]  Henry C. Tuckwell,et al.  Introduction to theoretical neurobiology , 1988 .