Dual and Opposing Modulatory Effects of Serotonin on Crayfish Lateral Giant Escape Command Neurons

Teshiba, Terri; Shamsian, Ashkan; Yashar, Bahram; Yeh, Shih-Rung; Edwards, Donald H.; Krasne, Franklin B.

doi:10.1523/jneurosci.21-12-04523.2001

Cited by 72 publications

(66 citation statements)

References 36 publications

(54 reference statements)

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“…Such opposing effects of 5-HT on identified neurons have also been reported elsewhere in the crayfish nervous system, specifically in the synaptic responses of the LG escape command neuron to afferent input (Lee et al 2008;Teshiba et al 2001). Such opposing of synaptic effects of a single neuromodulator seem to represent a common situation (for a review, see Harris-Warrick 2011;Harris-Warrick and Johnson 2010).…”

Section: Functional Significance Of the Spatial Separation Of Excitatsupporting

confidence: 54%

“…In vertebrates, this diversity is supported by a multiplicity of receptor subtypes, the localization of which seems functionally important (Riad et al 2000;Rumajogee et al 2006). In crayfish, serotonin (5-HT) influences aggressiveness (Huber and Delago 1998;Huber et al 1997a,b), social status (Huber et al 1997b(Huber et al , 2001, and escape behavior (Teshiba et al 2001). At the cellular level, the effects of 5-HT depend on the animal's social history (Le Bon-Jego et al 2004;Yeh et al 1996Yeh et al , 1997 but also on the regimen of serotonin application in animals that have been socially isolated.…”

mentioning

confidence: 99%

“…At the cellular level, the effects of 5-HT depend on the animal's social history (Le Bon-Jego et al 2004;Yeh et al 1996Yeh et al , 1997 but also on the regimen of serotonin application in animals that have been socially isolated. In isolated animals, both a slowly applied high concentration (5 ϫ 10 Ϫ5 M) and a rapidly applied low concentration (10 Ϫ6 M) of 5-HT facilitate the synaptic response of the lateral giant escape command neurons (LGs), whereas a rapid application of the same concentration inhibits the response (Teshiba et al 2001;Yeh et al 1996Yeh et al , 1997. In addition, the ionic mechanisms involved in the effects of 5-HT on LG in social isolates are complex.…”

mentioning

confidence: 99%

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Spatial segregation of excitatory and inhibitory effects of 5-HT on crayfish motoneurons

Bacqué-Cazenave

Issa

Edwards

et al. 2013

Journal of Neurophysiology

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Bacqué-Cazenave J, Issa FA, Edwards DH, Cattaert D. Spatial segregation of excitatory and inhibitory effects of 5-HT on crayfish motoneurons. J Neurophysiol 109: 2793-2802, 2013. First published March 13, 2013 doi:10.1152/jn.01063.2012.-Altering neuronal membrane properties, including input resistance, is a key modulatory mechanism for changing neural activity patterns. The effect of membrane currents generated by either synaptic or voltage-dependent channels directly depends on neuron input resistance. We found that local application of serotonin to different regions of identified motoneurons (MNs) of the postural/walking network of isolated crayfish produced different changes in input resistance. Puff-applied 5-HT in the periphery of the initial segment produced exclusively inhibitory responses. In contrast, when 5-HT was puff-applied on the central arbor of the same depressor (Dep) MN, exclusively depolarizing responses were obtained. Both inhibitory and excitatory responses were direct because they persisted in low-calcium saline. We found numerous close appositions between 5-HT-immunoreactive processes and the initial segment of dextran-rhodamine-filled Dep MNs. In contrast, almost no close apposition sites were found in Dep MN arbor. It seems that the 5-HT controls the level of excitability of postural network MNs by two mechanisms acting at two different sites: inhibitory responses (consistent with an action involving opening of K ϩ channels) occur in the initial segment region and may involve classic synaptic transmission, whereas depolarizing responses (consistent with an action involving closing of K ϩ channels) occur on MN branches via apparent paracrine effects.

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Section: Functional Significance Of the Spatial Separation Of Excitatsupporting

confidence: 54%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Spatial segregation of excitatory and inhibitory effects of 5-HT on crayfish motoneurons

Bacqué-Cazenave

Issa

Edwards

et al. 2013

Journal of Neurophysiology

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“…In crustacea, serotonin (5HT) was shown to modify synaptic transmission (Fischer and Florey, 1983;Delaney et al, 1991;Pearlstein et al, 1998;Wang and Zucker, 1998;Southard et al, 2000) and endogenous properties of neurons (Rossi-Durand, 1993;Alvarado-Alvarez et al, 2000;Nagayama, 2002). At the behavioral level 5HT can influence posture and walking (Teshiba et al, 2001;Tierney and Mangiamele, 2001), aggressiveness (Huber et al, 1997a,b), and social status in crayfish (Huber et al, 1997b(Huber et al, , 2001. For example, when injected into freely moving lobsters, 5HT and octopamine generate stable and stereotypical postures that resemble those seen in dominant (5HT) and subordinate (octopamine) lobsters (Livingstone et al, 1980;Kravitz, 1988).…”

Section: Introductionmentioning

confidence: 99%

Serotonin Enhances the Resistance Reflex of the Locomotor Network of the Crayfish through Multiple Modulatory Effects that Act Cooperatively

Bon-Jégo

Cattaert²,

Pearlstein³

2004

J. Neurosci.

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Serotonin (5HT) is an endogenous amine that modifies posture in crustacea. Here, we examined the mechanisms of action of 5HT on the resistance reflex in crayfish legs. This reflex, which counteracts movements imposed on a limb, is based on a negative feedback system formed by proprioceptors that sense joint angle movements and activate opposing motoneurons. We performed intracellular recordings from depressor motoneurons while repetitively stretching and releasing a leg joint proprioceptor in a resting in vitro preparation (i.e., a preparation that lacks spontaneous rhythmic activity). 5HT increased the amplitude of the depolarization during the release phase of the proprioceptor (corresponding to an upward movement of the leg) and the discharge frequency of the motoneurons. The 5HT-induced increase in the resistance reflex is caused, to a large extent, by polysynaptic pathways because it was very attenuated in the presence of high divalent cation solution. In addition to this activation of the polysynaptic pathways, 5HT also has postsynaptic effects that enhance the resistance reflex. 5HT causes a tonic depolarization, as well as an increase in the time constant and input resistance of motoneurons. We developed a simple mathematical model to describe the integrative properties of the motoneurons. The conclusion of this study is that the input frequency and the decay time constant of the EPSPs interact in such a way that small simultaneous changes in these parameters can cause a large effect on summation. Therefore, the conjunction of presynaptic and postsynaptic changes produces a strong cooperative effect on the resistance reflex response.

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“…Particularly in decapods, serotonin takes a prominent part in a number of physiological processes, such as feeding, walking, reproduction, heart rate, and aggression (e.g. Huber et al 1997a, b;Yeh et al 1997;Listerman et al 2000;Teshiba et al 2001;Tierney & Mangiamele 2001). Contrary to its mode of action in vertebrates (e.g.…”

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confidence: 99%

Biogenic amines influence aggressiveness in crayfish but not their force or hierarchical rank

Tricarico

Gherardi

2007

Animal Behaviour

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This study aimed at understanding the influence of biogenic amines on the agonistic behaviour of the crayfish Procambarus clarkii, a model organism for crustacean decapods. Specifically, we investigated whether the hierarchical rank of fighting individuals might be altered by injecting solutions of either serotonin or octopamine into their haemolymph. First, we assessed the effect and duration of the bioamines on the behaviour, posture, and chelar force of 60 adult males paired for size. Then, we examined their potential to modify dominance hierarchies by observing, for 2 h after the treatment, the behaviour of three categories of familiar size-matched pairs: (1) 20 'control pairs' (both individuals injected with a physiological solution), (2) 20 'reinforced pairs' (the dominant individual, alpha, injected with serotonin, and the subordinate individual, beta, with octopamine), and (3) 20 'inverted pairs' (alpha injected with octopamine and beta with serotonin). The results clearly show that the two bioamines were able to alter the posture and aggressiveness of the treated individuals in opposite directions without affecting their chelar force. However, the large majority of the 'inverted pairs' retained their former position in the hierarchy. The role that intrinsic characteristics and prior social experience play in maintaining dominance hierarchies in crayfish is discussed.

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Dual and Opposing Modulatory Effects of Serotonin on Crayfish Lateral Giant Escape Command Neurons

Cited by 72 publications

References 36 publications

Spatial segregation of excitatory and inhibitory effects of 5-HT on crayfish motoneurons

Spatial segregation of excitatory and inhibitory effects of 5-HT on crayfish motoneurons

Serotonin Enhances the Resistance Reflex of the Locomotor Network of the Crayfish through Multiple Modulatory Effects that Act Cooperatively

Biogenic amines influence aggressiveness in crayfish but not their force or hierarchical rank

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