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Effects of Social Experience on the Habituation Rate of Zebrafish Startle Escape Response: Empirical and Computational Analyses - PubMed

  • ️Mon Jan 01 2018

Effects of Social Experience on the Habituation Rate of Zebrafish Startle Escape Response: Empirical and Computational Analyses

Choongseok Park et al. Front Neural Circuits. 2018.

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.

Keywords: Mauthner neuron; aggression; computational model; habituation; learning; social status; zebrafish.

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Figures

Figure 1
Figure 1

Schematic illustrations of the M-cell escape circuit, experimental setup and recording. (A) Schematic illustration of the M-cell escape circuit. Zebrafish startle response is activated by auditory stimuli. C-start behavior is mediated by the Mauthner neural circuit. M-cell innervates contralateral spinal cord motor neurons that activate the musculature. Activation of the M-cell is necessary for C-start escape. (B) A pair of bath electrodes is placed on each end of each testing chamber. Bath electrodes detect neuromuscular field potentials generated as the M-cell escape response is activated. M-cell escape is activated by an auditory pulse. Field potentials and stimuli are time-locked and digitally recorded. (C) An illustrative example of a phasic field potential recording during activation of the C-start escape response mediated by the M-cell followed by C-start bend and counter-bends. (D) Representation of the repeated auditory stimuli at 1 and 0.2 Hz. (E) Latency between the stimulus and the phasic potential for communals (COMM), dominants (DOM), and subordinates (SUB) at 1 and 0.2 Hz. Mean±SEM was plotted.

Figure 2
Figure 2

Social status affects the response rates of startle escape. Repeated auditory stimuli at 1 Hz (left panel) causes rapid habituation in all animal groups particularly in dominant animals. However, stimuli at 0.2 Hz (right panel) leads to modest habituation in all animals groups. (A) Individual example of response pattern of a communal animal and one pair of dominant and subordinate animals to repeated stimuli at 1 Hz (left panel) and 0.2 Hz (right panel). Deflections are M-cell mediated field potentials. (B) Raster plots of all animals tested. Each row represents the responses of one animal, and each symbol represents one M-cell mediated escape response. (C) Cumulative percent response patterns binned over 2 s periods (left panel) at 1 Hz and 10 s period (right panel) at 0.2 Hz for each group. Mean ±SEM was plotted.

Figure 3
Figure 3

A schematic illustrations of the M-cell escape circuit for all animal groups. The M-cell receives excitatory input (solid line with arrow head) and inhibitory input (dashed line with filled circle). (A) Subordinate-like case (SUB) with higher agmax. (B) Communal-like case (COMM) with moderate agmax. (C) Dominant-like case (DOM) with lower agmax. Thickness represents the strength of the input.

Figure 4
Figure 4

Numerical simulation of the model for dominant-like case (DOM) (agmax = 41.5 upper panels), communal-like case (COMM) (agmax = 42.2 middle panels), and subordinate-like case (SUB) (agmax = 43.5 lower panels) under periodic inputs at 1 Hz (left panels) and 0.2 Hz (right panels). Membrane voltage trace in DOM (upper panel), COMM (middle panel), and SUB (lower panel) at 1 Hz (A) and 0.2 Hz (B). (C) Irregular activity patterns of SUB at 1 Hz (corresponds to E right panel). (D) Area Ai under the voltage trace above the threshold (dash line) with action potential (left panel) and subthreshold (right panel). (E,F) One-dimensional return map in DOM (left panel), COMM (middle panel), and SUB (right panel) at 1 Hz (E) and 0.2 Hz (F).

Figure 5
Figure 5

Activity patterns of [Ca] and Enet in dominant-like case (DOM) (lower curves with square symbols) and subordinate-like case (SUB) (upper curves with circle symbols) under periodic inputs at 1 Hz (A) and 0.2 Hz (B). Insect in each panel in (A,B) show activity patterns of [Ca] and Enet in communal-like case (COMM) (triangle symbols) in a half-size scale. These activity patterns lie in between DOM and SUB. Circle, triangle, and square symbols denote the moments when inputs are given. Closed symbols denote that the cell fires action potentials (AP) accordingly while open symbols denote no action potential (no AP). (C,D) ([Ca], Enet)-space with the projection of the solution trajectory in DOM (left panel), COMM (middle panel), and in SUB (right panel) at 1 Hz (C) and 0.2 Hz (D). The solid straight line that cuts the figure from lower left to upper right is the jump-up curve.

Figure 6
Figure 6

Activity patterns of voltage (A), [Ca] (B), and Enet (C) in subordinate-like case (SUB) from 200 to 250 s at 1 Hz. As in Figure 5, closed circle denotes that the cell fires action potentials (AP) accordingly while open circle denotes no action potential (no AP). (D) ([Ca], Enet)-space with the simplified projection of the solution trajectory with the jump-up curve (vertical line). The insert figure plots only the first 10 solution trajectories.

Figure 7
Figure 7

The projection of contour level curves of Faithfulness onto the plane. Faithfulness of M-cell with the frequency and agmax (A,B) and amplitude of the stimulation input Ii(τ) (C,D). (A,C) Faithfulness during 20–30 s period when the repeated stimulations delivered at 20 s. (B, D) Faithfulness during 40–70 s period. High agmax resembles the activity patterns for subordinate-like case (SUB) while low agmax resembles the activity patterns for dominant-like case (DOM). Different curves represent different values of Faithfulness.

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