Robust switches in thalamic network activity require a timescale separation between sodium and T-type calcium channel activations

Switches in brain states, synaptic plasticity and neuromodulation are fundamental processes in our brain that take place concomitantly across several spatial and timescales. All these processes target neuron intrinsic properties and connectivity to achieve specific physiological goals, raising the question of how they can operate without interfering with each other. Here, we highlight the central importance of a timescale separation in the activation of sodium and T-type calcium channels to sustain robust switches in brain states in thalamic neurons that are compatible with synaptic plasticity and neuromodulation. We quantify the role of this timescale separation by comparing the robustness of rhythms of six published conductance-based models at the cellular, circuit and network levels. We show that robust rhythm generation requires a T-type calcium channel activation whose kinetics are situated between sodium channel activation and T-type calcium channel inactivation in all models despite their quantitative differences. Author summary Our brain is constantly processing information either from the environment to quickly react to incoming events or learning from experience to shape our memory. These brain states translate a collective activity of neurons interconnected via synaptic connections. Here, we focus on the thalamic network showing a transition from an active to an oscillatory mode at the population level, reverberating a switch from tonic to bursting mode at the cellular level. We are questioning how these activity fluctuations can be robustly modeled despite synaptic plasticity affecting the network configuration and the presence of neuromodulators affecting neuron intrinsic properties. To do so, we investigate six conductance-based models and their ability to reproduce activity switches at the cellular, circuit and population levels. We highlight that the robustness requires the timescale separation between the fast activation of sodium channels compared to the slow activation of T-type calcium channels. Our results show that this kinetics difference is not a computational detail but rather makes a model suitable and robust to study the interaction between switches in brain states, synaptic plasticity and neuromodulation.

Automated summary

The time scale separation between the activation of sodium and T-type calcium channels is crucial for robust switches in brain states in thalamic neurons. Conductance-based models show that this difference in kinetics is essential for studying the interaction between switches in brain states, synaptic plasticity, and neuromodulation.