M-type potassium conductance controls the emergence of neural phase codes: a combined experimental and neuron modelling study

Rate and phase codes are believed to be important in neural information processing. Hippocampal place cells provide a good example where both coding schemes coexist during spatial information processing. Spike rate increases in the place field, whereas spike phase precesses relative to the ongoing theta oscillation. However, what intrinsic mechanism allows for a single neuron to generate spike output patterns that contain both neural codes is unknown. Using dynamic clamp, we simulate an in vivo-like subthreshold dynamics of place cells to in vitro CA1 pyramidal neurons to establish an in vitro model of spike phase precession. Using this in vitro model, we show that membrane potential oscillation (MPO) dynamics is important in the emergence of spike phase codes: blocking the slowly activating, non-inactivating K⁺ current (I_M), which is known to control subthreshold MPO, disrupts MPO and abolishes spike phase precession. We verify the importance of adaptive I_M in the generation of phase codes using both an adaptive integrate-and-fire and a Hodgkin–Huxley (HH) neuron model. Especially, using the HH model, we further show that it is the perisomatically located I_M with slow activation kinetics that is crucial for the generation of phase codes. These results suggest an important functional role of I_M in single neuron computation, where I_M serves as an intrinsic mechanism allowing for dual rate and phase coding in single neurons.