A first morphological and electrophysiological characterization of Fañanas cells of the mouse cerebellum.

Fañanas cells (FCs) are cerebellar glia of unknown function. First described more than a century ago, they have been almost absent from the scientific literature ever since. Here, we combined whole-cell, patch clamp recordings, near-UV laser photolysis, dye-loading and confocal imaging for a first characterization of FCs in terms of their morphology, electrophysiology and glutamate-evoked currents. We identified FCs of the molecular layer in cerebellar slices by their stubby process and small cell bodies. Despite their more compact shape compared to Bergmann glia (BGs), FCs showed similar membrane resistances and basal currents, suggesting that these passive currents are partly a result of electrical coupling between neighbouring glia. Dye filling and pharmacological experiments confirmed both homo- and heterotypic gap-junction coupling among FCs and BGs. Parallel-fibre stimulation evoked TTX-sensitive slow inward currents in FCs that were partially blocked by NBQX but not APV. Occasionally, we observed superimposed fast (milliseconds) current transients. Near-UV flash photolysis of MNI-caged glutamate revealed rapid desensitization of these AMPA-receptor mediated currents, which fully recovered only for stimulation intervals >500 ms. We mapped the highest current densities in proximal processes. We conclude that FCs respond with fast AMPA currents to local glutamate release and they integrate ambient glutamate rises to a slow inward current. Interestingly, we found FCs to prevail throughout adulthood at stable but different densities among cerebellar lobules, with the highest cell densities in lobules I-II and X. Our results strongly suggest that FCs are not just displaced BGs, and that they may have lobule-specific functions - both locally and at the circuit level, yet to be uncovered. KEY POINTS: Using whole-cell recordings and near-UV laser photolyisis of caged glutamate, we provide a first characterization of cells of Fañanas (FCs) in mouse cerebellar slices. FCs are present from postnatal day 5 onward throughout adulthood and have a lobule- dependent density. Parallel-fibre stimulation generates biphasic, predominantly AMPA-mediated currents in FCs. Currents induced in FCs by parallel fibre stimulation are not NMDA receptor-dependent and are enhanced upon glutamate-transporter block with TBOA. Local near-UV glutamate uncaging indicates that FCs can detect fast glutamatergic inputs on the millisecond-time scale. FCs functionally integrate into the glial syncytium.