Adverse Modulation of the Firing Patterns of Cold Receptors by Volatile Anesthetics Affecting Activation of TRPM8 Channels: a Modeling Study

Коrogod, S. М.; Maksymchuk, Natalia; Demianenko, L. E.; Vlasov, O. O.; Cymbalyuk, Gennady

doi:10.1007/s11062-021-09889-2

Cited by 2 publications

(2 citation statements)

References 32 publications

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“…Investigation of activation and inactivation parameters of TRP current enabled us to understand mechanisms of transient and steady cold temperature coding. Considering that TRP channels have Ca 2+ -dependent inactivation (desensitization), which leads to adaptation of cell response ( Nilius et al, 2005 ; Rohacs et al, 2005 ; Gordon-Shaag et al, 2008 ; McKemy, 2013 ; Hasan and Zhang, 2018 ; Korogod et al, 2020 ) and that temporal scale for TRP channel inactivation is of the similar order as a spiking rate adaptation of cold-sensitive neurons ( Latorre et al, 2011 ; Olivares et al, 2015 ), we used in our model TRP current with temperature-dependent activation and Ca 2+ -dependent inactivation. We created a family of CIII models, varying parameters of TRP activation and inactivation and tested them on different temperature protocols that were consistent with those applied to biological neurons.…”

Section: Discussionmentioning

confidence: 99%

Transient and Steady-State Properties of Drosophila Sensory Neurons Coding Noxious Cold Temperature

Maksymchuk

Sakurai

Cox

et al. 2022

Front. Cell. Neurosci.

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Coding noxious cold signals, such as the magnitude and rate of temperature change, play essential roles in the survival of organisms. We combined electrophysiological and computational neuroscience methods to investigate the neural dynamics of Drosophila larva cold-sensing Class III (CIII) neurons. In response to a fast temperature change (–2 to –6°C/s) from room temperature to noxious cold, the CIII neurons exhibited a pronounced peak of a spiking rate with subsequent relaxation to a steady-state spiking. The magnitude of the peak was higher for a higher rate of temperature decrease, while slow temperature decrease (–0.1°C/s) evoked no distinct peak of the spiking rate. The rate of the steady-state spiking depended on the magnitude of the final temperature and was higher at lower temperatures. For each neuron, we characterized this dependence by estimating the temperature of the half activation of the spiking rate by curve fitting neuron’s spiking rate responses to a Boltzmann function. We found that neurons had a temperature of the half activation distributed over a wide temperature range. We also found that CIII neurons responded to decrease rather than increase in temperature. There was a significant difference in spiking activity between fast and slow returns from noxious cold to room temperature: The CIII neurons usually stopped activity abruptly in the case of the fast return and continued spiking for some time in the case of the slow return. We developed a biophysical model of CIII neurons using a generalized description of transient receptor potential (TRP) current kinetics with temperature-dependent activation and Ca2+-dependent inactivation. This model recapitulated the key features of the spiking rate responses found in experiments and suggested mechanisms explaining the transient and steady-state activity of the CIII neurons at different cold temperatures and rates of their decrease and increase. We conclude that CIII neurons encode at least three types of cold sensory information: the rate of temperature decrease by a peak of the firing rate, the magnitude of cold temperature by the rate of steady spiking activity, and direction of temperature change by spiking activity augmentation or suppression corresponding to temperature decrease and increase, respectively.

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Section: Discussionmentioning

confidence: 99%

Transient and Steady-State Properties of Drosophila Sensory Neurons Coding Noxious Cold Temperature

Maksymchuk

Sakurai

Cox

et al. 2022

Front. Cell. Neurosci.

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“…Informed by feature coding in other sensory systems, we investigated temporal characteristics of thermal signals and classified qualitatively distinct events in patterns of CIII responses to cold stimulation. For example, bursting and spiking distinguish types of information in electric stimuli coding in electric fish, Apteronotus leptorhynchus [20], temperature coding in mammalian cold receptors [21][22][23][24], and mechanical stimuli in normal, inflammatory, and neuropathic conditions in mammalian high-threshold mechanoreceptors [25]. The importance of temporal properties of electrical activity (patterns) was shown in studying physiological versus pathological conditions such as mechanical and cold hypersensitivity and inflammatory conditions [25][26][27].…”

Section: Introductionmentioning

confidence: 99%

Cold-Temperature Coding with Bursting and Spiking Based on TRP Channel Dynamics in Drosophila Larva Sensory Neurons

Maksymchuk,

Sakurai,

Cox

et al. 2023

IJMS

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Temperature sensation involves thermosensitive TRP (thermoTRP) and non-TRP channels. Drosophila larval Class III (CIII) neurons serve as the primary cold nociceptors and express a suite of thermoTRP channels implicated in noxious cold sensation. How CIII neurons code temperature remains unclear. We combined computational and electrophysiological methods to address this question. In electrophysiological experiments, we identified two basic cold-evoked patterns of CIII neurons: bursting and spiking. In response to a fast temperature drop to noxious cold, CIII neurons distinctly mark different phases of the stimulus. Bursts frequently occurred along with the fast temperature drop, forming a peak in the spiking rate and likely coding the high rate of the temperature change. Single spikes dominated at a steady temperature and exhibited frequency adaptation following the peak. When temperature decreased slowly to the same value, mainly spiking activity was observed, with bursts occurring sporadically throughout the stimulation. The spike and the burst frequencies positively correlated with the rate of the temperature drop. Using a computational model, we explain the distinction in the occurrence of the two CIII cold-evoked patterns bursting and spiking using the dynamics of a thermoTRP current. A two-parameter activity map (Temperature, constant TRP current conductance) marks parameters that support silent, spiking, and bursting regimes. Projecting on the map the instantaneous TRP conductance, governed by activation and inactivation processes, reflects temperature coding responses as a path across silent, spiking, or bursting domains on the map. The map sheds light on how various parameter sets for TRP kinetics represent various types of cold-evoked responses. Together, our results indicate that bursting detects the high rate of temperature change, whereas tonic spiking could reflect both the rate of change and magnitude of steady cold temperature.

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Adverse Modulation of the Firing Patterns of Cold Receptors by Volatile Anesthetics Affecting Activation of TRPM8 Channels: a Modeling Study

Cited by 2 publications

References 32 publications

Transient and Steady-State Properties of Drosophila Sensory Neurons Coding Noxious Cold Temperature

Transient and Steady-State Properties of Drosophila Sensory Neurons Coding Noxious Cold Temperature

Cold-Temperature Coding with Bursting and Spiking Based on TRP Channel Dynamics in Drosophila Larva Sensory Neurons

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