Transient Electrical Coupling Delays the Onset of Chemical Neurotransmission at Developing Synapses

Szabo, Theresa M.; Faber, Donald S.; Zoran, Mark J.

doi:10.1523/jneurosci.4336-03.2004

Cited by 36 publications

(42 citation statements)

References 71 publications

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“…Electrical connections formed in a manner similar to that seen previously in vivo (Szabo et al, 2004). After 24h of cell-cell contact, 19-19 and 19-110 pairs possessed coupling coefficients (ECCs) of 0.32 ± 0.06 (n = 29) and 0.33 ± 0.06 (n = 32), respectively.…”

Section: Electrical and Chemical Neurotransmission In Two-cell Neuronsupporting

confidence: 70%

“…We first determined whether the sequence of synaptogenic events previously observed in these neurons lacking neurites (Szabo et al, 2004) also occurred in neurite-bearing networks. Cells were plated in each possible two-cell configuration, as 19-19, 19-110 and 110-110 partners, and were then incubated for 1 or 5 days of contact.…”

Section: Resultsmentioning

confidence: 99%

“…Four to five trains of 10 action potentials (APs, 1 per second) were evoked presynaptically in neuron 110, while the corresponding postsynaptic potentials (PSPs) in neuron 19 were recorded simultaneously. Criteria were developed to distinguish between electrical and chemical contributions (see Szabo et al, 2004). An analysis of 110-19 preparations possessing exclusively chemical connectivity indicated that the average latency from AP peak to PSP peak was 95msec.…”

Section: General Electrophysiologymentioning

confidence: 99%

“…At a period of transition from electrical to chemical communication, the two types of synaptic transmission appear to be inversely related; i.e., gap junctional coupling is sustained when cholinergic neurotransmission is blocked with tubocurare and chemical synaptic transmission is increased when electrical coupling is reduced (Szabo et al, 2004). While many examples of the temporal progression from electrical to chemical neurotransmission have been reported (Kandler and Katz, 1998;Szabo et al, 2004;Arumagam et al, 2005;Dupont et al, 2006) and underlying mechanisms have been proposed (Arumugam et al, 2005;Neunuebel and Zoran, 2005), much is still unknown about the influence of these interactions on the formation of neuronal networks. To directly address this question, we have used the defined synapses formed between identified Helisoma neurons in vitro to determine if the process of transient electrical coupling affects subsequent synapse formation in three-cell neuronal networks.…”

Section: Introductionmentioning

confidence: 99%

“…Transient electrical synaptic connections develop between Helisoma motoneurons 110 and 19, forming and then disappearing over a 48-72 hour period (Szabo et al, 2004;Neunuebel and Zoran, 2005). The decline in electrical coupling is coincident with the emergence of unidirectional cholinergic synaptic transmission between presynaptic neuron 110 and postsynaptic neuron 19.…”

Section: Introductionmentioning

confidence: 99%

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Transient electrical coupling regulates formation of neuronal networks

Szabo

Zoran

2007

Brain Research

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Electrical synapses are abundant before and during developmental windows of intense chemical synapse formation, and might therefore contribute to the establishment of neuronal networks. Transient electrical coupling develops and is then eliminated between regenerating Helisoma motoneurons 110 and 19 during a period of 48-72 hours in vivo and in vitro following nerve injury. An inverse relationship exists between electrical coupling and chemical synaptic transmission at these synapses, such that the decline in electrical coupling is coincident with the emergence of cholinergic synaptic transmission. In this study, we have generated two-and three-cell neuronal networks to test whether predicted synaptogenic capabilities were affected by previous synaptic interactions. Electrophysiological analyses demonstrated that synapses formed in three-cell neuronal networks were not those predicted based on synaptogenic outcomes in two-cell networks. Thus, new electrical and chemical synapse formation within a neuronal network is dependent on existing connectivity of that network. In addition, new contacts formed with established networks have little impact on these existing connections. These results suggest that network-dependent mechanisms, particularly those mediated by gap junctional coupling, regulate synapse formation within simple neural networks.

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Section: Electrical and Chemical Neurotransmission In Two-cell Neuronsupporting

confidence: 70%

Section: Resultsmentioning

confidence: 99%

Section: General Electrophysiologymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Transient electrical coupling regulates formation of neuronal networks

Szabo

Zoran

2007

Brain Research

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Regeneration of olfactory afferent axons in the locust brain

Stern¹,

Scheiblich²,

Eickhoff³

et al. 2012

J of Comparative Neurology

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The insect olfactory system consists of thousands of sensory neurons on each antenna, which project into the primary olfactory center, the glomerular antennnal lobe. There, they form synapses with local interneurons and projection neurons, which relay olfactory information to the second-order olfactory center, the mushroom body. Olfactory afferents of adult locusts (Locusta migratoria) were axotomized by crushing the base of the antenna. We studied the resulting degeneration and regeneration in the antennal lobe by size measurements, anterograde dye labeling through the antennal nerve, and immunofluorescence staining of cell surface markers. Within 3 days postcrush, the antennal lobe size was reduced by 30% and from then onward regained size back to normal by 2 weeks postinjury. Concomitantly, anterograde labeling revealed regenerating afferents reaching the antennal lobe by day 4 postcrush, and reinnervating the olfactory neuropil almost back to normal within 2 weeks. Regenerated fibers were directed precisely into the antennal lobe, where they reinnervated glomeruli. As a remarkable exception, a few regenerating fibers projected erroneously into the mushroom body on a pathway that is normally chosen by second-order projection neurons. Regenerating afferents expressed the cell surface proteins lachesin and fasciclin I. The antennal lobe neuropil expressed the cell surface marker semaphorin 1a. In conclusion, axonal regeneration in the locust olfactory system appears to be possible, precise, and fast, opening the possibility of future functional and mechanistic studies.

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Dye coupling in developing vestibular nuclei

Shao¹,

Gottesman-Davis²,

Popratiloff³

et al. 2007

J of Neuroscience Research

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The chick tangential nucleus is a major vestibular nucleus whose principal cells participate in the vestibular reflexes. During development, most mature vestibular nucleus neurons must acquire repetitive firing of action potentials on depolarization and spontaneous spike activity to process signals effectively. In the chicken, these properties emerge gradually in the embryo, starting the week before (E13, E16) and continuing through the first week after hatching (H7). Since gap junctionmediated cell coupling may influence the emergence of neuronal excitability, we investigated whether neuronneuron and neuron-glia coupling are present in this morphologically distinctive vestibular nucleus during the period for establishing signal processing. In brain slices, principal cells were injected with biocytin in the whole-cell configuration and visualized via confocal imaging at E13, E16, and H7. The incidence of dye coupling between the injected principal cell and neurons was 42% at E13, 75% at E16, and 7% at H7, whereas the incidence of dye coupling with glia was 100% at both embryonic ages but decreased to 27% by H7. For each injected principal cell at E13, one coupled neuron and 35 coupled glia were detected, whereas three coupled neurons and 12 coupled glia were observed at E16, and few if any coupled neurons and glia were detected at H7. These results suggest that neuron-neuron and neuron-glia coupling are developmentally regulated and present before, but not after, the onset of mature signal processing by these neurons. Thus, transient neuron-neuron and neuronglia coupling may both play roles in establishing excitability in vestibular nucleus neurons during development. V V C 2007 Wiley-Liss, Inc.

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Transient Electrical Coupling Delays the Onset of Chemical Neurotransmission at Developing Synapses

Cited by 36 publications

References 71 publications

Transient electrical coupling regulates formation of neuronal networks

Transient electrical coupling regulates formation of neuronal networks

Regeneration of olfactory afferent axons in the locust brain

Dye coupling in developing vestibular nuclei

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