Synchronization of excitable cells coupled by reciprocal inhibition is a topic of significant interest due to the important
role that inhibitory synaptic interaction plays in the generation and regulation of coherent rhythmic activity in a variety
of neural systems. While recent work revealed the synchronizing influence of inhibitory coupling on the dynamics of many networks,
it is known that strong coupling can destabilize phase-locked firing. Here we examine the loss of synchrony caused by an increase
in inhibitory coupling in networks of type-I Morris–Lecar model oscillators, which is characterized by a period-doubling cascade
and leads to mode-locked states with alternation in the firing order of the two cells, as reported recently by Maran and Canavier
(J Comput Nerosci,
2008) for a network of Wang-Buzsáki model neurons. Although alternating-order firing has been previously reported as a near-synchronous
state, we show that the stable phase difference between the spikes of the two Morris–Lecar cells can constitute as much as
70% of the unperturbed oscillation period. Further, we examine the generality of this phenomenon for a class of type-I oscillators
that are close to their excitation thresholds, and provide an intuitive geometric description of such “leap-frog” dynamics.
In the Morris–Lecar model network, the alternation in the firing order arises under the condition of fast closing of K
+ channels at hyperpolarized potentials, which leads to slow dynamics of membrane potential upon synaptic inhibition, allowing
the presynaptic cell to advance past the postsynaptic cell in each cycle of the oscillation. Further, we show that non-zero
synaptic decay time is crucial for the existence of leap-frog firing in networks of phase oscillators. However, we demonstrate
that leap-frog spiking can also be obtained in
pulse-coupled inhibitory networks of one-dimensional oscillators with a multi-branched phase domain, for instance in a network of quadratic
integrate-and-fire model cells. Finally, for the case of a homogeneous network, we establish quantitative conditions on the
phase resetting properties of each cell necessary for stable alternating-order spiking, complementing the analysis of Goel
and Ermentrout (Physica D 163:191–216,
2002) of the order-preserving phase transition map.
Keywords Synchronization - Non-weak coupling - Non-synchronous dynamics - Inhibitory network - Type-I excitability - Synaptic inhibition - Leader switching - Spike-time response - Phase resetting
Action Editor: Frances K. Skinner