Altered heat nociception in cockroach Periplaneta americana L. exposed to capsaicin

Abstract

Some natural alkaloids, e.g. capsaicin and camphor, are known to induce a desensitization state, causing insensitivity to pain or noxious temperatures in mammals by acting on TRP receptors. Our research, for the first time, demonstrated that a phenomenon of pharmacological blockade of heat sensitivity may operate in American cockroach, Periplaneta americana (L.). We studied the escape reaction time from 50°C for American cockroaches exposed to multiple doses of different drugs affecting thermo-TRP. Capsaicin, capsazepine, and camphor induced significant changes in time spent at noxious ambient temperatures. Moreover, we showed that behavioral thermoregulation in normal temperature ranges (10–40°C) is altered in treated cockroaches, which displayed a preference for warmer regions compared to non-treated insects. We also measured the levels of malondialdehyde (MDA) and catalase activity to exclude the secondary effects of the drugs on these processes. Our results demonstrated that increase in time spent at 50°C (five versus one trial at a heat plate) induced oxidative stress, but only in control and vehicle-treated groups. In capsaicin, capsazepine, menthol, camphor and AITC-treated cockroaches the number of exposures to heat had no effect on the levels of MDA. Additionally, none of the tested compounds affected catalase activity. Our results demonstrate suppression of the heat sensitivity by repeated capsazepine, camphor and capsaicin administration in the American cockroach.

Effect of Capsaicin and Other Thermo-TRP Agonists on Thermoregulatory Processes in the American Cockroach

“…Camphor was also shown to inhibit the heat-induced activation of Painless receptor in Drosophila [24]. We previously demonstrated that repeated treatment with camphor increases the latency to escape from noxious heat in the American cockroach [7]. Results obtained in the present study correspond well with these data—Insects after camphor treatment found the optimal environment for the control insects as too cold and chose higher temperatures.…”

“…Based on the obtained results and our previous experiments [5,7], we suggest that in the American cockroach:…”

“…Some reports have shown the effect of capsaicin on thermoregulatory processes in invertebrates such as an induced preference for lower temperatures in Periplaneta americana [5] or Leptinotarsa decemlineata [6]. Moreover, exposure to this alkaloid has been reported to change the responsiveness to noxious heat in the American cockroach [7] and in land snail Megalobulimus abbreviatus [8]. Nocifensive behavioral responses after capsaicin application have also been observed in the medicinal leech [9].…”

“…We studied the effect of various ligands that have been shown to activate (allyl isothiocyanate) or inhibit (camphor) warm receptors, as well as activate (camphor) or inhibit (menthol and thymol) cold receptors in insects. In our previous studies [5,7], we demonstrated changes in thermal preferences in cockroaches exposed to capsaicin and capsazepine; thus, the present study was aimed at determining only the body temperature changes after exposure to these ligands. This let us observe whether tested TRP ligands change physiological thermoregulation.…”

Nociceptive Pathway in the Cockroach Periplaneta americana

“…For example, Drosophila larvae and adults produce a stereotyped defensive behavior in response to noxious mechanical, chemical or thermal stimuli (Tracey et al, 2003; Xu et al, 2006; Fiala, 2008; Neely et al, 2011; Im and Galko, 2012; Honjo et al, 2016; Tokusumi et al, 2017; Hu et al, 2018). This type of behavior is also evoked in cockroaches in response to thermal noxious stimuli (Gritsai et al, 2004; Gritsai et al, 2009; Maliszewska et al, 2018). With this mind, the present paper has examined the nociceptive pathway from sensory reception to motor behavior in the cockroach Periplaneta americana using primarily electrophysiological recordings.…”