Dynamics of propagating waves in the olfactory network of a terrestrial mollusk: an electrical and optical study

Abstract

1. The procerebral (PC) lobe of the terrestrial mollusk Limax maximus contains a highly interconnected network of local olfactory interneurons that receives ipsilateral axonal projections from superior and inferior noses. This network exhibits an approximately 0.7-Hz intrinsic oscillation in its local field potential (LFP). 2. Intracellular recordings show that the lobe contains at least two classes of neurons with activity phase locked to the oscillation. Neurons in one class produce periodic bursts of spikes, followed by a period of hyperpolarization and subsequently a depolarizing afterpotential. There is a small but significant chance for a second burst to occur during the depolarizing afterpotential; this leads to a double event in the LFP. Bursting neurons constitute approximately 10% of the neurons in the lobe. 3. Neurons in the other class fire infrequently and do not produce periodic bursts of action potentials. However, they receive strong, periodic inhibitory input during every event in the LFP. These nonbursting cells constitute the major fraction of neurons in the lobe. There is a clear correlation between the periodic burst of action potentials in the bursting neurons and the hyperpolarization seen in nonbursting neurons. 4. Optical techniques are used to image the spatially averaged transmembrane potentials in preparations stained with voltage-sensitive dyes. The results of simultaneous optical and electrical measurements show that the major part of the optical signal can be interpreted as a superposition of the intracellular signals arising from the bursting and nonbursting neurons. 5. Successive 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 longitudinal axis. The direction of propagation in the unperturbed lobe is always from the distal to the proximal end. The wavelength varies between preparations but is on the order of the length of the preparation. 6. One-dimensional images along the longitudinal axis of the lobe are used to construct a space-time map of the optical activity, from which we calculate the absolute contribution of bursting and nonbursting neurons to the optical signal. The contribution of the intracellular signals from the two cell types appears to vary systematically across the lobe; bursting cells dominate at middle and proximal locations, and nonbursting cells dominate at distal locations. 7. The direction and form of the waves can be perturbed either by microsurgical manipulation of the preparation or by chemical modulation of its synaptic and neuronal properties.(ABSTRACT TRUNCATED AT 400 WORDS)

Voltage-gated membrane currents in neurons involved in odor information processing in snail procerebrum

“…Earlier optical and electrophysiological recordings confirmed that the PC contains at least two classes of neurons: bursting and non-bursting neurons (Ermentrout et al 1998;Kleinfeld et al 1994;Nikitin et al 2005). In the PC of Limax, bursting and non-bursting cells have been distinguished on the basis of their size, shape, and conduction velocity and it has been suggested that the somata of bursting neurons are larger than those of the non-bursting neurons (Watanabe et al 1998).…”

“…PC neurons display a resting cyclic electrical activity of 0.7 Hz, which is important for the storage of odor memory and odor discrimination (Balaban and Maksimova 1993;Delaney et al 1994;Gelperin and Tank 1990;Schütt et al 2000). This oscillatory activity was shown to be modulated by odor stimuli Gelperin and Tank 1990;Gervais et al 1996;Kimura et al 1998;Kleinfeld et al 1994) and by signal molecules such as nitrogen and carbon monoxide, c-aminobutyric acid, 5-hydroxytryptamine (5-HT), dopamine (DA), glutamate (Glu), acetylcholine (ACh) and endogenous neuropeptides such as FMRFa and catch-relaxing peptide, which are present in the PC Cooke and Gelperin 1988;Elekes and Nassel 1990;Gelperin et al 1993Gelperin et al , 2000Hernadi et al 1995;Inoue et al 2001;Kobayashi et al 2010). It was observed that 5-HT and DA excited PC neurons and promoted transitions from steady to bursting activity.…”

Nitric oxide-coupled signaling in odor elicited molecular events in the olfactory center of the terrestrial snail, Helix pomatia

“…Since NB cells, but not B cells, project to the internal neuropil it is assumed that NMDA-receptor-like immunoreactivity belongs to NB cells in the PC. If it is considered that B cells are the main source of Glu [12], then a glutamatergic input that evokes NO synthesis on NB cells seems reasonable (see Fig. 6.).…”

“…Track tracing experiments have revealed the members of the neuronal afferents and the types and morphology of PC interneurons [5,6,7,8,9,10]. In addition to morphological findings, electrophysiological recording has also demonstrated that the population of PC cells within the layer where the perikarya of PC interneurons are located (the cell mass layer) consists of large number (75%) of non-bursting (NB) neurons with small size (5-8 μm), and a smaller number (25%) of bursting (B) neurons of larger size (10-15 μm) [11,12].…”

Model for Transition from Waves to Synchrony in the Olfactory Lobe of Limax

“…The PC lobe also propagates activity waves from its apical to basal pole at 1.1 mm/sec in vitro Kimura et al, 1998b;Kleinfeld et al, 1994). The activity waves serve to separate odor representations set up in the PC lobe by associative conditioning when odors are used as conditioned stimuli Gelperin, 1999;Kimura et al, 1998a).…”