Neuronal Adaptations to Changes in the Social Dominance Status of Crayfish

Yeh, Shih-Rung; Musolf, Barbara E.; Edwards, Donald H.

doi:10.1523/jneurosci.17-02-00697.1997

Cited by 132 publications

(141 citation statements)

References 58 publications

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“…This hypothesis is in part confirmed by previous physiological studies (Yeh et al 1996(Yeh et al , 1997. Different populations of serotonin receptors, responsible for escape responses, were found to occur in the lateral giant neurons of crayfish (Yeh et al 1996(Yeh et al , 1997Edwards & Kravitz 1997;Kravitz 2000) and seemed to be either transformed or replaced following a change in social status (Yeh et al 1997).…”

Section: Discussionsupporting

confidence: 82%

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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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Section: Discussionsupporting

confidence: 82%

“…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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“…Social status affects neurogenesis in rodents (Kozorovitskiy and Gould, 2004) and crayfish (Song et al, 2007), neuronal size in fish (White et al, 2002), brain morphology in wasps (O'Donnell et al, 2007) and naked mole rats (Holmes et al, 2007), and cell receptor populations in crayfish (Spitzer et al, 2005) and fish (Burmeister et al, 2007). Social status also affects the serotonergic neuromodulation of synaptic responses in both crayfish (Yeh et al, 1996(Yeh et al, , 1997 and fish (Whitaker et al, 2011), and the excitability of neural circuits that produce different behaviors (Krasne et al, 1997;Herberholz et al, 2001;Neumeister et al, 2010). It remains unclear, however, how neural circuits are altered to produce status-dependent behavioral responses.…”

Section: Introductionmentioning

confidence: 99%

Neural Circuit Reconfiguration by Social Status

Issa¹,

Drummond²,

Cattaert³

et al. 2012

J. Neurosci.

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The social rank of an animal is distinguished by its behavior relative to others in its community. Although social-status-dependent differences in behavior must arise because of differences in neural function, status-dependent differences in the underlying neural circuitry have only begun to be described. We report that dominant and subordinate crayfish differ in their behavioral orienting response to an unexpected unilateral touch, and that these differences correlate with functional differences in local neural circuits that mediate the responses. The behavioral differences correlate with simultaneously recorded differences in leg depressor muscle EMGs and with differences in the responses of depressor motor neurons recorded in reduced, in vitro preparations from the same animals. The responses of local serotonergic interneurons to unilateral stimuli displayed the same status-dependent differences as the depressor motor neurons. These results indicate that the circuits and their intrinsic serotonergic modulatory components are configured differently according to social status, and that these differences do not depend on a continuous descending signal from higher centers.

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“…Decisions may be made after only a brief encounter (seen particularly in the wild) or after prolonged periods of fighting when the physical asymmetries between animals are small. The presence of a highly structured, quantifiable behavioral system in these animals, combined with the potential to bring the analysis to the level of individual neurons (11)(12)(13)(14)(15)(16), offers unique vistas in crustaceans for a search for the proximate roots of aggression.…”

mentioning

confidence: 99%

“…These studies ultimately led to the postulate that amine neuron function might be changed by agonistic interactions between lobsters, with 5HT neuron function becoming more important in dominant animals and OA neuron function more important in subordinates. Recent studies in crayfish demonstrated long term changes in the distribution of 5HT receptor subtypes in specific synaptic regions (14,15) and changes in excitability of escape reflexes (16) accompanying changes in social status in these animals. With detailed information presently available on the locations of, and physiological roles served by, 5HT and OA neurons in crustaceans (11-13, 32, 33), these systems become even more valuable in the search for linkages between changes in behavior and changes in the functioning of particular neurons and their targets.…”

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confidence: 99%

Serotonin and aggressive motivation in crustaceans: Altering the decision to retreat

Huber

Smith

Delago

et al. 1997

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

242

139

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In crustaceans, as in most animal species, the amine serotonin has been suggested to serve important roles in aggression. Here we show that injection of serotonin into the hemolymph of subordinate, freely moving animals results in a renewed willingness of these animals to engage the dominants in further agonistic encounters. By multivariate statistical analysis, we demonstrate that this reversal results principally from a reduction in the likelihood of retreat and an increase in the duration of fighting. Serotonin infusion does not alter other aspects of fighting behavior, including which animal initiates an encounter, how quickly fighting escalates, or which animal eventually retreats. Preliminary studies suggest that serotonin uptake plays an important role in this behavioral reversal.Intraspecific encounters among clawed decapod crustaceans are characterized by a distinct shortage of diplomatic skills. With the exception of mating behavior, most interactions are agonistic in nature, escalating until one of the combatants withdraws. Success is based largely on physical superiority (1-3). Thus, resident populations are bound by a system of dominant/subordinate relationships based on initial agonistic encounters (4, 5). Fights escalate according to rules closely matching predictions of game theory (i.e., sequential assessment strategies), in which animals acquire information about an opponent's strength and fighting abilities in a stepwise manner (6-10). In this context, the timing of the decision to withdraw by either animal becomes the key element in determining the duration and progress of a fight (6,8,9). Decisions may be made after only a brief encounter (seen particularly in the wild) or after prolonged periods of fighting when the physical asymmetries between animals are small. The presence of a highly structured, quantifiable behavioral system in these animals, combined with the potential to bring the analysis to the level of individual neurons (11-16), offers unique vistas in crustaceans for a search for the proximate roots of aggression.The amine serotonin [5-hydroxytryptamine creatinine sulfate complex (5HT)] has been linked to aggression in a wide and diverse range of species, including humans (17-20). The nature of the linkage, however, is not simple, and it has proven difficult to unravel the role of the amine in the behavior. In vertebrates, lowered levels of 5HT (endogenous or experimentally induced) or changes in amine neuron function that lower the effectiveness of serotonergic neurons generally correlate with increased levels of aggression (19,20) whereas in invertebrates, the converse is believed to be true (11-13). Genetic alterations of amine neuron function also can change aggressive behavior in animals (21-24) and in people (25-27) although, again, in most cases, it is not clear how the genetic change is linked to the behavior. For example, in humans, a mutation leading to inactivation of one form of the enzyme monoamine oxidase leads to a particular form of explosive violent beha...

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Neuronal Adaptations to Changes in the Social Dominance Status of Crayfish

Cited by 132 publications

References 58 publications

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

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

Neural Circuit Reconfiguration by Social Status

Serotonin and aggressive motivation in crustaceans: Altering the decision to retreat

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