Novel automated method to assess group dynamics reveals deficits in behavioral contagion in rats with social deficits

Abstract

Behavioral copying is a key process in group actions, but it is challenging for individuals with autism spectrum disorder (ASD). We investigated behavioral contagion, or instinctual replication of behaviors, in Krushinky-Molodkina (KM) rats (n = 16), a new potential rodent model for ASD, compared to control Wistar rats (n = 15). A randomly chosen healthy Wistar male ("demonstrator rat") was introduced to the homecage of experimental rats ("observers") 10-14 days before the experiments to become a member of the group. For the implementation of the behavioral contagion experiment, we used the IntelliCage system, where rats can live in a group of 5-6 rats and their water visits can be automatically scored. During the experiment, the demonstrator was taken out of IntelliCage for a pre-test water deprivation and then placed back for the behavioral contagion test. As a result, a drinking behavior of the water-deprived demonstrator rat prompted water-seeking and drinking behaviors in the whole group. Unlike the Wistar controls, KM observers showed fewer visits to the drinking bottles, particularly lacking inspection visits (i.e., visits without drinking). The control group, in contrast, exhibited a dynamic, cascade-like visiting of the water corners. The proportion of activated observers in KM rats was significantly lower, as compared to Wistar ones, and they did not mimic other observer rats. KM rats, therefore, displayed an attenuated pattern of behavioral contagion, highlighting social deficits in this strain. This study suggests that measuring group dynamics of behavioral contagion in an automated, non-invasive setup offers valuable insights into social behavior in rodents.

Keywords: IntelliCage; autism spectrum disorder; automated behavioral testing; behavioral contagion; group behavior; rat; social deficit.

FIGURE 1

Group aspects of behavioral contagion. (A) Experimental design. (B,C) Group graphs showing the dynamics of contagion in the cohorts of control Wistar (panel B) and KM (panel C) rats. The group graphs represent 30 min of observation. Red rat heads indicate the demonstrator rats (i.e., water-deprived animals) in each group. Yellow rat heads represent the activated observer rats, i.e., non-deprived animals that made at least one visit to the water corner. Gray rat heads correspond to passive observers, which did not visit the water corners. Red edges between the nodes represent quickly (< 4 s) copied visits to the water corner, as demonstrated by any groupmate. The thickness of the lines is proportional to the number of rapidly copied visits (ranging from 0 to 3 in this study).

FIGURE 2

Timeline of behavioral contagion in Wistar and KM Rats. Water corner visits were recorded for Wistar (left panels) and KM (right panels) rats. The timeline shows activities over a 4-hour period, starting from the re-introduction of the demonstrators. The contagion period, marked by red shading, is the period analyzed in the study (the first 30 min). Visits to the water corner by the demonstrators (denoted by “D” on the left side of each individual group chart) are indicated by red vertical stripes at the top of the chart. Visits by the observer rats (denoted by “O” on the left side of each individual group chart) are shown with black vertical stripes. The thickness of the lines is proportional to the duration of time each individual rat spent in the water corner.

FIGURE 3

Quantitative parameters of behavioral contagion in Wistar and KM rats. (A) Total number of visits (B) Number of inspection (without drinking) visits. (C) Number of drinking visits. (D) Licking time, in seconds. For panels (A–D), the significance level was set at p < 0.05. Between-strain differences are marked with “*”; contagion effects (test vs. baseline) are indicated by “##”; and cage × contagion interactions are shown with “&”. A single symbol represents p < 0.05, two symbols represent p < 0.01. See the Results section for more details.