Synergy between Electrical Coupling and Membrane Properties Promotes Strong Synchronization of Neurons of the Mesencephalic Trigeminal Nucleus

Abstract

Electrical synapses are known to form networks of extensively coupled neurons in various regions of the mammalian brain. The mesencephalic trigeminal (MesV) nucleus, formed by the somata of primary afferents originating in jaw-closing muscles, constitutes one of the first examples supporting the presence of electrical synapses in the mammalian CNS, however, the properties, functional organization and developmental emergence of electrical coupling within this structure remain unknown. By combining electrophysiological, tracer coupling and immunochemical analysis in brain slices of rat and mouse, we found that coupling is mostly restricted to pairs or small clusters of MesV neurons. Electrical transmission is supported by connexin36 (Cx36)-containing gap junctions at somato-somatic contacts where only a small proportion of channels appear to be open (~0.1%). In marked contrast with most brain structures, coupling among MesV neurons increases with age, such that it is absent during early development and appears at postnatal day 8. Interestingly, the development of coupling parallels the development of intrinsic membrane properties responsible for repetitive firing in these neurons. We found that, acting together, sodium and potassium conductances enhance the transfer of signals with high frequency content via electrical synapses, leading to strong spiking synchronization of the coupled neurons. Taken together, our data indicate that coupling in the MesV nucleus is restricted to mostly pairs of somata between which electrical transmission is supported by a surprisingly small fraction of the channels estimated to be present, and that coupling synergically interacts with specific membrane conductances to promote synchronization of these neurons.

Do gap junctions regulate synchrony in the Parkinsonian basal ganglia?

“…Fukuda et al [2006] mention that about 2-5% of Cx36 spots in the visual cortex indicate functional gap junctions. This is in rough accordance with the estimations of Curti et al [2012] that only about 0.1% of gap junction channels are functional and in the open configuration, under the assumption that each Cx36 spot includes tens to hundreds of gap junction channels Zukin, 2004, Bukauskas et al, 2000]. Supposing that this ratio is similar for GPe, i.e.…”

“…Firstly, detection of Cx36 on cell membranes does not directly imply gap junction coupling, but can also indicate hemi-channels or non-functional gap junctions. Fukuda et al [2006] mentioned that 2-5% of Cx36 spots indicate functional gap junctions in the open configuration, whereas Curti et al [2012] estimate about 0.1% of Cx36 spots to be open, functional gap junctions. In pathological states such as PD, the average function of the gap junctions may change.…”

Pacifier Use May Decrease the Risk of SIDS

“…Me5 cells have gap junctions that form somato-somatic synapses among small groups of neurons [16,17]. Each neuron is almost entirely covered with processes that radiate from two or more astrocytes (usually astrocytes cover more neurons) [17].…”

Electrophysiological Features of Neurons in the Mesencephalic Trigeminal Nuclei

“…However, this direct approach for the detailed analyses of the features of these electrical contacts has not been further pursued until recently. Curti et al [95] found that electrical coupling is restricted to small clusters of Mes V neurons. They also indicated that connexin-36-containing gap junctions mediated electrical transmission between Mes V neurons [96].…”