Flexible auditory training, psychophysics, and enrichment of common marmosets with an automated, touchscreen-based system

Abstract

Devising new and more efficient protocols to analyze the phenotypes of non-human primates, as well as their complex nervous systems, is rapidly becoming of paramount importance. This is because with genome-editing techniques, recently adopted to non-human primates, new animal models for fundamental and translational research have been established. One aspect in particular, namely cognitive hearing, has been difficult to assess compared to visual cognition. To address this, we devised autonomous, standardized, and unsupervised training and testing of auditory capabilities of common marmosets with a cage-based standalone, wireless system. All marmosets tested voluntarily operated the device on a daily basis and went from naïve to experienced at their own pace and with ease. Through a series of experiments, here we show, that animals autonomously learn to associate sounds with images; to flexibly discriminate sounds, and to detect sounds of varying loudness. The developed platform and training principles combine in-cage training of common marmosets for cognitive and psychoacoustic assessment with an enriched environment that does not rely on dietary restriction or social separation, in compliance with the 3Rs principle.

Group-based, autonomous, individualized training and testing of long-tailed macaques (Macaca fascicularis) in their home enclosure to a visuo-acoustic discrimination task

“…In this study, we adapted a visuo-acoustic automated unsupervised training protocol (AUT) we previously used to train marmoset monkeys ( Calapai et al, 2022 ). Here, 5 long-tailed macaques belonging to 2 groups underwent an AUT comprised 49 training steps.…”

“…Specifically, it shared the structural design of the apparatus described for Rhesus macaques (Berger et al, 2018) while replacing costly hardware (Apple computers) with an open-source system (Raspberry Pi computers), allowing for more straightforward modification and expansion of the system by others. It additionally used a visuo-acoustic protocol developed for common marmosets Frontiers in Psychology 09 frontiersin.org (Calapai et al, 2022). Furthermore, our protocol relies on computer vision technology for the identification of subjects on a trial basis, which could, in principle, allow for testing subjects in natural settings.…”

“…Therefore, we would like to argue that the optimization of training protocols has the potential to enhance animal welfare while increasing the standardization of training and ultimately broadening the scope of scientific research. Toward such aims, several studies have already reported various optimization of behavioral training ( Calapai et al, 2017 , 2022 ; Berger et al, 2018 ; Butler and Kennerley, 2019 ; Walker et al, 2019 ; Sacchetti et al, 2021 ) across two important NHP models used in neuroscience, rhesus macaques ( Macaca mulatta ), and common marmosets ( Callithrix jacchus ). However, to the best of our knowledge, there is a lack of reported attempts to develop automated training and testing protocols for long-tailed macaques ( Macaca fascicularis ), a ubiquitous NHP model in neuroscience and—in particular—pharmaceutical research.…”

Development of a new 3D tracking system for multiple marmosets under free-moving conditions

“…This system would be able to accurately quantify the behavior of marmosets throughout their lives to discover behavioral changes before and after the onset of diseases, even at an extremely early stage. Recently Calapai et al reported a new touch screen based cognitive auditory analysis system that allows marmosets to perform tasks in a free moving environment in the paired home cage 44 . By incorporating such a freely operable cognitive function task device into our system, it is possible to provide a behavior analysis system that comprehensively and continuously analyzes the marmoset's natural behavior, activity, and cognitive functions without stress.…”

Evaluating Cognitive Enrichment for Zoo-Housed Gorillas Using Facial Recognition

“…The collection of these data can be automated using radio frequency identification (RFID) tags. RFID tags are worn on a collar or implanted into the skin and have been used to monitor several laboratory primate species, such as rhesus macaques ( Macaca mulatta ) ( 17 ); common marmosets ( Callithrix jacchus ) ( 18 ); guinea baboons ( Papio papio ) ( 19 , 20 ). However, there are several reasons why this approach may be deemed unsuitable.…”