scholarly journals Antidromic-rectifying gap junctions amplify chemical transmission at functionally mixed electrical-chemical synapses

2017 ◽  
Vol 8 (1) ◽  
Author(s):  
Ping Liu ◽  
Bojun Chen ◽  
Roger Mailler ◽  
Zhao-Wen Wang
2020 ◽  
Author(s):  
Abagael M. Lasseigne ◽  
Fabio A. Echeverry ◽  
Sundas Ijaz ◽  
Jennifer Carlisle Michel ◽  
E. Anne Martin ◽  
...  

SUMMARYElectrical synaptic transmission relies on neuronal gap junctions containing channels constructed by Connexins. While at chemical synapses neurotransmitter-gated ion channels are critically supported by scaffolding proteins, it is unknown if channels at electrical synapses require similar scaffold support. Here we investigated the functional relationship between neuronal Connexins and Zonula Occludens 1 (ZO1), an intracellular scaffolding protein localized to electrical synapses. Using model electrical synapses in zebrafish Mauthner cells, we demonstrated that ZO1 is required for robust synaptic Connexin localization, but Connexins are dispensable for ZO1 localization. Disrupting this hierarchical ZO1/Connexin relationship abolishes electrical transmission and disrupts Mauthner-cell-initiated escape responses. We found that ZO1 is asymmetrically localized exclusively postsynaptically at neuronal contacts where it functions to assemble intercellular channels. Thus, forming functional neuronal gap junctions requires a postsynaptic scaffolding protein. The critical function of a scaffolding molecule reveals an unanticipated complexity of molecular and functional organization at electrical synapses.


1985 ◽  
Vol 54 (2) ◽  
pp. 304-317 ◽  
Author(s):  
H. Kolb ◽  
J. Jones

Red and green cones of two turtle species (Pseudemys scripta elegans and Chelydra serpentina) retina have been stained with Golgi procedures and examined by light microscopy of whole-mount tissue and by electron microscopy of serial thin sections. By light microscopy, red and green single cones appear indistinguishable, but double cones can be readily identified. All Golgi-stained photoreceptors in turtle retina have a spray of telodendria radiating from their synaptic pedicles. The telodendria of single cones are 10-20 micron long and end in clusters of terminals, whereas double cones have 30- to 50-micron long telodendria in addition to a very short bush of telodendria arising from one side of the pedicle. Electron microscopy of the Golgi-stained cones allows them to be distinguished into red or green spectral types by the appearance of their oil droplets. Furthermore, the spectral identity of cones contacted by the telodendria of identified Golgi-stained cones can similarly be determined. Red single cones make telodendrial contacts with other red singles, both members of the double cones, and with green single cones. Green single cones likewise connect to many surrounding red cones, both single and double types, and a few other green singles. Both members of the double cone connect to neighboring red and green singles and occasionally to double cones. The telodendria of stained cones end on spectrally homologous or heterologous cone types at basal junctions, central elements of ribbon synapses or, sometimes, as lateral elements of ribbon synapses. However, all these synaptic contacts appear to be of the same type, i.e., narrow-cleft basal junctions. Small gap junctions occur between neighboring cone pedicles, regardless of spectral type, in the visual streak area of the retina. Large gap junctions occur between unidentified cone telodendria in the neuropil of the outer plexiform layer. The telodendrial connections between red and green cones in the turtle retina have the appearance of chemical synapses and suggest an anatomical pathway responsible for the mixing of red and green signals in red or green cones of the turtle retina as reported in the accompanying physiological paper by Normann, Perlman, and Daly (27).


2008 ◽  
Vol 68 (3) ◽  
pp. 281-294 ◽  
Author(s):  
Hyun-Woo Oh ◽  
Jorge M. Campusano ◽  
Lutz G.W. Hilgenberg ◽  
Xicui Sun ◽  
Martin A. Smith ◽  
...  

Nature ◽  
1978 ◽  
Vol 273 (5661) ◽  
pp. 410-410
Author(s):  
Anne Warner

1989 ◽  
Vol 236 (1284) ◽  
pp. 253-268 ◽  

Experiments have been made to follow the development of chemical and electrical transmission between pairs of leech neurons in culture. 1. The cell bodies of identified neurons were isolated from the CNS by suction after mild enzyme treatment, together with a length of the initial segment (or ‘stump’). The neurons tested were Retzius cells (R), annulus erector motoneurons (AE), Anterior pagoda cells (AP) and pressure sensory cells (P). Pairs of cells were placed together in various configurations, with different sites on their surfaces making contact. 2. When pairs of Retzius cells were apposed with their stumps touching, serotonergic, chemically mediated synaptic transmission became apparent before electrical transmission. By 2.5 h impulses in either of the two Retzius cells produced hyperpolarizing inhibitory potentials in the other. These potentials were reversed by raised intracellular CI and showed clear facilitation. The strength of chemical transmission between Retzius cells increased over the next 72 h. 3. After chemical transmission had been established, weak non-recti­fying electrical transmission became apparent between Retzius cells at about 24–72 h. By 4 days coupling became stronger and tended to obscure chemically evoked synaptic potentials. 4. When pairs of Retzius cells were aligned in culture with the tip of one cell stump touching the soma of the other, chemical transmission also developed rapidly. Transmission was, however, in one direction, from stump to soma. At later stages non-rectifying electrical coupling devel­oped as with stump-stump configuration. With the cell bodies of two Retzius cells apposed, electrical coupling developed after several days, before chemical transmission could be observed. 5. When Retzius and P cells were cultured with their stumps in con­tact, inhibitory chemical synaptic transmission developed within 24 h. Transmission was always in one direction, from Retzius to P cell. Electrical coupling of Retzius and P cells never occurred whatever the spatial relations of the cells to one another. 6. Annulus erector motoneurons, which contain ACh and a peptide resembling FMRFamide, first developed electrical coupling when the two stumps were in contact and then, later, bi-directional chemical transmission. Anterior Pagoda pairs placed stump-to-stump showed electrical connections. 7. Electronmicrographs revealed the presence of synaptic structures within24 h after Retzius-Retzius, Retzius-P or AE–AE stumps were apposed. 8. The specificity of connections between cultured cells was similar to that observed in earlier experiments. A marked difference was in the speed and reliability with which chemical synapses developed when stumps were in contact. The results show that the tip of a neuron represents a preferential site for the formation of chemical synapses.


1999 ◽  
Vol 22 (5) ◽  
pp. 838-839 ◽  
Author(s):  
Stuart Hameroff

As presently implemented, the neuron doctrine (ND) portrays the brain's neurons and chemical synapses as fundamental components in a computer-like switching circuit, supporting a view of brain = mind = computer. However, close examination reveals individual neurons to be far more complex than simple switches, with enormous capacity for intracellular information processing (e.g., in the internal cytoskeleton). Other poorly appreciated factors (gap junctions, apparent randomness, dendritic-dendritic processing, possible quantum computation, the living state) also suggest that the ND grossly oversimplifies neuronal functions. In the quest to understand consciousness, the presently implemented ND may throw out the baby with the bath water.


2014 ◽  
Vol 112 (9) ◽  
pp. 2102-2113 ◽  
Author(s):  
Cong Yao ◽  
Kimberly G. Vanderpool ◽  
Matthew Delfiner ◽  
Vanessa Eddy ◽  
Alexander G. Lucaci ◽  
...  

In contrast to the knowledge of chemical synapses, little is known regarding the properties of gap junction-mediated electrical synapses in developing zebrafish, which provide a valuable model to study neural function at the systems level. Identifiable “mixed” (electrical and chemical) auditory synaptic contacts known as “club endings” on Mauthner cells (2 large reticulospinal neurons involved in tail-flip escape responses) allow exploration of electrical transmission in fish. Here, we show that paralleling the development of auditory responses, electrical synapses at these contacts become anatomically identifiable at day 3 postfertilization, reaching a number of ∼6 between days 4 and 9. Furthermore, each terminal contains ∼18 gap junctions, representing between 2,000 and 3,000 connexon channels formed by the teleost homologs of mammalian connexin 36. Electrophysiological recordings revealed that gap junctions at each of these contacts are functional and that synaptic transmission has properties that are comparable with those of adult fish. Thus a surprisingly small number of mixed synapses are responsible for the acquisition of auditory responses by the Mauthner cells, and these are likely sufficient to support escape behaviors at early developmental stages.


2018 ◽  
Author(s):  
Sami H. Jezzini ◽  
Amelia Merced ◽  
Jonathan M. Blagburn

AbstractThe synapse between auditory Johnston’s Organ neurons (JONs) and the giant fiber (GF) of Drosophila is structurally mixed, being composed of cholinergic chemical synapses and Neurobiotin-(NB) permeable gap junctions, which consist of the innexin Shaking-B (ShakB). Misexpression of one ShakB isoform, ShakB(N+16), in a subset of JONs that do not normally form gap junctions, results in their de novo dye coupling to the GF. This is similar to the effect of misexpression of the transcription factor Engrailed (En) in these same neurons, which also causes the formation of additional chemical synapses. In order to test the hypothesis that ShakB misexpression would similarly affect the distribution of chemical synapses, fluorescently-labeled presynaptic active zone protein (Brp) was expressed in JONs and the changes in its distribution were assayed with confocal microscopy. Both ShakB(N+16) and En increased the dye-coupling of JONs with the GF, indicating the formation of ectopic gap junctions. Conversely, expression of the ‘incorrect’ isoform, ShakB(N) abolishes dye coupling. However, while En misexpression increased the chemical contacts with the GF and the amount of GF medial branching, ShakB misexpression did not. ShakB immunocytochemistry showed that misexpression of ShakB(N+16) increases gap junctional plaques in JON axons but ShakB(N) does not. We conclude that both subsets of JON form chemical synapses onto the GF dendrites but only one population forms gap junctions, comprised of ShakB(N+16). Misexpression of this isoform in all JONs does not result in the formation of new mixed synapses but in the insertion of gap junctions, presumably at the sites of existing chemical synaptic contacts with the GF.


2020 ◽  
Author(s):  
Jennifer Crodelle ◽  
David W. McLaughlin

AbstractRecent experiments in the developing mammalian visual cortex have revealed that gap junctions couple excitatory cells and potentially influence the formation of chemical synapses. Though gap junctions between inhibitory cells are ubiquitous in the adult cortex, and their presence has been shown to promote synchronous network firing, their function among excitatory, pyramidal cells remains poorly understood. During development, pyramidal cells that were derived from the same progenitor cell, called sister cells, are preferentially connected by a gap junction during the first postnatal week, while chemical synapses are still being formed. Additionally, these sister cells tend to share an orientation preference and a chemical synapse in the adult cortex, a property that is diminished when gap junctions are blocked. In this work, we construct an idealized model of the mouse visual cortex during the first two postnatal weeks of development to analyze the response properties of gap-junction-coupled cells and their effect on synaptic plasticity. Further, as an application of this model, we investigate the interplay of gap-junction coupling and synaptic plasticity on the order, or organization, of the resulting cortical map of orientation preference.Author summaryGap junctions, or sites of direct electrical connections between neurons, have a significant presence in the cortex, both during development and in adulthood. Their primary function during either of these periods, however, is still poorly understood. In the adult cortex, gap junctions between local, inhibitory neurons have been shown to promote synchronous firing, a network characteristic thought to be important for learning, attention, and memory. During development, gap junctions between excitatory, pyramidal cells, have been conjectured to play a role in synaptic plasticity and the formation of cortical circuits. In the visual cortex, where neurons exhibit tuned responses to properties of visual input such as orientation and direction, recent experiments show that excitatory cells are coupled by gap junctions during the first postnatal week and are replaced by chemical synapses during the second week. In this work, we explore the possible contribution of gap-junction coupling during development to the formation of chemical synapses both into the visual cortex from the thalamus and within the visual cortex between cortical cells. Specifically, within a mathematical model of the visual cortex during development, we identify the response properties of gap-junction-coupled cells and their influence on the formation of the cortical map of orientation preference.


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