Testing synaptic plasticity in dynamic mate choice decisions: N -methyl d -aspartate receptor blockade disrupts female preference

Abstract

Social behaviours such as mate choice require context-specific responses, often with evolutionary consequences. Increasing evidence indicates that the behavioural plasticity associated with mate choice involves learning. For example, poeciliids show age-dependent changes in female preference functions and express synaptic-plasticity-associated molecular markers during mate choice. Here, we test whether social cognition is necessary for female preference behaviour by blocking the central player in synaptic plasticity, NMDAR (N-methyl D-aspartate receptor), in a poeciliid fish, Xiphophorus nigrensis. After subchronic exposure to NMDAR antagonist MK-801, female preference behaviours towards males were dramatically reduced. Overall activity levels were unaffected, but there was a directional shift from 'social' behaviours towards neutral activity. Multivariate gene expression patterns significantly discriminated between females with normal versus disrupted plasticity processes and correlated with preference behaviours-not general activity. Furthermore, molecular patterns support a distinction between 'preference' (e.g. neuroserpin, neuroligin-3, NMDAR) and 'sociality' (isotocin and vasotocin) gene clusters, highlighting a possible conservation between NMDAR disruption and nonapeptides in modulating behaviour. Our results suggest that mate preference may involve greater social memory processing than overall sociality, and that poeciliid preference functions integrate synaptic-plasticity-oriented 'preference' pathways with overall sociality to invoke dynamic, context-specific responses towards favoured males and away from unfavoured males.

Divergent neurogenomic responses shape social learning of both personality and mate preference

“…Boldness covaries with expression of stress-related genes in both dopaminergic (Thörnqvist et al, 2018) and serotonergic (Backström and Winberg, 2017) pathways of the brain, and immune response genes functionally link the immune system in the brain to anxiety-like behaviors and memory consolidation (Tonelli and Postolache, 2005;Marin and Kipnis, 2013). Mate choice measures, in contrast, are linked to a subset of pathways within the SDMN, including sex steroid hormone signaling (Davis and Leary, 2015;Sisneros et al, 2004), nonapeptide systems (Donaldson and Young, 2008) and synaptic-plasticity-linked genes such as neuroligins (Ramsey et al, 2014;Liang et al, 2015). Mating preference functions likely integrate these signaling pathways with social memory processing to make socially based decisions (Ramsey et al, 2014).…”

“…Mate choice measures, in contrast, are linked to a subset of pathways within the SDMN, including sex steroid hormone signaling (Davis and Leary, 2015;Sisneros et al, 2004), nonapeptide systems (Donaldson and Young, 2008) and synaptic-plasticity-linked genes such as neuroligins (Ramsey et al, 2014;Liang et al, 2015). Mating preference functions likely integrate these signaling pathways with social memory processing to make socially based decisions (Ramsey et al, 2014). Finally, mate choice depends on sensory perception and an individual's ability to integrate multimodal signals, and sensory gene expression can change markedly as a function of social and non-social experience (Ronald et al, 2012).…”

The integration of sociality, monoamines and stress neuroendocrinology in fish models: applications in the neurosciences

“…Defensive behaviours have been explored in different fish species, including Xiphophorus nigrensis Rosen 1960 (Ramsey et al ., ), G.aculeatus (Thompson et al ., ) and guppies Poecilia reticulata (Peters 1859) (Maximino et al ., ). Nonetheless, D. rerio are the most widely studied species when it comes to responses to threatening and aversive stimuli (Jesuthasan & Mathuru, ; Maximino et al ., ; Kalueff et al ., ; Gerlai, ).…”

The Integration of Sociality, Monoamines, and Stress Neuroendocrinology in Fish Models: Applications in the Neurosciences

“…A summary of this innervation patterns, as well as the homologies proposed for the teleostean brain, can be found in Table 1. & Northoff, 2011;Jovanovic & Norrholm, 2011), and overlaps extensively with the aversive behaviour network (LeDoux, 2012b (Ramsey et al, 2014), sticklebacks (Gasterosteus aculeatus L.) (Thompson et al, 2016), and guppies (Poecilia reticulata Peters 1859) (Maximino et al, 2010b). Nonetheless, zebrafish is the most widely studied species when it comes to responses to threatening and aversive stimuli (Jesuthasan & Mathuru, 2008;Maximino et al, 2010a;Kalueff et al, 2012;Gerlai, 2013).…”