Nitric Oxide, Odour Processing and Plasticity

Abstract

We are pursuing a cellular and computational analysis of odour recognition and odour learning in the terrestrial gastropod Limax maximus. Two design features in the olfactory system of Limax may be common elements of generalist olfactory systems. They are 1) coherent oscillations in the second-order circuitry processing the sensory input and 2) involvement of the intercellular messenger nitric oxide in both sensory responses and the circuit dynamics of the oscillating olfactory network. The procerebral (PC) lobe of the Limax cerebral ganglion contains of order 105 local interneurons and receives direct input from olfactory receptors. Field potential recordings in the PC show a 0.7 Hz oscillation which is altered by odour input. Optical recordings of voltage changes in local regions of the PC show waves of depolarization originating at the distal pole and propagating to its base. Weak odour stimulation transiently switches PC activity from wave propagating mode to a spatially uniform activity mode. Both attractive and repellent odours cause this mode switch in PC activity. The field potential oscillation in the PC lobe depends on intercellular communication via nitric oxide (NO), based on effects of agents which eliminate or increase NO levels in the PC. Application of oxyhemeprotein or NO synthase inhibitor stops the field potential oscillation, reversibly. Application of exogenous NO using several NO donors increases the oscillation frequency. Liberation of caged NO by near UV flashes applied to preparations treated with dipotassium nitrosylpentachlororuthenate (NPR) also speeds the field potential oscillation. Nystatin perforated-patch recordings from the bursting cells in the PC presumed to drive the oscillation show that NO increases the burst frequency in these cells. These design features of the PC lobe odour processing circuitry may relate to the highly developed odour sensitivity and odour learning ability of Limax.