DYNAMICS OF PROPAGATING WAVES IN THE OLFACTORY NETWORK OF A TERRESTRIAL MOLLUSK - AN ELECTRICAL AND OPTICAL STUDY

1. The procerebral (PC) lobe of the terrestrial mollusk Limax maximus contains a highly interconnected network of local olfactory interneuro ns that receives ipsilateral axonal projections from superior and infe rior noses. This network exhibits an similar to 0.7-Hz intrinsic oscil lation in its local field potential (LFP). 2. Intracellular recordings show that the lobe contains at least two classes of neurons with acti vity phase locked to the oscillation. Neurons in one class produce per iodic bursts of spikes, followed by a period of hyperpolarization and subsequently a depolarizing afterpotential. There is a small but signi ficant chance for a second burst to occur during the depolarizing afte rpotential; this leads to a double event in the LFP. Bursting neurons constitute similar to 10% of the neurons in the lobe. 3. Neurons in th e other class fire infrequently and do not produce periodic bursts of action potentials. However, they receive strong, periodic inhibitory i nput during every event in the LFP. These nonbursting cells constitute the major fraction of neurons in the lobe. There is a dear correlatio n between the periodic burst of action potentials in the bursting neur ons and the hyperpolarization seen in nonbursting neurons. 5. Successi ve images of the entire PC lobe show waves of electrical activity that span the width of the lobe and travel its full length along a longitu dinal axis. The direction of propagation in the unperturbed lobe is al ways from the distal to the proximal end. The wavelength varies betwee n preparations but is on the order of the length of the preparation. 6 . One-dimensional images along the longitudinal axis of the lobe are u sed to construct a space-time map of the optical activity, from which we calculate the absolute contribution of bursting and nonbursting neu rons to the optical signal. The contribution of the intracellular sign als from the two cell types appears to vary systematically across the lobe; bursting cells dominate at middle and proximal locations, and no nbursting cells dominate at distal locations. 4. Optical techniques ar e used to image the spatially averaged transmembrane potentials in pre parations stained with voltage-sensitive dyes. The results of simultan eous optical and electrical measurements show that the major part of t he optical signal can be interpreted as a superposition of the intrace llular signals arising from the bursting and nonbursting neurons. 7. T he direction and form of the waves can be perturbed either by microsur gical manipulation of the preparation or by chemical modulation of its synaptic and neuronal properties. These results suggest that the dire ction of propagation arises from dynamic properties of the network, as opposed to an architecture with unidirectional connectivity. Further, fragments of the lobe oscillate after surgical isolation, showing tha t there is not a single pacemaker region in the lobe. 8. The periodic LFP occasionally exhibits rapid, double events during which the propag ating wave state is seen to transiently shift to one with nearly spati ally synchronized activity along the lengthof the lobe. This indicates that the lobe can support a state with essentially no temporal phase gradient, as well as one with propagating waves. 9. Although details o f the circuitry within the lobe are largely unknown, analogies between the dynamics reported here and theoretical understanding of excitable media suggest that the temporal phase gradient originates from a spat ial gradient of excitability along the lobe. Consistent with this hypo thesis is the observation that surgically isolated distal halves of th e lobe oscillate faster than isolated proximal halves.