Social avoidance behavior in male tree shrews and prosocial behavior in male mice toward unfamiliar conspecifics in the laboratory
Adult male tree shrews vigorously defend against intruding male conspecifics. However, the characteristics of social behavior have not been entirely explored in these males. In this study, male wild-type tree shrews (Tupaia belangeri chinensis) and C57BL/6J mice were first allowed to familiarize themselves with an open-field apparatus. The tree shrews exhibited a short duration of movement (moving) in the novel environment, whereas the mice exhibited a long duration of movement. In the 30 min social preference-avoidance test, target animals significantly decreased the time spent by the experimental tree shrews in the social interaction (SI) zone, whereas experimental male mice exhibited the opposite. In addition, experimental tree shrews displayed a significantly longer latency to enter the SI zone in the second 15 min session (target-present) than in the first 15 min session (target-absent), which was different from that found in mice. Distinct behavioral patterns in response to a conspecific male were also observed in male tree shrews and mice in the first, second, and third 5 min periods. Thus, social behaviors in tree shrews and mice appeared to be time dependent. In summary, our study provides results of a modified social preference-avoidance test designed for the assessment of social behavior in tree shrews. Our findings demonstrate the existence of social avoidance behavior in male tree shrews and prosocial behavior in male mice toward unfamiliar conspecifics. The tree shrew may be a new animal model, which differs from mice, for the study of social avoidance and prosocial behaviors.
Figure 1. Total distance and movement provide information about general activity of tree shrews and mice
A: Total distance moved by tree shrews and mice in box during 5 min open-field test and every 2.5 min (left). Heatmaps show locomotor activity expressed as distance traveled in successive 1 min bins in open-field test over a 5 min period for each tree shrew and mouse (right). B: Total cumulative duration of movement (moving) of tree shrews and mice in open-field box during a 5 min sample period and every 2.5 min. Values are means±SEM (tree shrew: n=19; mouse: n=23).
Figure 2. Social preference-avoidance test in tree shrews
A: Schematic of social preference-avoidance test in tree shrews. Social interaction (SI) behaviors were assessed in the compartment. Test arena (SI zone and non-SI zone) and target (novel tree shrew) zone were blocked by perforated Plexiglas partition. Shadow indicates SI zone. B: Heatmaps show cumulative duration spent by wild-type tree shrews throughout compartment during social preference-avoidance test.
3. Behavioral differences in tree shrews and mice between target-absent and target-present trials in social preference-avoidance test
A: Comparison of total distance moved in compartment when target (novel tree shrew or mouse) is absent or present during 30 min sample period (first 15 min session: No target; second 15 min session: Target) and every 5 min. Heatmaps show total distance traveled in successive 1 min bins in social preference-avoidance test over a 30 min period for each tree shrew and mouse. B: In first 3 min of 15 min session, tree shrews demonstrated greater moving distances when target was absent than when target was present. C: Significant differences in total traveling distance in mice were found in first 6 min of 15 min session. D: Total cumulative duration of movement (moving) of tree shrews and mice in compartment during 30 min sample period and every 5 min. Heatmaps show total duration of movement (moving) of tree shrews and mice in successive 1 min bins. E, F: Cumulative duration of movement over time by tree shrews and mice from starting point through 15 min of each session. Values are means±SEM (tree shrew: n=19; mouse: n=23). Significant differences are indicated by *: P<0.05; **: P<0.01; #: P<0.05; ##: P<0.01; $: P<0.05; $$: P<0.01 (*: No target vs. target; #: Significantly different among target0-5 min, target5-10 min, and target10-15 min; $: Significantly different among no target0-5 min, no target5-10 min, and no target10-15 min).
4. Behavioral differences in tree shrews and mice between target-absent and target-present trials in social preference-avoidance test
A: Distance moved in social interaction (SI) zone when target is absent or present during 30 min social preference-avoidance test and every 5 min. Heatmaps show locomotor activity expressed as distance moved by each tree shrew and mouse in SI zone in successive 1 min bins. B: Experimental tree shrews showed higher motor activity from 2 min to 6 min when target animals were absent (target-absent vs. target-present). C: Experimental mice showed higher motor activity from 1 min to 14 min when target animals were present. D, E: Cumulative duration of movement (moving) of tree shrews and mice in SI zone during 30 min sample period and every 5 min. Values are means±SEM (tree shrew: n=19; mouse: n=23). Significant differences are indicated by *: P<0.05; **: P<0.01; #: P<0.05; $$: P<0.01 (*: No target vs. target; #: Significantly different among target0-5 min, target5-10 min, and target10-15 min; $: Significantly different among no target0-5 min, no target5-10 min, and no target10-15 min).
5. Behavioral differences in tree shrews and mice between target-absent and target-present trials
A: Comparison of time spent by tree shrews and mice in social interaction (SI) zone during 30 min social preference-avoidance test and every 5 min. Heatmaps show time spent by each tree shrew and mouse in SI zone in successive 1 min bins. B: Experimental tree shrews showed lower cumulative duration spent in SI zone from 2 min to 15 min when target animals were present. C: Experimental mice showed higher cumulative duration spent in SI zone during second 15 min session (target-present) than during first 15 min session. D: Latency to enter SI zone of tree shrews and mice during 30 min sample period. Heatmaps show latency to enter SI zone of tree shrews and mice over 30 min period (target-absent and target-present sessions) in successive 1 min bins. E: Experimental tree shrews showed significantly longer latency to enter SI zone in second 15 min session (target-present) than in first 15 min session (target-absent). F: Experimental mice showed significantly shorter latency to enter SI zone when target mice were present. Values are means±SEM (tree shrew: n=19; mouse: n=23). Significant differences are indicated by *: P<0.05; **: P<0.01; ##: P<0.01; $$: P<0.01 (*: No target vs. target; #: Significantly different among target0-5 min, target5-10 min, and target10-15 min; $: Significantly different among no target0-5 min, no target5-10 min, and no target10-15 min).
Figure 6. Behavioral differences in tree shrews and mice between target-absent and target-present trials
A, B: Comparison of frequency of entrances in social interaction (SI) zone when target (novel tree shrew or mouse) is absent or present during 30 min social preference-avoidance test and every 5 min. C: In tree shrews, target animals significantly decreased cumulative frequency of entrances in SI zone from 2 min to 4 min. D: Cumulative frequency of entrances of mice significantly increased in first 6 min of second session. Values are means±SEM (tree shrew: n=19; mouse: n=23). Significant differences are indicated by *: P<0.05; **: P<0.01; #: P<0.05; $$: P<0.01 (*: No target vs. target; #: Significantly different among target0-5 min, target5-10 min, and target10-15 min; $: Significantly different among no target0-5 min, no target5-10 min, and no target10-15 min).
Table 1. Mean, minimum, and maximum speeds of mice and tree shrews in open-field test (mean±SEM)
Minimum (cm/s) Mean (cm/s) Maximum (cm/s) Mouse 0.014±0.002 4.683±0.283 34.023±1.614 Tree shrew 0 3.851±0.514 165.003±24.974
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