Postexcitatory Inhibition of the Crayfish Lateral Giant Neuron: A Mechanism for Sensory Temporal Filtering

Vu, Eric T.; Berkowitz, Ari; Krasne, Franklin B.

doi:10.1523/jneurosci.17-22-08867.1997

Cited by 16 publications

(20 citation statements)

References 39 publications

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“…In fact, fewer Com preparations were activated by 100 mmol l −1 EtOH than by 20 mmol l −1 EtOH, and they produced fewer LG action potentials (20 mmol l Com crayfish (20 mmol l −1 : 25.57±7.26, 100 mmol l −1 : 16.33±7.2) or Iso crayfish (20 mmol l −1 : 8.2±7.95, 100 mmol l −1 : 10.5±6.17). The resilience of LG to saline washout has also been shown in other studies following exposure to different neuropharmacological agents such as serotonin and picrotoxin (Yeh et al, 1996;Vu et al, 1997).…”

Section: Resultssupporting

confidence: 57%

Prior social experience affects the behavioral and neural responses to acute alcohol in juvenile crayfish

Swierzbinski

Lazarchik

Herberholz

2017

Journal of Experimental Biology

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The effects of alcohol on society can be devastating, both as an immediate consequence of acute intoxication and as a powerful drug of abuse. However, the neurocellular mechanisms of alcohol intoxication are still elusive, partly because of the complex interactions between alcohol and nervous system function. We found that juvenile crayfish are behaviorally sensitive to acute alcohol exposure and progress through stages that are strikingly similar to those of most other intoxicated organisms. Most surprisingly, we found that the social history of the animals significantly modified the acute effects of alcohol. Crayfish taken from a rich social environment became intoxicated more rapidly than animals that were socially isolated before alcohol exposure. In addition, we found that the modulation of intoxicated behaviors by prior social experience was paralleled on the level of individual neurons. These results significantly improve our understanding of the mechanisms underlying the interplay between social experience, alcohol intoxication and nervous system function.

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Section: Resultssupporting

confidence: 57%

Prior social experience affects the behavioral and neural responses to acute alcohol in juvenile crayfish

Swierzbinski

Lazarchik

Herberholz

2017

Journal of Experimental Biology

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“…4B). In others (not shown), excitation of the MSIs was prevented by superfusing the preparation with 50 M mecamylamine, which blocks nicotinic transmission from primary afferents to MSIs (34). In both cases the alpha component was largest when the two nerves were stimulated simultaneously and declined with increasing delay between them.…”

Section: Resultsmentioning

confidence: 95%

Neuronal coincidence detection by voltage-sensitive electrical synapses

Edwards

Yeh

Krasne

1998

Proc. Natl. Acad. Sci. U.S.A.

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Coincidence detection is important for functions as diverse as Hebbian learning, binaural localization, and visual attention. We show here that extremely precise coincidence detection is a natural consequence of the normal function of rectifying electrical synapses. Such synapses open to bidirectional current f low when presynaptic cells depolarize relative to their postsynaptic targets and remain open until well after completion of presynaptic spikes. When multiple input neurons fire simultaneously, the synaptic currents sum effectively and produce a large excitatory postsynaptic potential. However, when some inputs are delayed relative to the rest, their contributions are reduced because the early excitatory postsynaptic potential retards the opening of additional voltage-sensitive synapses, and the late synaptic currents are shunted by already opened junctions. These mechanisms account for the ability of the lateral giant neurons of crayfish to sum synchronous inputs, but not inputs separated by only 100 sec. This coincidence detection enables crayfish to produce ref lex escape responses only to very abrupt mechanical stimuli. In light of recent evidence that electrical synapses are common in the mammalian central nervous system, the mechanisms of coincidence detection described here may be widely used in many systems.Despite the importance of coincidence detection in many systems (1), including Hebbian learning (2-4), binaural localization (5-7), and visual attention (8, 9), the cellular mechanisms responsible for such detection are not well understood. Brevity of transmitter action, short postsynaptic membrane time constants, and rapidly activating outward currents that are triggered by excitatory postsynaptic potentials (EPSPs) can contribute to selective responsiveness to coincident stimuli (10-13). We report here that the properties of rectifying electrical synapses enable precise coincidence detection by a postsynaptic neuron that receives excitatory inputs from a converging array of these synapses. Coincidence detection is therefore an emergent property of rectifying synapses in a convergent network. Converging networks of this kind are realized in the afferent pathway to the lateral giant (LG) neuron of the crayfish, a command neuron for a tail flip escape reaction. We found that this network displays the predicted high degree of selection for coincident inputs. METHODS Theoretical.Each model neuron is a single electrical compartment with Hodgkin-Huxley conductances (14), and an electrical rectifier (Fig. 1A, diode symbol) with a voltage dependence similar to that of the giant motor synapse of crayfish (15, 16). For both model neurons, G NaMax ϭ 720 S, G KMax ϭ 216 S, G L ϭ 1 S, E Na ϭ ϩ45 mV (relative to a Ϫ70 mV rest potential), E K ϭ Ϫ82 mV, E L ϭ Ϫ60 mV, and C (compartmental capacitance) ϭ 6 nF. These values are equivalent to those of the Hodgkin-Huxley model of the squid axon calculated for a temperature of 19°C and are not critical for the operation of the model. For the rectifying elect...

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“…A comparable dendritic feedforward inhibitory circuit has been described in the crayfish startle escape system where it provides for a temporal filter that allows only abrupt stimuli to activate the lateral giant neuron (Vu et al 1997). Activation of the M-cell appears less restrictive because both abrupt acoustic and gradually building visual looms evoke M-cell-mediated startles Weiss et al 2006).…”

Section: Discussionmentioning

confidence: 97%

Social and Ecological Regulation of a Decision-Making Circuit

Neumeister

Whitaker

Hofmann

et al. 2010

Journal of Neurophysiology

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Ecological context, sensory inputs, and the internal physiological state are all factors that need to be integrated for an animal to make appropriate behavioral decisions. However, these factors have rarely been studied in the same system. In the African cichlid fish Astatotilapia burtoni, males alternate between two phenotypes based on position in a social hierarchy. When dominant (DOM), fish display bright body coloration and a wealth of aggressive and reproductive behavioral patterns that make them conspicuous to predators. Subordinate (SUB) males, on the other hand, decrease predation risk by adopting cryptic coloration and schooling behavior. We therefore hypothesized that DOMs would show enhanced startle-escape responsiveness to compensate for their increased predation risk. Indeed, behavioral responses to sound clicks of various intensities showed a significantly higher mean startle rate in DOMs compared with SUBs. Electrophysiological recordings from the Mauthner cells (M-cells), the neurons triggering startle, were performed in anesthetized animals and showed larger synaptic responses to sound clicks in DOMs, consistent with the behavioral results. In addition, the inhibitory drive mediated by interneurons (passive hyperpolarizing potential [PHP] cells) presynaptic to the M-cell was significantly reduced in DOMs. Taken together, the results suggest that the likelihood for an escape to occur for a given auditory stimulus is higher in DOMs because of a more excitable M-cell. More broadly, this study provides an integrative explanation of an ecological and social trade-off at the level of an identifiable decision-making neural circuit.

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Postexcitatory Inhibition of the Crayfish Lateral Giant Neuron: A Mechanism for Sensory Temporal Filtering

Cited by 16 publications

References 39 publications

Prior social experience affects the behavioral and neural responses to acute alcohol in juvenile crayfish

Prior social experience affects the behavioral and neural responses to acute alcohol in juvenile crayfish

Neuronal coincidence detection by voltage-sensitive electrical synapses

Social and Ecological Regulation of a Decision-Making Circuit

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