Analysis of temperature-dependent abnormal bursting patterns of neurons in Aplysia.

Temperature affects the firing pattern and electrical activity of neurons in animals, eliciting diverse responses depending on neuronal cell type. However, the mechanisms underlying such diverse responses are not well understood. In the present study, we performed in vitro recording of abdominal ganglia cells of Aplysia juliana, and analyzed their burst firing patterns. We identified atypical bursting patterns dependent on temperature that were totally different from classical bursting patterns observed in R15 neurons of A. juliana. We classified these abnormal bursting patterns into type 1 and type 2; type 1 abnormal single bursts are composed of two kinds of spikes with a long interspike interval (ISI) followed by short ISI regular firing, while type 2 abnormal single bursts are composed of complex multiplets. To investigate the mechanism underlying the temperature dependence of abnormal bursting, we employed simulations using a modified Plant model and determined that the temperature dependence of type 2 abnormal bursting is related to temperaturedependent scaling factors and activation or inactivation of potassium or sodium channels.

Temperature-dependent bursting pattern analysis by modified Plant model.

Many electrophysiological properties of neuron including firing rates and rhythmical oscillation change in response to a temperature variation, but the mechanism underlying these correlations remains unverified. In this study, we analyzed various action potential (AP) parameters of bursting pacemaker neurons in the abdominal ganglion of Aplysia juliana to examine whether or not bursting patterns are altered in response to temperature change. Here we found that the inter-burst interval, burst duration, and number of spike during burst decreased as temperature increased. On the other hand, the numbers of bursts per minute and numbers of spikes per minute increased and then decreased, but interspike interval during burst firstly decreased and then increased. We also tested the reproducibility of temperature-dependent changes in bursting patterns and AP parameters. Finally we performed computational simulations of these phenomena by using a modified Plant model composed of equations with temperature-dependent scaling factors to mathematically clarify the temperature-dependent changes of bursting patterns in burst-firing neurons. Taken together, we found that the modified Plant model could trace the ionic mechanism underlying the temperature-dependent change in bursting pattern from experiments with bursting pacemaker neurons in the abdominal ganglia of Aplysia juliana.

Temperature dependence of action potential parameters in Aplysia neurons.

Although the effects of temperature changes on the activity of neurons have been studied in Aplysia, the reproducibility of the temperature dependence of the action potential (AP) parameters has not been verified. To this end, we performed experiments using Aplysia neurons. Fourteen AP parameters were analyzed using the long-term data series recorded during the experiments. Our analysis showed that nine of the AP parameters decreased as the temperature increased: the AP amplitude (A(AP)), membrane potential at the positive peak (V(pp)), interspike interval, first half (Δt(r1)) and last half (Δt(r2)) of the temperature rising phase, first half (Δt(f1)) and last half (Δt(f2)) of the temperature falling phase, AP (Δt(AP, 1/2)), and differentiated signal (Δt(DS, 1/2)) half-width durations. Five of the AP parameters increased with temperature: the differentiated signal amplitude (A(DS)), absolute value of the membrane potential at negative peak (|V(np)|), absolute value of the maximum slope of the AP during the temperature rising (|-MSR|) and falling (|MSF|) phases, and spiking frequency (Frequency). This work could provide the basis for a better understanding of the elementary processes underlying the temperature-dependent neuronal activity in Aplysia.

A Computational Model of the Temperature-dependent Changes in Firing Patterns in Aplysia Neurons.

We performed experiments using Aplysia neurons to identify the mechanism underlying the changes in the firing patterns in response to temperature changes. When the temperature was gradually increased from 11℃ to 31℃ the firing patterns changed sequentially from the silent state to beating, doublets, beating-chaos, bursting-chaos, square-wave bursting, and bursting-oscillation patterns. When the temperature was decreased over the same temperature range, these sequential changes in the firing patterns reappeared in reverse order. To simulate this entire range of spiking patterns we modified nonlinear differential equations that Chay and Lee made using temperature-dependent scaling factors. To refine the equations, we also analyzed the spike pattern changes in the presence of potassium channel blockers. Based on the solutions of these equations and potassium channel blocker experiments, we found that, as temperature increases, the maximum value of the potassium channel relaxation time constant, τ(n)(t) increases, but the maximum value of the probabilities of openings for activation of the potassium channels, n(t) decreases. Accordingly, the voltage-dependent potassium current is likely to play a leading role in the temperature-dependent changes in the firing patterns in Aplysia neurons.