IP3-mediated octopamine-induced synaptic enhancement of crayfish LG neurons

Abstract

The biogenic amines, octopamine and serotonin, modulate the synaptic activity of the lateral giant interneuron (LG) circuitry of the crayfish escape behavior. Bath application of both octopamine and serotonin enhances the synaptic responses of LG to sensory stimulation. We have shown previously (Araki et al. J Neurophysiol 94:2644-2652, 2005) that a serotonin-induced enhancement of the LG response was mediated by an increase in cAMP levels following activation of adenylate cyclase; however, octopamine acts independently. Here, we clarify how octopamine enhances the LG response during sensory stimulation using physiological and pharmacological analyses. When phospholipase C inhibitor U-73122 was directly injected into the LG before biogenic amine application, it abolished the enhancing effect of octopamine on direct sensory input to the LG, but did not block indirect input via sensory interneurons or the effect of serotonin. Direct injection of IP(3), and its analogue adenophostin A, into the LG increased the synaptic response of the LG to sensory stimulation. Thus, IP(3) mediates octopamine-induced synaptic enhancement of the LG, but serotonin acts independently. These results indicate that both octopamine and serotonin enhance the synaptic responses of the LG to sensory stimulation, but that they activate two different signaling cascades in the LG.

Serotonergic modulation of social status-dependent behavioural plasticity of the crayfish avoidance reaction

“…In the crayfish and lobster, serotonin and octopamine are frequently shown to have opposite modulatory effects on synaptic transmission in the central nervous system (Harris-Warrick and Kravitz 1984;Harris-Warrick 1985;Glanzman and Krasne 1983;Yeh et al 1997;Araki et al 2005Araki et al , 2013Araki and Nagayama 2012). Direct injection of serotonin into the systemic circulation of crayfish and lobsters results in long-lasting tonic postural flexion, while the injection of octopamine enhances tonic postural extension (Livingstone et al 1980;Tierney and Mangiamele 2001).…”

Cellular, molecular, and epigenetic mechanisms in non-associative conditioning: Implications for pain and memory

“…For example, the crayfish LG-mediated tailflip escape behavior is augmented through release of octapamine, which is dependent on IP3 (Araki and Nagayama, 2012), but not cAMP (Araki, Nagayama, and Sprayberry, 2005) signaling cascades. Mechanosensory afferents from the crayfish tailfan excite behavior primarily through electrical synapses on the LG (Zucker, 1972); however they also impact cholinergic signaling on sensory interneurons (Miller, Vu, and Krasne, 1992).…”

Habituation of LG-mediated tailflip in the crayfish

“…Descending tonic inputs are thought necessary to maintain habituation for long periods (Krasne and Teshiba 1995). The action of serotonin and octopamine is related to the activation of cAMP and IP 3 s messenger systems Araki and Nagayama 2012). Since descending inputs from brain exert moment-to-moment control over LG's excitability and habituation (Krasne and Teshiba 1995;Shirinyan et al 2006), further studies to clarify the interactions between descending inputs and the local regulation of LG habituation within the terminal abdominal ganglion will provide the neurophysiological basis for the long-term memory of habituation.…”

“…b component of the EPSP is not affected significantly since responses of sensory interneurons to sensory stimulation also increase during bath application of octopamine. Thus, effect of octopamine is mediated by an increase in the level of IP 3 (Araki and Nagayama 2012). The second messenger, cAMP system, is linked to the serotonin-induced synaptic enhancement of the LG response, while IP 3 system is linked to the octopamine-induced synaptic enhancement of LG.…”

“…These findings suggest that the increment in the number of stimuli required to habituate the LG response to sensory stimulation is possibly linked to serotonin and octopamine levels of dominant and subordinate crayfish. Serotonin and octopamine enhance the LG responsiveness to sensory stimulation Araki and Nagayama 2012).…”