Central and reflex neuronal responses elicited by odor in a terrestrial mollusk

Abstract

1. We studied the responses to odor of a central olfactory processing organ and subsequent central outputs in the terrestrial mollusk Limax maximus. We used extracellular recording techniques and optical recording from preparations stained with a voltage-sensitive dye to characterize network responses in the central organ and whole nerve recording to characterize central odor-elicited outputs. 2. The central olfactory organ, the procerebral (PC) lobe, is a highly interconnected network of local olfactory interneurons that receives input from primary olfactory receptors. In the absence of odor the PC network is known to exhibit periodic waves of excitation and inhibition at a frequency of approximately 0.7 Hz. Here we study how different odor inputs affect the intrinsic oscillatory dynamics. 3. Odor stimulation causes the propagation of electrical activity along the lobe to transiently switch from the state with propagating waves, with typical phase shifts of one half cycle along the lobe, to a state with few or no phase differences along the lobe. The collapse of the phase gradient typically occurs without spatially localized changes in the amplitude of the oscillation, at least on the scale of our optical resolution, approximately 0.1 times the length of the lobe. In some trials, however, we resolved spatial nonuniformities in the magnitude of excitation across the lobe. 4. The collapse of the phase gradient along the lobe in response to odor stimulation is robust on a trial-by-trial basis. Further, the change in phase gradient can occur with little or no change in the frequency of oscillation, as occasionally observed in response to weak odor stimulation. 5. Typically odor stimulation causes changes in the frequency of the oscillation. Two odors, one attractive (potato) and one repellent (amyl acetate), produced different patterns of change; potato induced a transient increase in frequency, whereas amyl acetate produced an initial decrease in frequency followed by a transient increase in frequency. We do not yet know whether these frequency change patterns are unique to these specific odors or to their behavioral meaning. 6. Previous work demonstrated direct connections from the PC lobe to the buccal and pedal ganglia, centers controlling feeding and locomotion, respectively. To establish a correlation between odor-induced changes in the PC lobe and activation of such centers and subsequently effector organs, we recorded from selected central connectives and peripheral nerve roots. The dependence of odor-elicited activity recorded in connectives and nerve roots on PC integrity was assessed by measurements of odor-elicited activity before and after PC ablation. 7. Odor stimulation caused activation of multiple units in the cerebrobuccal connective. One output of the buccal ganglion, the salivary nerve, also showed odor-elicited activation of an identified unit, the slow burster. The necessity of the PC lobe for activation of the slow burster was established by measurements of odor-elicited activity before and after PC ablation. 8. Odor stimulation also caused activation of multiple units in the buccal mass retractor nerve. Activation of a fraction of these units (3 of 10) was dependent on an intact PC lobe, like the slow burster neuron in the salivary nerve. 9. Our results clearly show how stimuli may lead to changes in the spatial-temporal pattern of activity in a central circuit without changing the overall average level of activity in that circuit.