Lidocaine treatment during synapse reformation periods permanently inhibits NGF-induced excitation in an identified reconstructed synapse of Lymnaea stagnalis

Onizuka, Shin; Shiraishi, Seiji; Tamura, Ryuuji; Yonaha, Tetsu; Oda, Nobuko; Kawasaki, Yuko; Syed, Naweed I.; Shirasaka, Tetsuro; Tsuneyoshi, Isao

doi:10.1007/s00540-011-1257-6

Cited by 12 publications

(11 citation statements)

References 35 publications

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“…Our results demonstrated that the synaptic responses (EPSPs) had higher sensitivity to neonicotinoids and the inhibition was less reversible compared to the membrane responses (depolarization) evoked by ACh on the same follower, RPeD1 (as seen on (Onizuka et al, 2012). These results confirm a potential functional heterogeneity, in terms of different sensitivities or coupling mechanisms, of the nACh receptors which are located synaptically versus extrasynaptically on the same neuron.…”

Section: Discussionsupporting

confidence: 75%

“…Both connections have also been shown to re-form between the isolated neurons when placed in culture conditions (Syed et al, 1990;Hamakawa et al, 1999). The first, excitatory component of these monosynaptic connections provides a suitable in vitro model while studying synaptogenesis (Feng et al, 1997;Woodin et al, 2002), or toxin-induced alterations of cholinergic neurotransmission (Woodall et al, 2003;Onizuka et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Neonicotinoid insecticides inhibit cholinergic neurotransmission in a molluscan (Lymnaea stagnalis) nervous system

et al. 2015

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Neonicotinoids are highly potent and selective systemic insecticides, but their widespread use also has a growing impact on non-target animals and contaminates the environment, including surface waters. We tested the neonicotinoid insecticides commercially available in Hungary (acetamiprid, Mospilan; imidacloprid, Kohinor; thiamethoxam, Actara; clothianidin, Apacs; thiacloprid, Calypso) on cholinergic synapses that exist between the VD4 and RPeD1 neurons in the central nervous system of the pond snail Lymnaea stagnalis. In the concentration range used (0.01-1 mg/ml), neither chemical acted as an acetylcholine (ACh) agonist; instead, both displayed antagonist activity, inhibiting the cholinergic excitatory components of the VD4-RPeD1 connection. Thiacloprid (0.01 mg/ml) blocked almost 90 % of excitatory postsynaptic potentials (EPSPs), while the less effective thiamethoxam (0.1mg/ml) reduced the synaptic responses by about 15 %. The ACh-evoked membrane responses of the RPeD1 neuron were similarly inhibited by the neonicotinoids, confirming that the same ACh receptor (AChR) target was involved. We conclude that neonicotinoids act on nicotinergic acetylcholine receptors (nAChRs) in the snail CNS. This has been established previously in the insect CNS; however, our data indicate differences in the background mechanism or the nAChR binding site in the snail. Here we provide the first results concerning neonicotinoid-related toxic effects on the neuronal connections in the molluscan nervous system. Aquatic animals, including molluscs, are at direct risk while facing contaminated surface waters, and snails may provide a suitable model for further studies of the behavioural/neuronal consequences of intoxication by neonicotinoids.Tihany, Hungary, July 22, 2015 Dr. Mikko Nikinmaa Editorial Office Aquatic ToxicologyDear Dr Nikinmaa, Thank you very much for your response to our manuscript submission. We gratefully thank you and our reviewers for reading the manuscript, and we appreciate all the helpful comments made.After carefully checking the Reviewers' comments we improved the manuscript on the basis of their suggestions. Please find our detailed answers to the Reviewers below. Reviewer #1:We greatly appreciate the Reviewer's comment "one of the best written manuscripts that I have reviewed" Minor points Materials and Methods How was Lymnaea saline obtained? Is this the modified HiDi saline? If not, what is HiDi?For isolating the monosynaptic components of the synaptic responses between two neurons the perfusion chamber was filled with a modified saline which reduces the polysynaptically evoked postsynaptic responses and enhances the monosynaptic component (Berry and Pentreath, 1976). This modified saline contains higher amount of divalent cations (Ca 2+ and Mg 2+ ), therefore often nicknamed as HiDi saline (Brierly et al., 1997, Sivaramakrishnan et al., 2013. We added details to the text accordingly Electrophysiological recordingThere is a Winlow 1991 anda Syed et al. 1990 (PNEC, EC50, mechanistic...) We...

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Section: Discussionsupporting

confidence: 75%

Section: Introductionmentioning

confidence: 99%

Neonicotinoid insecticides inhibit cholinergic neurotransmission in a molluscan (Lymnaea stagnalis) nervous system

et al. 2015

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“…The following are examples of the main types of research conducted using cultured neuronal cells. (1) identification and functional characterization of neurotrophic factors regulating neurite outgrowth and regeneration (Spence et al 1998; Goldberg 1998; Munno et al 2000; Dmetrichuk et al 2008; Milanese et al 2009; Nejatbakhsh et al 2011 and others ), (2) growth cone motility and development (Spencer et al 1998; Dmetrichuk et al 2008; Suter 2011), (3) neurite-soma and soma-soma synaptogenesis (Munno et al 2000; Hu et al 2004; Onizuka et al 2012) and (4) neuronal receptors and cell-to-cell neurotransmitter signaling (White and Laczmarek 1997; Mapara et al 2008; Giachello et al 2010; Ye et al 2010). …”

Section: Molluscan Primary Cell Culturesmentioning

confidence: 99%

Molluscan cells in culture: primary cell cultures and cell lines

2013

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In vitro cell culture systems from molluscs have significantly contributed to our basic understanding of complex physiological processes occurring within or between tissue-specific cells, yielding information unattainable using intact animal models. In vitro cultures of neuronal cells from gastropods show how simplified cell models can inform our understanding of complex networks in intact organisms. Primary cell cultures from marine and freshwater bivalve and gastropod species are used as biomonitors for environmental contaminants, as models for gene transfer technologies, and for studies of innate immunity and neoplastic disease. Despite efforts to isolate proliferative cell lines from molluscs, the snail Biomphalaria glabrata Say, 1818 embryonic (Bge) cell line is the only existing cell line originating from any molluscan species. Taking an organ systems approach, this review summarizes efforts to establish molluscan cell cultures and describes the varied applications of primary cell cultures in research. Because of the unique status of the Bge cell line, an account is presented of the establishment of this cell line, and of how these cells have contributed to our understanding of snail host-parasite interactions. Finally, we detail the difficulties commonly encountered in efforts to establish cell lines from molluscs and discuss how these difficulties might be overcome.

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“…Its actions can be accounted for by assuming that procaine binds preferentially to the activated receptor-channel complex and converts it into a non-conducting state (Ascher et al, 1976; Marty, 1978). In Achatina fulica (Ferussac), procaine initiated paroxysmal depolarizing shifts (PDSs) in the RP1 neuron, which were decreased if lithium replaced Na + in the bathing medium or in a high magnesium solution (Lin and Tsai, 2005), suggesting similar effects to those observed with lidocaine by Onizuka et al (2012a) (see above). In addition, PDS was associated with phospholipase activity and calcium mobilization in the neuron (Lin et al, 2010).…”

Section: Actions Of Clinical Anesthetics On Gastropod Molluscsmentioning

confidence: 81%

“…By pairing VD4 with neurons from the left pedal E (LPeE) cluster it has also been possible to show that lidocaine treatment during synapse formation permanently suppresses nerve growth factor (NGF) induced excitation by suppressing both axonal growth and neurotransmitter release from presynaptic neurons (Onizuka et al, 2012a) probably by suppressing voltage-dependent calcium currents (Kasaba et al, 2006). …”

Section: Actions Of Clinical Anesthetics On Gastropod Molluscsmentioning

confidence: 99%

Sense and Insensibility – An Appraisal of the Effects of Clinical Anesthetics on Gastropod and Cephalopod Molluscs as a Step to Improved Welfare of Cephalopods

et al. 2018

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Recent progress in animal welfare legislation stresses the need to treat cephalopod molluscs, such as Octopus vulgaris, humanely, to have regard for their wellbeing and to reduce their pain and suffering resulting from experimental procedures. Thus, appropriate measures for their sedation and analgesia are being introduced. Clinical anesthetics are renowned for their ability to produce unconsciousness in vertebrate species, but their exact mechanisms of action still elude investigators. In vertebrates it can prove difficult to specify the differences of response of particular neuron types given the multiplicity of neurons in the CNS. However, gastropod molluscs such as Aplysia, Lymnaea, or Helix, with their large uniquely identifiable nerve cells, make studies on the cellular, subcellular, network and behavioral actions of anesthetics much more feasible, particularly as identified cells may also be studied in culture, isolated from the rest of the nervous system. To date, the sorts of study outlined above have never been performed on cephalopods in the same way as on gastropods. However, criteria previously applied to gastropods and vertebrates have proved successful in developing a method for humanely anesthetizing Octopus with clinical doses of isoflurane, i.e., changes in respiratory rate, color pattern and withdrawal responses. However, in the long term, further refinements will be needed, including recordings from the CNS of intact animals in the presence of a variety of different anesthetic agents and their adjuvants. Clues as to their likely responsiveness to other appropriate anesthetic agents and muscle relaxants can be gained from background studies on gastropods such as Lymnaea, given their evolutionary history.

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Lidocaine treatment during synapse reformation periods permanently inhibits NGF-induced excitation in an identified reconstructed synapse of Lymnaea stagnalis

Cited by 12 publications

References 35 publications

Neonicotinoid insecticides inhibit cholinergic neurotransmission in a molluscan (Lymnaea stagnalis) nervous system

Neonicotinoid insecticides inhibit cholinergic neurotransmission in a molluscan (Lymnaea stagnalis) nervous system

Molluscan cells in culture: primary cell cultures and cell lines

Sense and Insensibility – An Appraisal of the Effects of Clinical Anesthetics on Gastropod and Cephalopod Molluscs as a Step to Improved Welfare of Cephalopods

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