scholarly journals Electrical Transmission among Neurons in the Buccal Ganglion of a Mollusc, Navanax inermis

1970 ◽  
Vol 55 (4) ◽  
pp. 484-496 ◽  
Author(s):  
H. Levitan ◽  
L. Tauc ◽  
J. P. Segundo

The opisthobranch mollusc, Navanax, is carnivorous and cannibalistic. Prey are swallowed whole by way of a sudden expansion of the pharynx. The buccal ganglion which controls this sucking action was isolated and bathed in seawater. Attention was focused upon 10 identifiable cells visible on the ganglion's rostral side. Two cells were observed simultaneously, and each was penetrated with two glass microelectrodes, one for polarizing the membrane and the other for recording membrane potential variations. The coupling coefficients for direct current flow and action potentials of several identified cells were tabulated. Attenuation was essentially independent of the direction of current flow, but depended upon the relative size of the directly and indirectly polarized cells. The attenuation of subthreshold sinusoidally varying voltages increased with frequency above about 1 Hz. The coupling coefficient for spikes was lower than for DC due to greater high frequency attenuation. There is considerable similarity in the spontaneous PSP's of all cells, which is not due to the electrical coupling but to input from a common source. The 10 cells were not chemically interconnected but some were electrically connected to interneurons which fed back chemically mediated PSP's. The feedback can be negative or positive depending upon the membrane potential of the postsynaptic cell. We conclude that electrical coupling among the 10 cells plays a minor role in sudden pharyngeal contractions but that the dual electrical-chemical coupling with interneurons may be important in this respect.

2011 ◽  
Vol 106 (2) ◽  
pp. 680-689 ◽  
Author(s):  
Colin G. Evans ◽  
Bjoern Ch. Ludwar ◽  
Timothy Kang ◽  
Elizabeth C. Cropper

The growing realization that electrical coupling is present in the mammalian brain has sparked renewed interest in determining its functional significance and contrasting it with chemical transmission. One question of interest is whether the two types of transmission can be selectively regulated, e.g., if a cell makes both types of connections can electrical transmission occur in the absence of chemical transmission? We explore this issue in an experimentally advantageous preparation. B21, the neuron we study, is an Aplysia sensory neuron involved in feeding that makes electrical and chemical connections with other identified cells. Previously we demonstrated that chemical synaptic transmission is membrane potential dependent. It occurs when B21 is centrally depolarized prior to and during peripheral activation, but does not occur if B21 is peripherally activated at its resting membrane potential. In this article we study effects of membrane potential on electrical transmission. We demonstrate that maximal potentiation occurs in different voltage ranges for the two types of transmission, with potentiation of electrical transmission occurring at more hyperpolarized potentials (i.e., requiring less central depolarization). Furthermore, we describe a physiologically relevant type of stimulus that induces both spiking and an envelope of depolarization in the somatic region of B21. This depolarization does not induce functional chemical synaptic transmission but is comparable to the depolarization needed to maximally potentiate electrical transmission. In this study we therefore characterize a situation in which electrical and chemical transmission can be selectively controlled by membrane potential.


1979 ◽  
Vol 79 (1) ◽  
pp. 23-40
Author(s):  
A.G. M. BULLOCH ◽  
D. A. DORSETT

Three phases of activity may be recognized in the buccal mass of Tritonia hombergi during the feeding cycle. These have been termed Protraction, Retraction and Flattening. Each phase is driven by a group of motoneurones along the posterior border of the buccal ganglia. The patterned bursting observed in the motoneurone groups during feeding activity is phased by synaptic inputs which are common to two or more groups. Evidence is presented which indicates these inputs are derived from three unidentified multi-action interneurone sources within each buccal ganglion, and whose action primarily determines the patterned output of the motoneurones. Electrical coupling between between synergistic motoneurones and, in one case, post-inhibitory rebound, contribute to the synchronization of group activity. Proprioceptive input to the motoneurones was not identified, but may project to the interneurones. Some small neurones having synaptic inputs on the motoneurones appropriate to two of the interneurones were found, but require confirmation in this role. The cerebral giant cells synapse on representatives of three motoneurone groups, and also activate the buccal interneurones driving the feeding cycle. The patterned activity of the motoneurones can occur in the absence of cerebral cell activity.


2007 ◽  
Vol 98 (6) ◽  
pp. 3796-3801 ◽  
Author(s):  
Kosei Sasaki ◽  
Michael R. Due ◽  
Jian Jing ◽  
Klaudiusz R. Weiss

In the context of motor program generation in Aplysia, we characterize several functional aspects of intraneuronal compartmentalization in an interganglionic interneuron, CBI-5/6. CBI-5/6 was shown previously to have a cerebral compartment (CC) that includes a soma that does not generate full-size action potentials and a buccal compartment (BC) that does. We find that the synaptic connections made by the BC of CBI-5/6 in the buccal ganglion counter the activity of protraction-phase neurons and reinforce the activity of retraction-phase neurons. In buccal motor programs, the BC of CBI-5/6 fires phasically, and its premature activation can phase advance protraction termination and retraction initiation. Thus the BC of CBI-5/6 can act as an element of the central pattern generator (CPG). During protraction, the CC of CBI-5/6 receives direct excitatory inputs from the CPG elements, B34 and B63, and during retraction, it receives antidromically propagating action potentials that originate in the BC of CBI-5/6. Consequently, in its CC, CBI-5/6 receives depolarizing inputs during both protraction and retraction, and these depolarizations can be transmitted via electrical coupling to other neurons. In contrast, in its BC, CBI-5/6 uses spike-dependent synaptic transmission. Thus the CPG directly and differentially controls the program phases in which the two compartments of CBI-5/6 may transmit information to its targets.


2019 ◽  
Vol 122 (1) ◽  
pp. 151-175
Author(s):  
Federico Davoine ◽  
Sebastian Curti

Electrical synapses represent a widespread modality of interneuronal communication in the mammalian brain. These contacts, by lowering the effectiveness of random or temporally uncorrelated inputs, endow circuits of coupled neurons with the ability to selectively respond to simultaneous depolarizations. This mechanism may support coincidence detection, a property involved in sensory perception, organization of motor outputs, and improvement signal-to-noise ratio. While the role of electrical coupling is well established, little is known about the contribution of the cellular excitability and its modulations to the susceptibility of groups of neurons to coincident inputs. Here, we obtained dual whole cell patch-clamp recordings of pairs of mesencephalic trigeminal (MesV) neurons in brainstem slices from rats to evaluate coincidence detection and its determinants. MesV neurons are primary afferents involved in the organization of orofacial behaviors whose cell bodies are electrically coupled mainly in pairs through soma-somatic gap junctions. We found that coincidence detection is highly heterogeneous across the population of coupled neurons. Furthermore, combined electrophysiological and modeling approaches reveal that this heterogeneity arises from the diversity of MesV neuron intrinsic excitability. Consistently, increasing these cells’ excitability by upregulating the hyperpolarization-activated cationic current ( IH) triggered by cGMP results in a dramatic enhancement of the susceptibility of coupled neurons to coincident inputs. In conclusion, the ability of coupled neurons to detect coincident inputs is critically shaped by their intrinsic electrophysiological properties, emphasizing the relevance of neuronal excitability for the many functional operations supported by electrical transmission in mammals. NEW & NOTEWORTHY We show that the susceptibility of pairs of coupled mesencephalic trigeminal (MesV) neurons to coincident inputs is highly heterogenous and depends on the interaction between electrical coupling and neuronal excitability. Additionally, upregulating the hyperpolarization-activated cationic current ( IH) by cGMP results in a dramatic increase of this susceptibility. The IH and electrical synapses have been shown to coexist in many neuronal populations, suggesting that modulation of this conductance could represent a common strategy to regulate circuit operation supported by electrical coupling.


2014 ◽  
Vol 112 (11) ◽  
pp. 2946-2958 ◽  
Author(s):  
Sonal Shruti ◽  
David J. Schulz ◽  
Kawasi M. Lett ◽  
Eve Marder

Gap junctions are intercellular channels that allow for the movement of small molecules and ions between the cytoplasm of adjacent cells and form electrical synapses between neurons. In invertebrates, the gap junction proteins are coded for by the innexin family of genes. The stomatogastric ganglion (STG) in the crab Cancer borealis contains a small number of identified and electrically coupled neurons. We identified Innexin 1 ( Inx1), Innexin 2 (Inx2), Innexin 3 (Inx3), Innexin 4 ( Inx4), Innexin 5 (Inx5), and Innexin 6 ( Inx6) members of the C. borealis innexin family. We also identified six members of the innexin family from the lobster Homarus americanus transcriptome. These innexins show significant sequence similarity to other arthropod innexins. Using in situ hybridization and reverse transcriptase-quantitative PCR (RT-qPCR), we determined that all the cells in the crab STG express multiple innexin genes. Electrophysiological recordings of coupling coefficients between identified pairs of pyloric dilator (PD) cells and PD-lateral posterior gastric (LPG) neurons show that the PD-PD electrical synapse is nonrectifying while the PD-LPG synapse is apparently strongly rectifying.


2012 ◽  
Vol 2012 ◽  
pp. 1-6 ◽  
Author(s):  
Masayuki Yamashita

During the embryonic development of the central nervous system, neuroepithelial cells act as neural stem cells. They undergo interkinetic nuclear movements along their apico-basal axis during the cell cycle. The neuroepithelial cell shows robust increases in the nucleoplasmic [Ca2+] in response to G protein-coupled receptor activation in S-phase, during which the nucleus is located in the basal region of the neuroepithelial cell. This response is caused by Ca2+release from intracellular Ca2+stores, which are comprised of the endoplasmic reticulum and the nuclear envelope. The Ca2+release leads to the activation of Ca2+entry from the extracellular space, which is called capacitative, or store-operated Ca2+entry. These movements of Ca2+are essential for DNA synthesis during S-phase. Spontaneous Ca2+oscillations also occur synchronously across the cells. This synchronization is mediated by voltage fluctuations in the membrane potential of the nuclear envelope due to Ca2+release and the counter movement of K+ions; the voltage fluctuation induces alternating current (AC), which is transmitted via capacitative electrical coupling to the neighboring cells. The membrane potential across the plasma membrane is stabilized through gap junction coupling by lowering the input resistance. Thus, stored Ca2+ions are a key player in the maintenance of the cellular activity of neuroepithelial cells.


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.


1977 ◽  
Vol 55 (5) ◽  
pp. 511-519 ◽  
Author(s):  
John M. Cheeseman ◽  
Barbara G. Pickard

Extract containing Ricca's factor depolarizes the membrane potential of at least three types of cells in Lycopersicon leaves : mesophyll, midrib parenchyma, and midrib epidermis. The depolarization has been studied in some detail for the epidermal cells, in which depolarization appears to begin without a lag and is completed within 60–90 s. The maximum rate of depolarization is typically about 3 mV s−1. No changes in resistivity, capacivity, or intercellular electrical coupling have been detected during the depolarization.Extract from 0.5 mg fresh leaf tissue in 1 ml of water at pH 6.6 causes threshold depolarization in many experiments, and a concentration only 40 times greater is usually saturating. Raising the pH increases the concentration of factor required for saturation.With subsaturating concentrations of factor, the potential recovers somewhat after depolarization, and when factor-free medium is washed over the tissue the potential depolarizes briefly before returning to its baseline value. With saturating concentrations of factor, the potential depolarizes to an essentially stable level and no transient depolarization occurs when the factor is washed out.The potential remaining after application of a saturating concentration of factor is independent of the initial baseline potential but depends on the concentration of K+ in the equilibration medium and in the extract. The saturation level of depolarization is in the range of the Nernstian potential for K+, but whether it is precisely equal to the Nernstian potential for K+ has not been established.Evidently, the occurrence and influence of Ricca's factor should be taken into account in all electrophysiological studies of shoot tissue since the factor appears to be released whenever cells are wounded and may be released during other kinds of stress as well.


2018 ◽  
Vol 150 (12) ◽  
pp. 1606-1639 ◽  
Author(s):  
Andrew L. Harris

As the physiology of synapses began to be explored in the 1950s, it became clear that electrical communication between neurons could not always be explained by chemical transmission. Instead, careful studies pointed to a direct intercellular pathway of current flow and to the anatomical structure that was (eventually) called the gap junction. The mechanism of intercellular current flow was simple compared with chemical transmission, but the consequences of electrical signaling in excitable tissues were not. With the recognition that channels were a means of passive ion movement across membranes, the character and behavior of gap junction channels came under scrutiny. It became evident that these gated channels mediated intercellular transfer of small molecules as well as atomic ions, thereby mediating chemical, as well as electrical, signaling. Members of the responsible protein family in vertebrates—connexins—were cloned and their channels studied by many of the increasingly biophysical techniques that were being applied to other channels. As described here, much of the evolution of the field, from electrical coupling to channel structure–function, has appeared in the pages of the Journal of General Physiology.


Neuroglia ◽  
2018 ◽  
Vol 1 (1) ◽  
pp. 271-279 ◽  
Author(s):  
Mi Huang ◽  
Yixing Du ◽  
Conrad Kiyoshi ◽  
Xiao Wu ◽  
Candice Askwith ◽  
...  

Due to strong electrical coupling, syncytial isopotentiality emerges as a physiological mechanism that coordinates astrocytes into a highly efficient system in brain homeostasis. Although this electrophysiological phenomenon has now been observed in astrocyte networks established by different astrocyte subtypes, the spinal cord remains a brain region that is still unexplored. In ALDH1L1-eGFP transgenic mice, astrocytes can be visualized by confocal microscopy and the spinal cord astrocytes in grey matter are organized in a distinctive pattern. Namely, each astrocyte resides with more directly coupled neighbors at shorter interastrocytic distances compared to protoplasmic astrocytes in the hippocampal CA1 region. In whole-cell patch clamp recording, the spinal cord grey matter astrocytes exhibit passive K+ conductance and a highly hyperpolarized membrane potential of −80 mV. To answer whether syncytial isopotentiality is a shared feature of astrocyte networks in the spinal cord, the K+ content in a physiological recording solution was substituted by equimolar Na+ for whole-cell recording in spinal cord slices. In uncoupled single astrocytes, this substitution of endogenous K+ with Na+ is known to depolarize astrocytes to around 0 mV as predicted by Goldman–Hodgkin–Katz (GHK) equation. In contrast, the existence of syncytial isopotentiality is indicated by a disobedience of the GHK predication as the recorded astrocyte’s membrane potential remains at a quasi-physiological level that is comparable to its neighbors due to strong electrical coupling. We showed that the strength of syncytial isopotentiality in spinal cord grey matter is significantly stronger than that of astrocyte network in the hippocampal CA1 region. Thus, this study corroborates the notion that syncytial isopotentiality most likely represents a system-wide electrical feature of astrocytic networks throughout the brain.


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