In Situ Characterization of a Rectifying Electrical Junction

Abstract

. Electrical synapses play significant roles in neural processing in invertebrate and vertebrate nervous systems. The view of electrical synapses as plain bidirectional intercellular channels represents a partial picture because rectifying electrical synapses expand the complexity in the communication capabilities of neurons. Rectification derives, mostly, from the sensitivity of electrical junctions to the transjunctional potential (V j ) across the coupled cells. We analyzed the characteristics of this sensitivity and their effect on neuronal signaling, studying rectifying junctions present in the leech nervous system. The NS neurons, a pair of premotor nonspiking neurons present in each midbody ganglion, are electrically coupled to virtually every excitatory motor neuron. Studied at rest, only hyperpolarizing signals can be transmitted from NS to the motoneurons, and only depolarizing signals are conducted in the opposite direction. Our results show that small changes in the NS membrane potential (V m ) exerted an effective control of the firing frequency of the CV motoneurons (excitor of circular muscles). This effect revealed the existence of a threshold V j across which the electrical synapse shifts from a nonconducting to a conducting state. The junction can operate as a relatively symmetrical bidirectional bridge provided that the transmitted signals do not cross this threshold transjunctional potential. I N T R O D U C T I O NElectrical synapses have been shown to play significant roles in neural processing in the central nervous systems of invertebrate and vertebrate adults (Auerbach and Bennett 1969;Edwards et al. 1999;Furshpan and Potter 1959;Galarreta and Hestrin 2001;Llinás et al. 1974;Nicholls and Purves 1970;Veruki and Hartveit 2002). The electrical properties of gap junctions, the intercellular channels underlying this form of cellular communication (Kumar and Gilula 1996), determine the characteristics of signal transmission. The common view of electrical synapses as plain bidirectional channels between cells represents only a partial picture of their communication capabilities (Bennett 1997;Hormuzdi et al. 2004;Rela and Szczupak 2004). Interestingly, the initial descriptions of electrical coupling in the nervous system were made on rectifying junctions in the giant synapse in the crayfish (Furshpan and Potter 1959) and in the hatchet fish (Auerbach and Bennett 1969) where the junctions allow the transmission of excitatory signals from premotor interneurons to the motoneurons and inhibitory signals in the opposite direction.The conductance of gap junctions displays two types of voltage sensitivities: most of them are sensitive to the transjunctional potential (V j , the difference in potential across the gap) (Barrio et al. 1991;Jaslove and Brink 1986;Spray et al. 1979;Oh et al. 1999;Verselis et al. 1994), but they can also be sensitive to the transmembrane potential (V m ) of either cell (Obaid et al. 1983;Revilla et al., 2000;Verselis et al. 1991). Sensitivity to V j can be symmetrical when...

Diversity of the Photoreceptors and Spectral Opponency in the Compound Eye of the Golden Birdwing, Troides aeacus formosanus

“…If the gap junctions have rectifying properties [39], then they could also contribute to producing negative responses in neighboring photoreceptors under certain circumstances.…”

Connexin-Dependent Neuroglial Networking as a New Therapeutic Target

“…As presented above and at least in specific brain areas, there is an overlap between neuronal circuitry and astroglial networking (Rela and Szczupak, 2007; Houades et al, 2008; Roux et al, 2011) or with the panglial networking (Claus et al, 2016). Such functional intersection can be correlated to the function of local astrocyte networks in complex cerebral functions, such as sleep-wake cycle regulation, and dysfunction (Franco-Perez et al, 2012), cognition (Dallerac and Rouach, 2016), behavior (Pannasch and Rouach, 2013), or sensory functions (Han et al, 2014).…”

“…This was reported in the hippocampus by performing dye coupling experiments in the eGFP-hGFAP mouse where it was observed that, in the coupling area defined by the intercellular spread of sulforhodamine B, several eGFP-positive astrocytes were excluded (Houades et al, 2006). Also in the olfactory bulb, olfactory ensheathing cells are reported to be preferentially coupled to a subset of their neighbors forming subdomains with the potential to affect specific axon fascicles (Rela and Szczupak, 2007). These observations suggest that astroglial networks, in addition to being plastic, do not involve all astrocytes of a considered location.…”

Gap junction proteins and the wiring (Rewiring) of neuronal circuits

“…Most of the 400 neurons (Macagno, 1980) that comprise the segmental ganglia in the CNS of the medicinal leech (two closely related species of the genus Hirudo, H. verbana, and H. medicinalis) are known to make select electrical synapses with certain cells while excluding others (Fig. 1;Baylor and Nicholls, 1969;Elliott and Muller, 1983;Marin-Burgin et al, 2005;Rela and Szczupak, 2007). Fifteen of the 21 innexin genes in the leech genome are expressed Figure 1 The leech ganglion contains a large variety of electrical neuronal circuits, ranging from as few as 2 or 3 cells to many 10s of neurons.…”