Abstract
While the effects of social experience on nervous system function have been extensively investigated in both vertebrate and invertebrate systems, our understanding of how social status differentially affects learning remains limited. In the context of habituation, a well-characterized form of non-associative learning, we investigated how the learning processes differ between socially dominant and subordinate in zebrafish (Danio rerio). We found that social status and frequency of stimulus inputs influence the habituation rate of short latency C-start escape response that is initiated by the Mauthner neuron (M-cell). Socially dominant animals exhibited higher habituation rates compared to socially subordinate animals at a moderate stimulus frequency, but low stimulus frequency eliminated this difference of habituation rates between the two social phenotypes. Moreover, habituation rates of both dominants and subordinates were higher at a moderate stimulus frequency compared to those at a low stimulus frequency. We investigated a potential mechanism underlying these status-dependent differences by constructing a simplified neurocomputational model of the M-cell escape circuit. The computational study showed that the change in total net excitability of the model M-cell was able to replicate the experimental results. At moderate stimulus frequency, the model M-cell with lower total net excitability, that mimicked a dominant-like phenotype, exhibited higher habituation rates. On the other hand, the model with higher total net excitability, that mimicked the subordinate-like phenotype, exhibited lower habituation rates. The relationship between habituation rates and characteristics (frequency and amplitude) of the repeated stimulus were also investigated. We found that habituation rates are decreasing functions of amplitude and increasing functions of frequency while these rates depend on social status (higher for dominants and lower for subordinates). Our results show that social status affects habituative learning in zebrafish, which could be mediated by a summative neuromodulatory input to the M-cell escape circuit, which enables animals to readily learn to adapt to changes in their social environment.
Highlights
Most animals make context-dependent behavioral decisions as they navigate their environment (Calabrese, 2003; Kristan, 2008; Nienborg et al, 2012)
When the same experiment was repeated with a 0.2 Hz stimulation protocol, we found that the habituation rate was reduced and differences of habituation rates among the three animal groups became less pronounced (Figure 2 right panels)
We investigated one possible mechanism of how social status affects habituation processes in zebrafish to repeated auditory stimulation
Summary
Most animals make context-dependent behavioral decisions as they navigate their environment (Calabrese, 2003; Kristan, 2008; Nienborg et al, 2012). For social animals these decisions are influenced in part by intraspecific social interactions that develop into long-term and stable dominance relationships (Issa et al, 2012; Miller et al, 2017). The effects of social experience on nervous system function has been investigated in both vertebrate and invertebrate systems, our understanding of how dominance relationships differentially affect learning remains limited (Yeh et al, 1996; Issa et al, 2012; Araki et al, 2013). While habituation has been described in many organisms including Cnidarians (Rushforth et al, 1964), aplysia (Kandel, 2009), crayfish (Krasne and Woodsmall, 1969; Araki et al, 2013), zebrafish (Eaton et al, 1977a; Marsden and Granato, 2015; Pantoja et al, 2016; Roberts et al, 2016) and humans (Davis, 1934), it remains unclear how social dominance leads to neural differences underlying habituation processes (Glanzman, 2009; Thompson, 2009)
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