# Impact of social and personalized visual enrichment on stereotypic behaviors in rhesus macaque monkeys in the laboratory: a case study

Nathan Lambert, Mathilde Pauchard, Clara Saleri, David Thura

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## To cite this version:

Nathan Lambert, Mathilde Pauchard, Clara Saleri, David Thura. Impact of social and personalized visual enrichment on stereotypic behaviors in rhesus macaque monkeys in the laboratory: a case study. 2025, 10.60675/vnga-dk52/sn20251202-5r/short-notes. hal-05409702

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# Impact of social and personalized visual enrichment on stereotypic behaviors in rhesus macaque monkeys in the laboratory: a case study

Nathan Lambert*<fnref n="1" />, Mathilde Pauchard*<fnref n="1" />,<fnref n="2" />, Clara Saleri†<fnref n="1" /> and David Thura†<fnref n="1" />

Correspondence: clara.saleri@inserm.fr or david.thura@inserm.fr

## Abstract

Stereotypies, defined as repetitive behaviors with no apparent purpose, are frequent in some animals kept in captivity, posing a major ethical and scientific challenge for biomedical research involving animals for scientific purposes. This article describes the case of a rhesus macaque who tends to express marked stereotypies when temporarily separated from his partner. In an attempt to improve the animal's condition during these short periods of separation, the impact of exposure to a video of his partner was tested. This video was shown to the animal during five experimental sessions, and the animal's behavior was analyzed using BORIS software, which quantifies the duration of stereotypies. The results indicate an immediate and significant reduction in stereotypic behaviors when the animal is first exposed to the video of his partner during her absence. However, a gradual return of stereotypies is observed during subsequent exposures, suggesting habituation to the visual enrichment offered. A lasting improvement in well-being through social visual enrichment is therefore not observed for this animal. These data are discussed in light of the specificity of the protocol used, the factors that may have interfered with its effectiveness, and the profile of the animal in question.

## Keywords

welfare, refinement, monotony, desensitization

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<footnote n="1">¹Centre de Recherche en Neurosciences de Lyon, équipe ImpAct - Université Claude Bernard Lyon 1, INSERM U1028, CNRS UMR5292 (Bron, France)</footnote>

<footnote n="2">²VetAgro Sup (Marcy-l'Étoile, France)</footnote>

<footnote>* These authors contributed equally to this work</footnote>

<footnote>† These authors contributed equally to the design and coordination of this study</footnote>
## Introduction

Nonhuman primates involved in biomedical research come from licensed breeders and are therefore born in captivity. Laboratory conditions provide a controlled environment, with constant temperature and humidity regulation, as well as a diet adapted to their physiological needs. Furthermore, these animals are now frequently housed in social groups in large enclosures, facilitating the expression of a wide range of their natural behavioral repertoire. These conditions contribute to a theoretically increased longevity of laboratory animals compared to their counterparts living in their natural environment (1).

Despite these positive aspects, a significant percentage of captive nonhuman primates may develop stereotypical behaviors (2,3), defined as repetitive and purposeless actions (4) and considered as signs of psychological distress. According to Broom (5), these behaviors become alarming when they occupy more than 10% of the animals' time.

Stereotypies and other compulsive disorders pose significant ethical and scientific challenges for those involved in biomedical research using animals for scientific purposes. On the one hand, suffering in animals is now seen as unacceptable in scientific research and calls for continuous improvements in their care and treatment. This suffering also impacts the well-being of the personnel involved in the conduct of this research, people who can develop "compassion fatigue" with significant societal impact (6,7). On the other hand, they compromise the scientific validity of the results obtained because chronic stress influences biological and behavioral responses, thus altering data quality and their reproducibility (8,9).

Approaches to alleviate psychological suffering in laboratory animals generally rely on various forms of environmental enrichment (10–12). A few studies have explored the effect of video enrichments on non-human primates (13–16). For example, Meunier et al. (14) showed that audiovisual stimuli could be useful in reducing certain stereotypical behaviors in monkeys housed individually, but that their impact remained partial, with some stereotypies persisting despite this. Platt and Novak (16) showed that videos including social scenes could be an appropriate means of promoting the welfare of captive rhesus macaques. However, to our knowledge, no study has yet explored the impact of personalized social videos, featuring familiar individuals or those specifically belonging to the social group of monkeys to which they are presented.

In this case study, we tested the impact of this type of socially-oriented and personalized visual enrichment on the stereotypic behaviors of an adult male rhesus macaque. For approximately one year and a half, this monkey expressed pronounced stereotypic behaviors when temporarily deprived of contact with his housing partner while she left their enclosure to participate in cognitive neuroscience experimental protocols. These manifestations, characteristic of discomfort related to social separation (17), motivated the implementation of a visual enrichment protocol based on the broadcasting of a video of his partner during these short periods of separation (see Supplementary material, section #1 for the reflection of the Animal Welfare Body (AWB) on the case of monkey N).

## Results

This case study aimed to determine whether visual enrichment based on the presentation of a socially personalized video can reduce stereotypic behavior in a rhesus macaque, monkey N, during periods of temporary separation from his partner, monkey G.

Monkey N's was filmed (Figure 1) in the presence of his partner (reference condition), when his partner was absent and without video enrichment, or when his partner was absent and the video of her was presented. His behavior was analyzed offline and categorized into two main types: non-stereotyped (e.g., locomotion, feeding, social interactions, vigilance, environmental observation, foraging, rest, grooming) and stereotyped or stress-related.

### Behavior of monkey N in the presence of his partner
The behavior of monkey N in the presence of monkey G was analyzed to establish a baseline measure of his time budget. These observations were conducted over three sessions (averaging 52 minutes), each on a separate day. Our analyses show that monkey N's behavior does not show any clear signs of distress. For example, he spends approximately 20% of his time expressing positive social behavior directed toward his partner. He nevertheless exhibits some stereotypical behaviors, primarily rocking and rubbing movements, which represent less than 4 ± 3% of the total observation time. Furthermore, he frequently adopts a posture of vigilance and/or observation of the environment (32 ± 6% of the time budget) (Figure 2A).

## Behavior of monkey N in the absence of his partner

We then examined monkey N's behavior in the absence of his partner and without visual enrichment. This condition corresponded to the context in which stereotypic behaviors appeared most pronounced and for which this study was initiated.

Behavioral analysis was based on three observation sessions (with an average duration of 17 minutes), each conducted on a different day. As expected, the results show a high proportion (77 ± 5%) of stereotypic behaviors expressed by monkey N when separated from his housing partner (Figure 2B). Rocking represents the majority (89 ± 4%) of the stereotypic behaviors observed in this condition, followed by finger rubbing on the cage bars (11 ± 5%). Consequently, non-stereotypic behaviors are significantly reduced compared to the condition where his partner is present. Overall, these observations confirm a marked state of stress, strongly accentuated (from ~4% to 77% of the total observation time) by social separation.

## In the absence of his partner and with visual enrichment

In an attempt to overcome this problem of increased stress expressed by monkey N when separated from his partner, we presented him with a video of her on a screen placed in front of the cage (Figure 1) and analyzed his behavior during 5 sessions (with an average duration of 22 minutes) spread over 5 different days.

The results show a strong reduction in stereotypic behaviors such as body rocking and finger rubbing in the presence of the video stimulus, while no pacing behavior is observed (when he is in the upper part of the cage and is therefore visible on the videos). The presentation of this enrichment leads on average to a decrease of 42 points in the proportion of time spent on stereotypic behaviors, dropping from 77 ± 5% to 35 ± 12% of the total time budget (Figure 2C).

Nevertheless, it is important to note the evolution of the time devoted to stereotypical movements during the five sessions during which monkey N was exposed to video enrichment. Indeed, during the first session, these behaviors represented less than 2% of the time budget. The proportion of stereotypical behaviors then increased progressively during the following sessions, reaching 75% of the time budget during the fifth session (Figure 2D). By contrast, the time spent observing the video overall decreased across sessions (from 38% to 6% of the time budget) and non-stereotypic behaviors showed a marked decline (from 61% to 18%). A negative correlation between stereotypic and non-stereotypic behaviors (r = -0.97, p<0.01) highlights this behavioral shift, with the animal progressively allocating more time to stereotypies while reducing other behaviors.

## Discussion

The case study described in this article aimed to evaluate the effectiveness of visual enrichment on reducing stereotypic behaviors in an anxious rhesus macaque. Unlike conventional enrichment approaches, including those based on video broadcasting (14,16), this protocol is distinguished by the use of social and personalized stimuli. The results indicate an immediate and significant reduction in stereotypic behaviors in the animal studied in the presence of visual enrichment. However, this effect does not persist over time. The lasting improvement in apparent well-being through social visual enrichment is therefore not observed for this animal. This finding is discussed in relation to the specific type of visual enrichment used, the individual personality traits of the animal in question, and other
contextual factors that may have interfered with its effectiveness. Indeed, it's important to mention that these observations were made outside of a dedicated experimental protocol, with the primary aim of improving this monkey's welfare during the regular activities of the laboratory in which he is housed.

## Effect of video type presented

The main finding of this study concerns the initial positive impact of social visual enrichment, which gradually dissipates over the five testing sessions (Figure 2D). One possible explanation for this effect is the monotony of the content presented to monkey N, which may have led to rapid habituation and, consequently, a decrease in the expected calming effect. Platt and Novak (16) also showed that monkeys' interest in the videos gradually decreased with repeated exposure, supporting the idea of a habituation phenomenon. This first attempt to reduce stress by showing social video stimuli consisted of showing the animal a single film featuring his partner. The striking results observed during the first testing session would encourage modification of the protocol to offer the monkey videos of his partner that varied from day to day.

Another observation was conducted in this regard by presenting monkey N with a video of unfamiliar macaques in their natural habitat during one of his partner's absences. The aim was to explore whether visual stimulation featuring non-familiar individuals could capture his attention and help reduce his stereotypic behaviors. No quantitative data were collected for this observation. However, it was visually noted that monkey N did not show any particular interest in the video. His behavior remained unchanged, and he continued to perform his usual stereotypic movements without displaying any signs of calming. This observation highlights the importance of considering individual differences in animals' responses to enrichment (18).

## Impact of the physical and social environment of captive animals

Many other factors that we were not necessarily able to control may have intervened and potentially impacted the effectiveness of the attempt to reduce stress through personalized visual and social enrichment.

For example, monkey N and monkey G do not live in housing isolated from the rest of the animal facility, but in visual and sound contact with other enclosures in which six other animals are living, also being required to leave their housing for the performance of cognitive neuroscience behavioral tests. During the outings of two other monkeys housed in adjacent enclosures, it has been noticed that monkey N vocalizes more than when all the monkeys are present in their respective enclosures. Although there is no increase in stereotypic behaviors, he presents a state of heightened vigilance. These observations nevertheless indicate that monkey N's behavior is sensitive to the social balance of his entire environment. This sensitivity to the broader social dynamics of his environment may have interfered with the effectiveness of the video-based enrichment. Indeed, the removal of the different animals from the animal facility represents a potential confounding factor that was not controlled in this case study.

Moreover, we observed that monkey N spent less time performing stereotypic behaviors when alone in his home enclosure compared to the reduced space (Supplementary material, section #2). Although this observation is based on a single experimental session, it suggests, as expected, that a familiar physical environment has a positive impact on the animal's well-being. However, Kaufman et al. (19) reported that placing animals in larger cages does not necessarily guarantee a reduction in stereotypic behaviors. In our specific case, keeping monkey N in the home enclosure during separation periods presents other challenges: being closer to the experimental room where his partner is 'working', his frequent vocalizations tend to disrupt her experimental sessions.

## Monkey N's personality

In the context of a case study, it is important to remember that the results described here are specific to the animal studied and are therefore not necessarily generalizable to other animals housed in a laboratory. Monkey N is a relatively old monkey who has exhibited stereotypical behaviors for several years during periods when he is isolated from a partner for short periods of time. It is possible that the
declining effectiveness of visual social enrichment reported above would not have been observed in an animal displaying less pronounced stereotypies (occupying about 75% of his time budget when alone, see Figure 2B) and/or more recent distress. Furthermore, male macaques appear to be more affected than females in the expression of stereotypies in captive individuals (17,20). It would therefore be interesting to test the effectiveness of social, video-based enrichment on both female and male captive monkeys in future experiments to more exhaustively assess its efficiency. Future approaches could also involve more interactive forms of enrichment, such as simple tasks on a mobile lab or manipulable puzzles (21). We hypothesize that active engagement, rather than passive observation, may help reduce stereotypic behaviors by focusing the animal's attention on alternative activities. Nevertheless, considering his elevated stress level, it is plausible that monkey N would have ignored such enrichment.

## Conclusions

Previous studies have not demonstrated a clear effect of video enrichment on reducing stereotypies (14,16). Similarly, we observed that the use of social and personalized video stimuli as enrichment did not sustainably reduce the production of stereotypical behaviors. As this case study was primarily qualitative and not designed for quantitative testing, further controlled experiments on a larger sample are needed to conclusively determine its effectiveness and to specifically assess the impact of personalization by comparing responses to videos featuring familiar versus unfamiliar macaques.
<figure><img src="image_4.png" /><figcaption>**Figure 1: Experimental setup.** During monkey G's testing periods, monkey N is temporally placed in an Allentown-type cage, and the screen displaying the video of monkey G is positioned in front of him. A camera, placed opposite, records his behavior (but only films the upper level of the cage).</figcaption></figure>
<figure><img src="image_5.png" /><figcaption>B</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>C</figcaption></figure>

<figure><img src="image_7.png" /><figcaption>D</figcaption></figure>

<figure><img src="image_8.png" /></figure>

**Figure 2:** Behavior of monkey N in the three conditions (with his partner, without her and without video enrichment and without her and with the video enrichment) in the reduced space. A: Time budget distribution of monkey N in the presence of his partner. Stereotypical behaviors (pacing, body rocking, finger rubbing) are highlighted in red. B: Same as A but in the absence of his partner and without video enrichment. C: Same as B with video enrichment. D: Evolution of the percentage of time budget that monkey N devoted to stereotyped movements, looking at the video and other non-stereotypical behaviors across sessions in which social visual enrichment was provided. The red bars represent the proportion of time budget allocated to stereotypies during the sessions in which the video was shown to monkey N during separation periods from his partner, grey bars indicate the proportion of time spent watching the video enrichment and green ones correspond to all other behaviors pooled together.
## Acknowledgements

The authors would like to warmly thank Gislène Gardechaux, Michel Filiptchenko, and Manon Dirheimer for their daily care of the animals in our animal facility. David Thura's work is funded by an ATIP/Avenir grant from the CNRS and Inserm, and by funds from the French National Research Agency (ANR-22-CE37-0010-02/BasalCost).

## Authors contributions

- Conceptualization: NL, MP, CS and DT

- Data curation: NL and MP

- Formal analysis: NL and MP

- Funding acquisition: DT

- Methodology: NL, MP, CS and DT

- Supervision: CS and DT

- Writing – original draft: NL, MP, CS and DT

- Writing – review & editing: NL, MP, CS and DT

## Ethics approval

The data presented in this article were collected on the margins of an ethically approved protocol. Monkey N is not directly involved in an experimental project, but his housing partner is. Her brief daily absences from their enclosure result in observable signs of stress in monkey N. This observation prompted discussions within the Animal Welfare Body of the laboratory in which monkey N is housed and, as a result, the protocol described in this paper was proposed and approved as a means of reducing this temporary stress (Supplementary material, section #1).

## Data availability statement

All datasets generated and analysed in this study are provided in the accompanying Excel file ("Data Tables," comprising seven worksheets). Worksheets 1–4 contain the data underlying Figure 2A–D of the main text (ie "In the Allentown"), and Worksheets 5–7 contain the data underlying Figure S1B in the Supplementary Materials (ie "Regular enclosure"). These datasets can also be accessed via the following online repository: https://share.inserm.fr/index.php/s/S9YgqZdH9XpT2CD

## Supporting information and files

- Supplementary Figure 1 (SupFig.1): Enlarged image presented Figure 1.

- Supplementary Figure 2 (SupFig.2): High-resolution diagrammes presented Figure 2.

- Supplementary Material Section #1 (S#1) and Section #2 (S#2):

- S#1: Reflection of the Animal Welfare Body (AWB) on the case of monkey N.

- S#2: Impact of enclosure size on monkey N's behavior and on the effectiveness of the visual enrichment (Figure S1 A-B).

- Supplementary Table 1: Excel file containing all datasets generated and analyzed in this study.
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# Materials and Methods

## Subject and context of the study

The subject of this study is monkey N, a castrated male rhesus macaque (*Macaca mulatta*), 14 years old and weighing 12 kg at the time of the observations. This macaque has been living in a pair with a female rhesus macaque (monkey G) for 3 years. Monkey N has had his left arm amputated since childhood, following an attack by an adult male congener.

As part of the research conducted in the neuroscience laboratory in which they are housed, the monkeys are required to leave their enclosure daily to enter a room dedicated to experimental sessions. Although monkey N is not directly involved in a protocol, monkey G is. Monkey N therefore finds himself alone in his enclosure for short periods of time (on average one hour per day, mainly in the morning). However, he is never completely isolated, as he is in a housing room with six other monkeys in neighboring enclosures.

Nevertheless, despite the routine nature of the situation for monkey N, it systematically triggers a reaction in this animal, including stereotypies such as pacing, repeated body rocking, or repeated rubbing of his finger against one of the cage walls. These behaviors persist despite the provision of "classic" enrichment (swings, food burying elements, etc.) and may be accompanied by displays of aggression, whether directed towards the observer (threats) or self-directed, such as biting his arm. These problematic behaviors stop as soon as monkey G returns in their enclosure and joins monkey N.

Despite the very temporary nature of these periods of stress, this observation has motivated reflections within the Animal Welfare Body in the laboratory in which monkey N is housed, and the protocol described in the present paper has been proposed and validated as a means of reducing this temporary stress (Supplementary material, section #1).

## Housing conditions

During the separation periods covered by this study, monkey N was placed in an Allentown-type cage. This cage, with a volume of approximately 4 m³, allowed experimenters to transfer monkey G from her enclosure to her primate chair, where she performed the tests in a dedicated experimental room. Monkey N accompanied her partner into this reduced space upon her exit and remained there until her return, thereby allowing animal care staff to perform routine cleaning in their housing enclosure. This cage was divided into two levels, offering the monkey the option of moving either in the lower or upper section, depending on his preference.

To control for the impact of this reduced space on monkey N's behavior and on the effectiveness of the proposed visual enrichment, we also conducted the tests when monkey N was returned to his housing enclosure after his partner's departure (Supplementary material, section #2). The enclosure and the Allentown-type cage were located in the same room. Therefore, these two conditions are subject to the same environmental parameters, such as noise, temperature, humidity, lighting, and the presence of conspecifics from other enclosures.

During these sessions, monkey N receives his daily food ration consisting of 20 kibbles (Osafe, complete food for non-human primates) accompanied by a vegetable and a fruit. This feeding routine aims to minimize stress factors and promote a reduction in his anxiety.

## Experimental design and enrichment used

For this case study, several video sequences of monkey G (monkey N's partner) in her enclosure were filmed at different times of the day and over several days. These sequences were assembled using an editing software (DaVinci Resolve, Blackmagic Design) to produce a single video file lasting 45 minutes. This video enrichment was played continuously to monkey N on a 17.3-inch monitor, without sound, during periods when he was separated from his partner. The monitor was placed about 20 centimeters from the cage so that he could not touch or grab it (Figure 1).
## Tested conditions

Monkey N's behavior (with or without visual enrichment) was analyzed from video recordings to avoid any interference related to live observations. The recordings began when monkey G leaved the housing room.

The conditions during which monkey N was filmed in the Allentown-type cage were as follows: a reference condition, in the presence of monkey G, for which three sessions were filmed, totaling 132 minutes of observation. A "partner absent/video enrichment absent" condition included three filmed sessions, for a total of 69 minutes of observation. A "partner absent/video enrichment present" condition included five filmed sessions, for a total duration of 144 minutes. However, since monkey N sometimes moved in the lower part of the cage (22% of the time on average), making him invisible in the videos, we analyzed only the periods when he was visible, i.e., 54 and 132 minutes respectively for the two test conditions described above.

## Identification and quantification of Monkey N's behaviors

The macaque ethogram (adapted from Akongo, https://www.akongo.fr and (22)) used to describe the behavioral repertoire of monkey N distinguishes two main categories of behavior: non-stereotyped behaviors (including movement, feeding behaviors, positive and negative social interactions, observer-directed behaviors, vigilance and/or observation of the environment, foraging exploration, resting, grooming behaviors and, when applicable, looking at the video-enrichment) and stereotyped or stress-related behaviors (see Table 1 for more details). The specific stereotypies of monkey N have been characterized as described in (22) and the main ones which are therefore the subject of the present study are: pacing (stereotypic movement), rocking the body back and forth, and rubbing the finger against the cage walls. Monkey N's behaviors were quantified using Behavioral Observation Research Interactive Software (BORIS), version 8.27.1 (https://www.boris.unito.it/), which enabled the creation of time budgets for the behaviors observed under each experimental condition.

For all conditions, the details of the time budgets allocated to non-stereotypic behaviors are presented.

The three types of stereotypies mentioned above (pacing, repetitive body rocking, and repeated finger rubbing) were identified and quantified from the video recordings described above. These parameters are measured in relative duration compared to the time monkey N was visible in the videos (percentage of the time budget). These data were extracted systematically, by reviewing all available video footage of monkey N, enabling a detailed analysis of behavioral variation across experimental conditions.

<table><caption>Table 1: List of behavioral categories and definitions used for scoring. Adapted from Akongo, https://www.akongo.fr and (22)</caption><thead><tr><td>Behavior</td><td>Description</td></tr></thead><tbody><tr><td>Maintenance behaviors</td><td>Grooms or scratches (parts fur, inspects skin, brings particles to the mouth)</td></tr><tr><td>Positive social behaviors</td><td>Social resting, grooming, lipsmacking</td></tr><tr><td>Exploration (foraging)</td><td>Searches the substrate with hands or feet for food (foraging)</td></tr><tr><td>Food-related behaviors</td><td>Drinks, handles food (or a food-containing object), eats</td></tr><tr><td>Movement, locomotion</td><td>Walks, runs, climbs or jumps</td></tr><tr><td>Rest</td><td>Inactive, sitting or lying down, relaxed posture</td></tr><tr><td>Vigilance, observation</td><td>Observes the environment or conspecifics (in a relaxed or alert posture)</td></tr><tr><td>Look at the video</td><td>Directs his gaze toward the screen displaying the video enrichment, maintaining visual attention for at least one second</td></tr><tr><td>Pacing</td><td>Walking back and forth or in a circular pattern, for at least three repetitions or 5 or more seconds</td></tr><tr><td>Body rocking</td><td>Rhythmic back-and-forth movement of the upper body, typically performed while sitting, for at least three repetitions or 5 or more seconds</td></tr><tr><td>Finger rubbing</td><td>Repetitive rubbing of one or more fingers against the cage walls or other surfaces, for at least three repetitions or 5 or more seconds</td></tr></tbody></table>
## Data analysis and processing

The proportions of time allocated to stereotypic behaviors (pacing, body rocking, and finger rubbing) were compared between sessions with visual enrichment (i.e., in the presence of the partner's video) and those without enrichment. We also examined the persistence of stereotypic behaviors across enrichment sessions and the time allocated to watching at the video-enrichment and to other non-stereotypic behaviors. This allowed us to assess the effectiveness of this type of enrichment in reducing stereotypies, and to detect potential habituation to the stimulus.

As the present article describes a case study with a limited number of sessions per condition, no statistical tests comparing conditions were conducted, but a Pearson correlation (with a level of significance fixed at 0.05) was performed to assess behavioral evolution across sessions with visual enrichment. Intersession variability is indicated with standard deviations around mean values.