Olfactory systems combine an extraordinary molecular sensitivity with
robust synaptic plasticity. Central neuronal circuits that perform pat
tern recognition in olfaction typically discriminate between hundreds
of molecular species and form associations between odor onsets and beh
avioral contingencies that can last a lifetime. Two design features in
the olfactory system of the terrestrial mollusk Limax maximus may be
common elements of olfactory systems that display the twin features of
broad molecular sensitivity and rapid odor learning: spatially cohere
nt oscillations in the second-order circuitry that receives sensory in
put; and involvement of the interneuronal messengers nitric oxide (NO)
and carbon monoxide (GO) in sensory responses and circuit dynamics of
the oscillating olfactory network. The principal odor processing cent
er in Limax, the procerebrum (PC) of the cerebral ganglion, contains o
n the order of 10(5) local interneurons and receives both direct and p
rocessed input from olfactory receptors. Field potential recordings in
the PC show an oscillation at approximately 0.7 Hz that is altered by
odor input, Optical recordings of voltage changes in local regions of
the PC show waves of depolarization that originate at the distal pole
and propagate to the base of the PC, Weak odor stimulation transientl
y switches PC activity from a propagating mode to a spatially uniform
mode, The field potential oscillation in the PC lobe depends on interc
ellular communication via NO, based on opposing effects of reagents th
at decrease or increase NO levels in the PC, Inhibition of NO synthase
slows the field potential oscillation, while application of exogenous
NO increases the oscillation frequency. A role for CO in PC dynamics
is suggested by experiments in which CO liberation increases the PC os
cillation frequency. These design features of the Limax PC lobe odor p
rocessing circuitry may relate to synaptic plasticity that subserves b
oth connection of new receptors throughout the life of the slug and it
s highly developed odor learning ability. (C) 1996 John Wiley & Sons,
Inc.