Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons

Exploring the organization and function of local inhibitory networks is an essential step on the way to understand the principles of brain operation. We show here that molecular layer inhibitory interneurons of the guinea pig cerebellar cortex are organized as local networks, generating synchronous activity. Simultaneous recording from two adjacent interneurons revealed a direct current flow between synchronized pairs of neurons. Blocking inhibitory or excitatory synaptic transmission did not alter the synchronization. The electrotonic coupling coefficient (average 0.1) depended mainly on the input resistance of the postsynaptic cell, indicating a homogenous coupling resistance between different pairs. A presynaptic action potential generated a short, attenuated spikelet in the postsynaptic cell. The passive current flow was amplified by voltage-dependent intrinsic currents to create a reciprocal interplay between the presynaptic and postsynaptic cells. This interplay results in a time window for synchronization that is wider than expected from the duration of the spikelet. Intracellular staining with biocytin revealed high incidence of dye coupling. Furthermore, the interneurons located superficially in the molecular layer tend to form larger networks compared with the inter interneurons. We propose that weakly coupled inhibitory networks can generate loosely synchronous activity, which results from the interaction of electrical coupling and intrinsic currents.