Chronic social isolation affects thigmotaxis and whole-brain serotonin levels in adult zebrafish

Shams, Soaleha; Chatterjee, Diptendu; Gerlai, Robert

doi:10.1016/j.bbr.2015.05.061

Cited by 91 publications

(66 citation statements)

References 24 publications

(48 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…One can hypothesize that a low stress-induced cortisol response, without any change in basal levels, and the accompanying low avoidance behavior might indicate a malfunction of challenge-responding. This phenotypic background may account for low avoidance in adult and decreased locomotion in 30 dpf juvenile zebrafish after social isolation as well, observed by Shams and colleagues (Shams et al, 2017a, 2015). This theory is also supported by our findings on isolation-induced low, delayed avoidance and inadequate arousal in response to a challenge and enhanced arousal under baseline, resting conditions.…”

Section: Discussionsupporting

confidence: 63%

“…phenomenological correlates of other anxiety-like domains were enhanced in response to social isolation. According to rodent and zebrafish literature, it is rare, but not unique (Parker, 2012; Shams et al, 2015), that such a chronic environmental perturbation as social isolation promotes a low anxiety phenotype (for reviews see Fone and Porkess, 2008; Hall, 1998; Lukkes et al, 2009), particularly, several authors discussed social isolation of zebrafish as beneficial, since it consistently decreased stress-induced cortisol response and in some cases avoidance as well (Forsatkar et al, 2017; Giacomini, 2015; Parker, 2012; Shams et al, 2015). Despite the importance of these results, we suggest a more careful interpretation of the above data.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Conserved serotonergic background of experience-dependent challenge-responding in zebrafish (Danio rerio)

Varga

Pejtsik

Biró

et al. 2019

Preprint

View full text Add to dashboard Cite

Forming effective responses to threatening stimuli requires the adequate and coordinated emergence of stress-related internal states. Such ability depends on early-life experiences and, in connection, the adequate formation of neuromodulatory systems, particularly serotonergic signaling. Here, we assess the serotonergic background of experience-dependent behavioral responsiveness employing a zebrafish (Danio rerio) model. For the first time, we have characterized a period during the behavioral metamorphosis in which zebrafish are highly reactive to their environment. Absence of social stimuli during this phase established by isolated rearing fundamentally altered the behavioral phenotype of post-metamorphic zebrafish in a challenge-specific manner, partially due to a decline in responsiveness and an inability to develop stress-associated arousal state. In line with this, isolation differently affected whole-brain 5-HT signaling in resting and stress-induced conditions, an effect that was present at the level of the dorsal pallium and was negatively associated with responsiveness. Administration of the 5HT1AR partial agonist buspirone prevented the isolation-induced serotonin response to novelty in the forebrain and rescued stress-induced arousal along with challenge-induced behaviors, which altogether indicates a functional connection between these changes. In summary, there is a consistent negative association between behavioral responsiveness and serotonergic signaling in zebrafish, which is well recognizable through the modifying effects of developmental perturbation and pharmacological manipulations as well. Our results imply a conserved serotonergic mechanism that context-dependently modulates environmental reactivity and is highly sensitive to experiences acquired during a specific early-life time-window, a phenomenon that was previously only suggested in mammals.Significance statementThe ability to respond to challenges is a fundamental factor in survival. We show that zebrafish that lack appropriate social stimuli in a sensitive developmental period show exacerbated alertness in non-stressful conditions while failing to react adequately to stressors. This shift is reflected inversely by central serotonergic signaling, a system that is implicated in numerous mental disorders in humans. Serotonergic changes in brain regions modulating responsivity and behavioral impairment were both prevented by the pharmacological blockade of serotonergic function. These results imply a serotonergic mechanism in zebrafish that transmits early-life experiences to the later phenotype by shaping stress-dependent behavioral reactivity, a phenomenon that was previously only suggested in mammals. Zebrafish provide new insights into early-life-dependent neuromodulation of behavioral stress-responses.

show abstract

Section: Discussionsupporting

confidence: 63%

Section: Discussionmentioning

confidence: 99%

Conserved serotonergic background of experience-dependent challenge-responding in zebrafish (Danio rerio)

Varga

Pejtsik

Biró

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…neurotransmitters such as dopamine and serotonin have been found to be positively correlated with shoaling in zebrafish (Buske and Gerlai, 2011;Dahlbom et al, 2012;Saif et al, 2013;Shams et al, 2015), specific functional mechanisms and brain regions that control shoaling remain poorly understood. Nonetheless, reliable paradigms that allow manipulation and quantification of shoaling and related behaviors provide unique opportunities to predict, test, and understand biological mechanisms that regulate shoaling and, in turn, enhance social behavior research.…”

Section: Social Behavior Of Zebrafishmentioning

confidence: 99%

“…The absence of specific visual or odor cues from siblings for the first seven days of life has been shown to result in the reduction or loss of future kin recognition, while complete social isolation across development has been found to impair social behavior later in life (Engeszer et al, 2004;Gerlach et al, 2008 anxiety-related responses and to reduce whole-brain serotonin and whole-body cortisol levels in adult zebrafish (Shams et al, 2015). Behavioral paradigms, in particular social interaction tasks and tests of anxiety and locomotor activity, may be unreliable if prior social experience and social environment of the testing or stimulus fish are not taken into consideration.…”

Section: The Effect Of Environmental Stimuli On Shoalingmentioning

confidence: 99%

“…Behavioral parameters one may extract include the area occupied by the whole group, interindividual distances, nearest-neighbor distances, polarization of movement, excursions or fissures from the group (Buske and Gerlai, 2011;Miller and Gerlai, 2007;2011a. 2011b2012;Miller et al, 2013;Shams et al, 2015). While lacking experimental control of the stimuli perceived (increased variability) and posing a greater challenge of the quantification of behavior (i.e., a larger number of dynamically moving agents to track and statistically analyze), the analysis of freely moving live shoals allows more precise description of the dynamic social responses of the zebrafish both in short (seconds) and longer (days, weeks or months) time scales (Miller and Gerlai, 2008;Buske and Gerlai, 2011 (Engeszer et al, 2004;Gerlach et al, 2008;Moretz et al, 2007) or pharmacological agents (Coe et al, 2010;Buske and Gerlai, 2010).…”

Section: How To Induce and Measure Shoaling In Zebrafishmentioning

confidence: 99%

See 1 more Smart Citation

The zebrafish as a promising tool for modeling human brain disorders: A review based upon an IBNS Symposium

Shams

Rihel

Ortíz

et al. 2018

Neuroscience & Biobehavioral Reviews

Self Cite

View full text Add to dashboard Cite

The zebrafish represents an excellent compromise between system complexity and practical simplicity, features that make it useful for modeling and mechanistic analysis of complex brain disorders. Also promising are screens for psychoactive drugs with effects on larval and adult zebrafish behavior. This review, based upon a recent symposium held at the 2016 IBNS Congress, provides different perspectives on how the zebrafish may be utilized to advance research into human central nervous system disorders. It starts with a discussion on an important bottleneck in zebrafish research, measuring the behavior of this species (specifically shoaling), and continues with examples on research on autism spectrum disorder in larval zebrafish, on screening natural products for compounds with psychoactive properties in adult zebrafish, and on the development of a zebrafish model of fetal alcohol spectrum disorders. By providing information on a broad spectrum of brain disorders, experimental methods, and scientific approaches using both larval and adult zebrafish, the review is intended to showcase this underutilized laboratory species for behavioral neuroscience and psychopharmacology research.

show abstract

Developmental social isolation affects adult behavior, social interaction, and dopamine metabolite levels in zebrafish

Shams

Amlani

Buske

et al. 2017

Developmental Psychobiology

Self Cite

View full text Add to dashboard Cite

The zebrafish is a social vertebrate and an excellent translational model for a variety of human disorders. Abnormal social behavior is a hallmark of several human brain disorders. Social behavioral problems can arise as a result of adverse early social environment. Little is known about the effects of early social isolation in adult zebrafish. We compared zebrafish that were isolated for either short (7 days) or long duration (180 days) to socially housed zebrafish, testing their behavior across ontogenesis (ages 10, 30, 60, 90, 120, 180 days), and shoal cohesion and wholebrain monoamines and their metabolites in adulthood. Long social isolation increased locomotion and decreased shoal cohesion and anxiety in the open-field in adult. Additionally, both short and long social isolation reduced dopamine metabolite levels in response to social stimuli. Thus, early social isolation has lasting effects in zebrafish, and may be employed to generate zebrafish models of human neuropsychiatric conditions. K E Y W O R D Sanxiety, dopamine, locomotor activity, social behavior, social isolation, Zebrafish

show abstract

Chronic social isolation affects thigmotaxis and whole-brain serotonin levels in adult zebrafish

Cited by 91 publications

References 24 publications

Conserved serotonergic background of experience-dependent challenge-responding in zebrafish (Danio rerio)

Conserved serotonergic background of experience-dependent challenge-responding in zebrafish (Danio rerio)

The zebrafish as a promising tool for modeling human brain disorders: A review based upon an IBNS Symposium

Developmental social isolation affects adult behavior, social interaction, and dopamine metabolite levels in zebrafish

Contact Info

Product

Resources

About