Temporal microstructure of dyadic social behavior during relationship formation in mice

Abstract

Socially competent animals must learn to modify their behavior in response to their social partner in a contextually appropriate manner. Dominant-subordinate relationships are a particularly salient social context for mice. Here we observe and analyze the microstructure of social and non-social behaviors as 21 pairs of outbred CD-1 male mice (Mus Musculus) establish dominant-subordinate relationships during daily 20-minute interactions for five consecutive days in a neutral environment. Firstly, using a Kleinberg burst detection algorithm, we demonstrate aggressive and subordinate interactions occur in bursting patterns followed by quiescent periods rather than being uniformly distributed across social interactions. Secondly, we identify three phases of dominant-subordinate relationship development (pre-, middle-, and post-resolution) by utilizing two statistical methods to identify stability in aggressive and subordinate behavior across these bursts. Thirdly, using First Order Markov Chains we find that dominant and subordinate mice show distinct behavioral transitions, especially between tail rattling and other aggressive/subordinate behaviors. Further, dominant animals engaged in more digging and allogrooming behavior and were more likely to transition from sniffing their partner's body to head, whereas subordinates were more likely to transition from head sniffing to side-by-side contact. Lastly, we utilized a novel method (Forward Spike Time Tiling Coefficient) to assess how individuals respond to the behaviors of their partner. We found that subordinates decrease their tail rattling and aggressive behavior in response to aggressive but not subordinate behavior exhibited by dominants and that tail rattling in particular may function to deescalate aggressive behavior in pairs. Our findings demonstrate that CD-1 male mice rapidly establish dominance relationships and modify their social and non-social behaviors according to their current social status. The methods that we detail also provide useful tools for other researchers wishing to evaluate the temporal dynamics of rodent social behavior.

Fig 1. Duration of aggressive and subordinate behaviors of eventual dominant and subordinate individuals across 5 days.

Grey lines represent each individual and red lines represent mean duration of each group.

Fig 2. Exemplar temporal pattern of aggressive and subordinate behaviors by the eventual dominant (D) and subordinate (S) males on days 1–5 (Dyad C and Dyad G).

Yellow bars represent individual bursts identified by the Kleinberg’s burst detection algorithm (gamma = 0.3).

Fig 3. Phi-coefficient of aggressive and subordinate behavior by burst number within each dyad.

Black dotted vertical lines represent when relationships are resolved according to phi-coefficient method. Red dots demonstrate significantly distinct levels of aggression versus subordinate behavior by each partner. Note that we excluded any bursts with less than 6 behavior bouts to determine the relationship resolution but those bursts are still shown in the graph.

Fig 4. Differences in aggressive and subordinate behaviors between dominant and subordinate males by burst number within each dyad.

The red line indicates the difference of aggressive behavior (dominant male–subordinate male) and the blue line indicate difference of subordinate behavior (dominant male–subordinate male). In difference method, the relationship is considered resolved at a point when the blue line is always below red line for all remaining bursts. Black dotted vertical lines represent when relationships are resolved according to the difference method.

Fig 5

Relative proportion of time each behavior is exhibited the by eventual dominant (red) and subordinate (blue) mice during each phase. Data are medians ± IQRs. The asterisks indicate p-values from paired Wilcoxon Signed Rank Tests; *: p<0.05, **: p<0.01, ***: p<0.001.

Fig 6

Kinetogram of transitions between behaviors for (A) dominants pre-resolution, (B) dominants post-resolution, (C) subordinates pre-resolution and (D) subordinates post-resolution. All transitions that occur with a median probability of above 0.075 are shown. Label size represents the relative frequency of each behavior. Line weight represents the relative transition probability. Red lines indicate transitions that occur at rates significantly greater than expected by chance. Abbreviations: A–moving, AG–allogrooming, Bite–biting, Dig–digging, Flee–fleeing, Freeze–freezing, I–inactive, Lun–lunge, Pur–pursuing, R–rearing, SG–self-grooming, Sn-AG–anogenital sniffing, Sn-B–body-sniffing, Sn-F–sniff-following, Sn-H–head-sniffing, SP–subordinate posture, SS–side-by-side contact, TR–tail rattling.

Fig 7

Forward STTC values with standard errors of nine selected contingencies in DOM→SUB (red) and SUB→DOM (blue) directions in pre- and post-resolution phases. The asterisks indicate significant differences between DOM→SUB and SUB→DOM directions. The differences in FSTTC values between the directions of each dyad were tested using paired Wilcoxon Signed Rank Tests. The asterisks indicate p-values from paired Wilcoxon Signed Rank Tests; *: p<0.05, **: p<0.01, ***: p<0.001.