Mechanisms of Flexible Information Sharing through Noisy Oscillations

Simple Summary To properly interact with our environment, the brain must be able to identify external stimuli, process them, and make the right decisions all in a short time. This may involve several brain regions interacting together by sharing information birectionally via rhythmic activity. Such flexibility requires the functional connectivity between the areas to be dynamic, and a key question is the relevant parameter and operating regimes that make this possible in spite of fixed structural connectivity. Working towards this goal, we consider two coupled brain regions, each of which exhibits a noisy rhythm, a commonly observed type of neural activity. Such rhythms can be induced by the stochasticity in the neural circuitry, or be autonomously generated through nonlinearities and not necessitating noise. For these two types of rhythms, we computed the amount of information shared between the brain areas and the preferred direction(s) of sharing. We found that without the coupling delay, the flexibility needed by the brain to perform cognitive tasks requires the rhythms to be autogenerated rather than noise-induced. This is the case even with asymmetry or heterogeneity. This suggests that the importance of the dynamical regime has to be taken into account when modeling interacting neural rhythms from an information theoretical point of view. Brain areas must be able to interact and share information in a time-varying, dynamic manner on a fast timescale. Such flexibility in information sharing has been linked to the synchronization of rhythm phases between areas. One definition of flexibility is the number of local maxima in the delayed mutual information curve between two connected areas. However, the precise relationship between phase synchronization and information sharing is not clear, nor is the flexibility in the face of the fixed structural connectivity and noise. Here, we consider two coupled oscillatory excitatory-inhibitory networks connected through zero-delay excitatory connections, each of which mimics a rhythmic brain area. We numerically compute phase-locking and delayed mutual information between the phases of excitatory local field potential (LFPs) of the two networks, which measures the shared information and its direction. The flexibility in information sharing is shown to depend on the dynamical origin of oscillations, and its properties in different regimes are found to persist in the presence of asymmetry in the connectivity as well as system heterogeneity. For coupled noise-induced rhythms (quasi-cycles), phase synchronization is robust even in the presence of asymmetry and heterogeneity. However, they do not show flexibility, in contrast to noise-perturbed rhythms (noisy limit cycles), which are shown here to exhibit two local information maxima, i.e., flexibility. For quasi-cycles, phase difference and information measures for the envelope-phase dynamics obtained from previous analytical work using the Stochastic Averaging Method (SAM) are found to be in good qualitative agreement with those obtained from the original dynamics. The relation between phase synchronization and communication patterns is not trivial, particularly in the noisy limit cycle regime. There, complex patterns of information sharing can be observed for a single value of the phase difference. The mechanisms reported here can be extended to I-I networks since their phase synchronizations are similar. Our results set the stage for investigating information sharing between several connected noisy rhythms in neural and other complex biological networks.

Automated summary

To properly interact with the environment, the brain must rapidly identify, process external stimuli, and make the right decisions, involving multiple brain regions sharing information through rhythmic activities. The flexibility in information sharing requires dynamic functional connectivity, even in the presence of fixed structural connectivity. The relationship between phase synchronization and information sharing is unclear, and the flexibility of information sharing depends on the dynamic origin of oscillations.