Evidence That the Swim Afferent Neurons ofTritonia diomedeaAre Glutamatergic

Abstract

The escape swim response of the marine mollusc Tritonia diomedea is a well-established model system for studies of the neural basis of behavior. While the swim neural network is reasonably well understood, little is known about the transmitters used by its constituent neurons. In the present study, we provide immunocytochemical and electrophysiological evidence that the S-cells, the afferent neurons that detect aversive skin stimuli and in turn trigger Tritonia’s escape swim response, use glutamate as their transmitter. First, immunolabeling revealed that S-cell somata contain elevated levels of glutamate compared to most other neurons in the Tritonia brain, consistent with findings from glutamatergic neurons in many species. Second, pressure-applied puffs of glutamate produced the same excitatory response in the target neurons of the S-cells as the naturally released S-cell transmitter itself. Third, the glutamate receptor antagonist CNQX completely blocked S-cell synaptic connections. These findings support glutamate as a transmitter used by the S-cells, and will facilitate studies using this model system to explore a variety of issues related to the neural basis of behavior.

An Argument for Amphetamine-Induced Hallucinations in an Invertebrate

“…Because SMPs also occurred spontaneously in the presence of AMPH (mean = 4.73 ± 0.76 SMPs, range = 1–10 per preparation), an SMP was considered to have been triggered by the S-cell current pulse if the speed-up of DSI tonic firing signaling motor program onset began within 2 s after the end of the S-cell current injection. Such triggering of SMPs by single S-cells has never been observed by us in normal saline, either during this study, or across several years of work with S-cells ( Frost et al, 2001 , 2003 ; Megalou et al, 2009 ; Lee et al, 2012 ). Ten of the 36 recorded S-cells, in 7 preparations, also exhibited firing that continued beyond the end of the current pulse in AMPH (mean = 24.08 ± 8.55 extra spikes, range = 1–101), a phenomenon also never observed in normal saline in these experiments or in prior work ( Figures 4A,B ).…”

“…Having traced the origin of the spontaneous AMPH-SMP as far as the swim command neurons, we next turned to their input, the well-characterized swim afferent neurons (S-cells). The S-cells have their cell bodies located in a cluster on the dorsal side of each pleural ganglion ( Getting, 1976 ; Megalou et al, 2009 ). Each pseudounipolar S-cell sends one or more axons out peripheral nerves to innervate specific regions of the skin ( Getting, 1976 ; Frost et al, 2003 ).…”

Axonal Conduction Block as a Novel Mechanism of Prepulse Inhibition

“…S-cells . These CNS afferent neurons for the animal’s escape swim startle response were identified based on their location, size, color, lack of activity at rest, and response to electrical stimulation (Getting, 1976; Megalou et al, 2009). The S cells form a bilateral cluster of approximately 100 orange-pigmented ~50μm diameter neurons per cluster (Fig.…”

Neural shutdown under stress: an evolutionary perspective on spreading depolarization

“…Hence, assuming that the similarity between insect and mammalian SD reflects a fundamental etiology, a focus on the potential role of a specific transmitter or receptor subtype in triggering SD may be short-sighted (except in the context of therapeutic drug discovery). To better understand SD, it may be more fruitful to consider what neural and CNS properties predispose to SD in insect and mammalian nervous tissue and how they differ from the properties of nervous systems that have well described CNS glutamate neurotransmission, such as in molluscs (Di Cosmo et al 2006;Ha et al 2006;Megalou et al 2009), but for which there is no current evidence for the existence of a process resembling SD. Modeling approaches that incorporate generic properties of channels and pumps independently of species-specific molecular identities have much to offer (Ullah et al 2015;Wei et al 2014).…”