Dichotomy between extracellular signatures of active dendritic chemical synapses and gap junctions

Local field potentials (LFPs) are intricate signals embodying the dynamic flow of information within the brain, traditionally linked to chemical synaptic inputs. The role of gap junctional inputs on active dendritic compartments in shaping LFPs remains unclear. A novel approach was devised to record extracellular potentials linked to distinct patterns of gap junctional inputs onto conductance-based models.

The findings revealed that synchronous chemical synaptic inputs elicited a negative deflection in neighboring extracellular electrodes, contrasting with the positive deflection observed with inputs via gap junctions. Notably, extracellular dipoles materialized exclusively in response to chemical synaptic inputs, absent in gap junction-mediated scenarios.

Intriguingly, hyperpolarization-activation cyclic nucleotide-gated channels, which generally facilitate inward currents, induced outward currents triggered by the sudden voltage transition induced by synchronous inputs.

Upon administering rhythmic inputs of varying frequencies through gap junctions, substantial suppression of LFP power at higher frequencies was noted. Furthermore, distinctive frequency-dependent variations in the spike phase associated with LFP were observed, contrasting with the corresponding chemical synaptic inputs. All these discrepancies in LFPs were attributable to the prevailing dominance of synaptic currents versus voltage-driven transmembrane currents associated with chemical synapses and gap junctions, respectively.

These observations shed light on the previously uncharted role of active dendritic gap junctions in sculpting extracellular potentials.