Abnormal repetitive behaviour and exposure to negative experiences in rhesus monkeys

We tested the hypothesis that, in rhesus macaques used in biomedical research, the performance of abnormal repetitive behaviours (ARBs; e.g. pacing, hair-plucking, eye-poking) reflects the cumulative burden of negative experiences. For 240 macaques living in two US National Primate Centres, we did this by cataloguing, weighing, and summing exposure to 12 types of negative event or practice (two current, ten past), over animals' entire lifespans; and then assessing their aggregated impact on current behaviour. When all recorded forms of ARB were pooled into one measure, the hypothesis was strongly supported at one facility: Pooled ARB increased with Lifetime Negative Experience Scores in a dose-response type manner, and reflected the combined effects of both Current and Past Negative Experiences. At the other facility, Current Negative Experience Scores had no apparent impact on Pooled ARB; however, Past Negative Experience Scores were still highly predictive. This approach, inspired by psychological research on humans, adds to growing evidence that ARBs can reflect the cumulative impact of the number and severity of negative experiences, past and potentially present.

Methods
Subjects were 240 indoor-housed rhesus macaques at the California and Oregon National Primate Research Centers (anonymized in dataset): all the residents of 5 rooms per centre. They lived in metal cages, some singly, some in double-size cages in pairs. Behavioural data were remotely collected via live-streaming cameras, in scans repeated every c. 5 minutes for 3-4 hours daily over 4 (ONPRC) or 5 (CNPRC) consecutive days. Pacing, ‘rocking+’ and a third previously validated ARB sub-category, hair-plucking, were recorded in both facilities; present in >5% subjects; and also performed with good internal reliability. After initial analysis attempts, however, pacing and rocking+ were combined as 'motor ARB' (shared here). After results for hair-plucking and motor ARB emerged, all recorded ARBs were also pooled for further analysis: Pooled ARB is also shared here. 

Data on negative experiences over the lifespan: we identified 12 types of challenge (either events or facility practices) likely to induce negative affect. Two pertained to current housing: an adverse cage location (low, near the door); and being singly-caged. Ten (extracted from facility records) pertained to past experiences: maternal loss in infancy; being born and raised indoors; living indoors; spending time singly-caged; being relocated; being aggressed by a cagemate; losing a cagemate; involvement in research projects; health events (including research procedures); and spending time in hospital. To capture variation in aversiveness, every monkey was scored (blind to their behavioural data) between 0 and 1 for each challenge. For robustness, for 10 of the items we used two methods that varied in how differential experiences were weighted: a 'min-max' method divided a subject's scores by the dataset's greatest value for that challenge; and a 'quantiles' method scored each subjects categorically by ranks (typically quartiles) for each challenge. The two items pertaining to infancy (age when separated from mother; type of indoor/outdoor reading facility) were always scored 0-1 based on categories. All 22 scores are shared here. (Raw values are not shared for reasons of confidentiality). These scores were totalled to create two Lifetime Negative Experience Scores (maximum 12). Current Negative Experience and Past Negative Experience Scores (respective maxima 2, 10) were also created for analysis (again two for each, one based on quantiles method and one based on the 'min-max' method). These six Negative Experience Scores are also shared here.