FMRFamide regulates oscillatory activity of the olfactory center in the slug

Abstract

In the olfactory center of terrestrial animals, changes in the oscillatory frequency of the local field potential (LFP) are thought to be involved in olfaction-based behavior and olfactory memory. The terrestrial slug Limax has a highly developed olfactory center, the procerebrum, in which the LFP spontaneously oscillates. Although changes in the oscillatory frequency are thought to correspond to the preference for specific odors, our knowledge about the mechanism of this frequency regulation is limited. To clarify the mechanism of the bidirectional frequency changes in the procerebrum, we focused on the neuropeptide Phe-Met-Arg-Phe-NH₂ (FMRFamide), which is known to have neuromodulatory functions in invertebrate nervous systems. Application of FMRFamide decreased the oscillatory frequency via G-protein-mediated cascades. Immunohistochemistry showed that FMRFamide-like-immunoreactive neuronal cell bodies are located in the cell mass layer of the procerebrum, projecting their neurites to the neuropile layers. The procerebrum was shown to also receive innervation from other regions of the cerebral ganglion. Furthermore, according to their morphological and projection characteristics, FMRFamide-containing neurons belong to the subpopulations of both bursting and nonbursting neurons in the procerebrum. The mRNA splice variant encoding multiple copies of canonical FMRFamide was specifically expressed in the procerebrum. Taking into account previous results showing that serotonin increases the oscillatory frequency, our results indicate that FMRFamide and serotonin both regulate the LFP frequency but in exactly the opposite direction in the olfactory center of the terrestrial slug.

Effects of tentacle amputation and regeneration on the morphology and activity of the olfactory center of the terrestrial slug Limax valentianus

“…To explore this possibility, the FMRFamidergic fibers were immunohistochemically stained in the sections of the cerebral ganglion cut in the coronal direction (Fig.4H). It has been demonstrated previously that FMRFamidergic primary sensory afferents ascend in the tentacular nerves to the cerebral ganglion, and these afferents disappear 14 days following amputation of the superior tentacle, possibly reflecting the nerve degeneration caused by tentacle amputation Kobayashi et al, 2010). We could reproduce this result 15 days after the surgical amputation of the right superior and inferior tentacles (Fig.4A,B).…”

“…We also examined the innervation of afferent inputs by immunohistochemical staining of the nerves containing Phe-Met-Arg-Phe-NH 2 (FMRFa) peptides that are thought to have projections from the tentacle Kobayashi et al, 2010). Finally, we analyzed the LFP oscillation of the PC in vitro to assess the recovery of its electrophysiological activity.…”

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

“…PC [41,72]. These observations, taken together with the findings of other authors [26,40,41,69] and our recent data [27,28] indicate that NO is a prominent neurochemical substance in the olfactory center of terrestrial snails. Applying NO-scavenger, fluorescence microscopy, and flow cytometry, we have provided further evidence that both the NB and B cell types of isolated PC neurons [1] are capable of synthesizing NO.…”

“…The presence of neurotransmitters (glutamate, Glu [and its vesicular transporter, vGluT, 23], GABA [24,25], 5-HT [22], nitric oxide [NO, 26,27,28], acetylcholine [29], histamine [30]), and different neuropeptides [31,32,33,34,35] were demonstrated immunohistochemically. This, together with the findings on their effect following exogenous application [23,29,30,35,36,37,38,39,40], underlined the complex intrinsic and extrinsic regulation of neuronal activity in the PC.…”

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

“…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.…”