CENTRAL AND REFLEX NEURONAL RESPONSES ELICITED BY ODOR IN A TERRESTRIAL MOLLUSK

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 record ing from preparations stained with a voltage-sensitive dye to characte rize network responses in the central organ and whole nerve recording to characterize central odor-elicited outputs. 2. The central olfactor y organ, the procerebral (PC) lobe, is a highly interconnected network of local olfactory interneurons that receives input from primary olfa ctory receptors. In the absence of odor the PC network is known to exh ibit periodic waves of excitation and inhibition at a frequency of sim ilar to 0.7 Hz. Here we study how different odor inputs affect the int rinsic oscillatory dynamics. 3. Odor stimulation causes the propagatio n of electrical activity along the lobe to transiently switch from the state with propagating waves, with typical phase shifts of one half c ycle 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 l east on the scale of our optical resolution, similar to 0.1 times the length of the lobe. In some trials, however, we resolved spatial nonun iformities in the magnitude of excitation across the lobe. 4. The coll apse of the phase gradient along the lobe in response to odor stimulat ion 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 oscill ation, as occasionally observed in response to weak odor stimulation. 5. Typically odor stimulation causes changes in the frequency of the o scillation. Two odors, one attractive(potato) and one repellent (amyl acetate), produced different patterns of change; potato induced a tran sient increase in frequency, whereas amyl acetate produced an initial decrease in frequency followed by a transient increase in frequency. W e do not yet know whether these frequency change patterns are unique t o these specific odors or to their behavioral meaning. 6. Previous wor k demonstrated direct connections from the PC lobe to the buccal and p edal ganglia, centers controlling feeding and locomotion, respectively . To establish a correlation between odor-induced changes in the PC lo be 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-elic ited activity before and after PC ablation. 7. Odor stimulation caused activation of multiple units in the cerebrobuccal connective. One out put of the buccal ganglion, the salivary nerve, also showed odor-elici ted activation of an identified unit, the slow burster. The necessity of the PC lobe for activation of the slow burster was established by m easurements of odor-elicited activity before and after PC ablation. 8. Odor stimulation also caused activation of multiple units in the bucc al 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 c ircuit without changing the overall average level of activity in that circuit.