Journal club: Gap junctions compensate for sublinear dendritic integration in an inhibitory network

Koen Vervaeke, Andrea Lőrincz, Zoltan Nusser, R. Angus Silver

Science 30 Mar 2012:

Vol. 335, Issue 6076, pp. 1624-1628

DOI: 10.1126/science.1215101

This paper describe how dendrites of cerebellar Golgi cells enhance synaptic signals by sharing them with neighboring Golgi cells via gap junctions rather than boosting them by generating action potentials.

Golgi cells are the inhibitory interneurons in the granular layer of the cerebellar cortex. They receive excitatory input from mossy fibres and parallel fibers.  In this study, the authors studied how the excitatory synaptic inputs onto Golgi cells are integrated by the dendrites and by electrical connections to other Golgi cells. Forming the gap junctions with neighboring cells counteracts with the dendritic attenuation due to membrane conductance.

The author first examined the efficiency of passive dendritic conduction of a local synaptic potential evoked by two-photon uncaging of glutamate. They found that the dendrite of Golgi cell is quite passive. Substantial attenuation of the electrotonic signals when occurred at many places at once.  This weakens the impact of distal excitatory inputs. 

 

However, the high density of dendritic gap junctions enables the synaptic potentials spread to the dendrites of neighboring GoCs. This gap junction-mediated lateral excitation counteracts the effects of sublinear dendritic behavior. Thus, electrical connections among GoCs counteract the dendritic attenuation without the need to boost electrically remote synaptic input with active dendritic conductances.  The combination of passive dendrites and dendritic gap junctions facilitates the excitatory synaptic signals by involving a larger number of interneurons to respond to localized patches of synaptic excitation.

The results also revealed how gap junctions on inhibitory interneuron dendrites could contribute to spatial averaging, which has been proposed in the retina, excitatory olfactory neurons in insects, and to the broad tuning of inhibitory interneurons in cortex.  These mechanisms are also likely to contribute to gain control in the granule cell layer through parallel-fiber mediated feedback.  The interneurons do not operate as fully independent neuronal units but share charge during chemical synaptic excitation and thus exhibit features of a syncitium.