Properties of cannabinoid-dependent long-term depression in the leech

Li, Qin; Burrell, Brian D.

doi:10.1007/s00359-010-0566-9

Cited by 9 publications

(10 citation statements)

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“…Intracellular heparin injection in the absence of T and S cell pairing had no effect on synaptic transmission. These findings indicate that Ca 2+ release from intracellular stores contributed to eCB-LTD, but not NMDAR-LTD and that store-released Ca 2+ was mediated by IP3 receptors and not RyRs, consistent with earlier studies of eCB-LTD in the leech (Li and Burrell 2010).…”

Section: Role Of Casupporting

confidence: 90%

“…Therefore, the role of VGCCs was tested during both forms of LTD using 1 mM NiCl 2 (Ni 2+ ), which has been shown to block low threshold, but not high threshold VGCCs in leech neurons (Ivanov and Calabrese 2006b). As shown in Figure 3B, Ni 2+ inhibited LTD following long interval pairing (one-way ANOVA, F (1,8) ¼ 19.07, P , 0.01; n ¼ 5 in each group) consistent with earlier studies indicating that Ca 2+ influx through VGCCs contributed to eCB-LTD in the leech (Li and Burrell 2010). Ni 2+ treatment did not inhibit LTD following short interval pairing (one-way ANOVA, F (1,13) ¼ 2.14, P .…”

Section: Role Of Casupporting

confidence: 89%

“…1A). The majority of synaptic input by the T cell to the S interneuron is through input to the C cells and small molecular weight dyes and pharmacological agents have been shown to spread from the S cell to the C cell (Muller and Scott 1981;Li and Burrell 2010).…”

Section: Properties Of Ecb-ltdmentioning

confidence: 99%

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Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms

Li¹,

Burrell²

2011

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Persistent, bidirectional changes in synaptic signaling (that is, potentiation and depression of the synapse) can be induced by the precise timing of individual pre-and postsynaptic action potentials. However, far less attention has been paid to the ability of paired trains of action potentials to elicit persistent potentiation or depression. We examined plasticity following the pairing of spike trains in the touch mechanosensory neuron (T cell) and S interneuron (S cell) in the medicinal leech. Long-term potentiation (LTP) of T to S signaling was elicited when the T-cell spike train preceded the S-cell train. An interval 0 to +1 sec between the T-and S-cell spike trains was required to elicit long-term potentiation (LTP), and this potentiation was NMDA receptor (NMDAR)-dependent. Long-term depression (LTD) was elicited when S-cell activity preceded T-cell activity and the interval between the two spike trains was 20.2 sec to 210 sec. This surprisingly broad temporal window involved two distinct cellular mechanisms; an NMDAR-mediated LTD (NMDAR-LTD) when the pairing interval was relatively brief (,21 sec) and an endocannabinoid-mediated LTD (eCB-LTD) when longer pairing intervals were used (21 to 210 sec). This eCB-LTD also required activation of a presynaptic transient receptor potential vanilloid (TRPV)-like receptor, presynaptic Ca 2+ release from intracellular stores and activation of voltage-gated Ca 2+ channels (VGCCs). These findings demonstrate that the pairing of spike trains elicits timing-dependent forms of LTP and LTD that are supported by a complex set of cellular mechanisms involving NMDARs and endocannabinoid activation of TRPV-like receptors.[Supplemental material is available for this article.]Associative forms of long-term neuroplasticity, as first proposed by Hebb (1949), depend on the temporal relationship between pre-and postsynaptic activity. Studies of spike-timing-dependent plasticity (STDP) have provided experimental confirmation of this principle, specifically that in most connections long-term potentiation (LTP) is produced when a presynaptic action potential (or spike) precedes the postsynaptic spike, whereas long-term depression (LTD) is produced when the order is reversed (see review by Caporale and Dan 2008). In addition to the temporal order being important in determining the sign of the synaptic change, temporal proximity is also critical in that the time between the pre-and postsynaptic activity must be sufficiently brief, usually ,40 msec, to support potentiation or depression.It has been noted that the time intervals between pre-and postsynaptic activity that support STDP are not as long as those observed in many associative learning experiments, in which interstimulus intervals on the scale of seconds can be used to elicit successful conditioning (Drew and Abbott 2006). Most studies of STDP involve pairing single pre-and postsynaptic spikes or brief bursts of two to three spikes; however, many neurons communicate using relatively long trains of action potentials that are tens...

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Section: Role Of Casupporting

confidence: 90%

Section: Role Of Casupporting

confidence: 89%

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Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms

Li¹,

Burrell²

2011

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“…Furthermore, this particular form of LTD also involves stimulation of nitric oxide synthase and a decrease in cAMP signalling [125]. However, because synaptic plasticity is being examined here in the context of a polysynaptic pathway, mechanistic interpretation of these findings is complicated.…”

Section: Review Evolution and Comparative Neurobiology M R Elphickmentioning

confidence: 99%

The evolution and comparative neurobiology of endocannabinoid signalling

Elphick

2012

Phil. Trans. R. Soc. B

154

137

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CB 1 -and CB 2 -type cannabinoid receptors mediate effects of the endocannabinoids 2-arachidonoylglycerol (2-AG) and anandamide in mammals. In canonical endocannabinoid-mediated synaptic plasticity, 2-AG is generated postsynaptically by diacylglycerol lipase alpha and acts via presynaptic CB 1 -type cannabinoid receptors to inhibit neurotransmitter release. Electrophysiological studies on lampreys indicate that this retrograde signalling mechanism occurs throughout the vertebrates, whereas system-level studies point to conserved roles for endocannabinoid signalling in neural mechanisms of learning and control of locomotor activity and feeding. CB 1 /CB 2 -type receptors originated in a common ancestor of extant chordates, and in the sea squirt Ciona intestinalis a CB 1 / CB 2 -type receptor is targeted to axons, indicative of an ancient role for cannabinoid receptors as axonal regulators of neuronal signalling. Although CB 1 /CB 2 -type receptors are unique to chordates, enzymes involved in biosynthesis/inactivation of endocannabinoids occur throughout the animal kingdom. Accordingly, non-CB 1 /CB 2 -mediated mechanisms of endocannabinoid signalling have been postulated. For example, there is evidence that 2-AG mediates retrograde signalling at synapses in the nervous system of the leech Hirudo medicinalis by activating presynaptic transient receptor potential vanilloid-type ion channels. Thus, postsynaptic synthesis of 2-AG or anandamide may be a phylogenetically widespread phenomenon, and a variety of proteins may have evolved as presynaptic (or postsynaptic) receptors for endocannabinoids.

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“…The endocannabinoids and endovanilloids AEA and 2-AG are present in the leech CNS (Matias et al, 2001), yet the leech and other protostomal invertebrates lack orthologs to the CB1 and CB2 receptors (Elphick, 2012). There is, however, evidence that central TRPV-like channels mediate synaptic plasticity in the leech via mechanisms that are similar to those observed in vertebrates (Li and Burrell, 2010;Yuan and Burrell, 2010;Li and Burrell, 2011;Yuan and Burrell, 2012; Higgins et al, 2013;Yuan and Burrell, 2013). …”

mentioning

confidence: 98%

Physiological and behavioral evidence of a capsaicin sensitive TRPV-like channel in the medicinal leech

Summers

Holec

Burrell

2014

Journal of Experimental Biology

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Transient receptor potential vanilloid (TRPV) channels are found throughout the animal kingdom, where they play an important role in sensory transduction. In this study, we combined physiological studies with in vivo behavioral experiments to examine the presence of a putative TRPV-like receptor in the medicinal leech, building upon earlier studies in this lophotrochozoan invertebrate. The leech polymodal nociceptive neuron was activated by both peripheral and central application of the TRPV1-activator capsaicin in a concentration-dependent manner, with 100 μmol l −1 being the lowest effective concentration. Responses to capsaicin were inhibited by the selective TRPV1 antagonist SB366791. The polymodal nociceptive neuron also responded to noxious thermal stimuli (>40°C), and this response was also blocked by SB366791. Capsaicin sensitivity was selective to the polymodal nociceptor with no direct response being elicited in the mechanical nociceptive neuron or in the nonnociceptive touch-or pressure-sensitive neurons. Capsaicin also elicited nocifensive behavioral responses (withdrawals and locomotion) in a concentration-dependent manner, and these behavioral responses were significantly attenuated with SB366791. These results suggest the presence of a capsaicin-sensitive TRPVlike channel in the medicinal leech central nervous system and are relevant to the evolution of nociceptive signaling. KEY WORDS: Leech, TRPV, Invertebrate, Nociception INTRODUCTIONTransient receptor potential (TRP) channels are a diverse class of non-specific cation channels that are found throughout the animal kingdom (Damann et al., 2008). TRP channels are typically associated with sensory transduction and are often polymodal, such as the mammalian TRP-vanilloid 1 (TRPV1) channel, which responds to noxious thermal (>42°C), mechanical and chemical (low pH, capsaicin) stimuli (Szallasi and Blumberg, 1999). Capsaicin sensitivity varies greatly throughout metazoans, with mammals displaying the greatest response to capsaicin. Birds, once thought to be capsaicin insensitive, have been shown to respond to capsaicin at increased concentrations (30 μmol l −1 ) compared with mammals (Kirifides et al., 2004). Even among mammals, capsaicin sensitivity varies greatly between species, and this variance is further complicated by ontogentic shifts in capsaicin sensitivity within specific strains of mice (Holzer, 1991). Invertebrate sensitivity to capsaicin is no less complicated because ecdysozoans, such as Drosophila (Vriens et al., 2004) and Caenorhabditis elegans (Tobin RESEARCH ARTICLECenter for Brain and Behavior Research, Division of Basic Biomedical Sciences, Sanford, School of Medicine, University of South Dakota, Vermillion, SD 57069, USA. *Author for correspondence (bburrell@usd.edu)Received 23 June 2014; Accepted 7 October 2014 et al., 2002), are reported to be capsaicin insensitive, whereas lophotrochozoans, specifically the gastropod Megalobulimus (KalilGaspar et al., 2007) and the medicinal leech (Hirudo verbana, Carena 1820) (Pasto...

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Properties of cannabinoid-dependent long-term depression in the leech

Cited by 9 publications

References 63 publications

Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms

Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms

The evolution and comparative neurobiology of endocannabinoid signalling

Physiological and behavioral evidence of a capsaicin sensitive TRPV-like channel in the medicinal leech

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