A Touchscreen-Based, Multiple-Choice Approach to Cognitive Enrichment of Captive Rhesus Macaques (Macaca mulatta).

Research on the psychological and physiological well-being of captive animals has focused on investigating different types of social and structural enrichment. Consequently, cognitive enrichment has been understudied, despite the promising external validity, comparability, and applicability. As we aim to fill this gap, we developed an interactive, multiple-choice interface for cage-mounted touchscreen devices that rhesus monkeys (Macaca mulatta) can freely interact with, from within their home enclosure at the Cognitive Neuroscience Laboratory of the German Primate Center. The multiple-choice interface offers interchangeable activities that animals can choose and switch between. We found that all 16 captive rhesus macaques tested consistently engaged with the multiple-choice interface across 6 weekly sessions, with 11 of them exhibiting clear task preferences, and displaying proficiency in performing the selected tasks. Our approach does not require social separation or dietary restriction and is intended to increase animals' sense of competence and agency by providing them with more control over their environment. Thanks to the high level of automation, our multiple-choice interface can be easily incorporated as a standard cognitive enrichment practice across different facilities and institutes working with captive animals, particularly non-human primates. We believe that the multiple-choice interface is a sustainable, scalable, and pragmatic protocol for enhancing cognitive well-being and animal welfare in captivity.

Home-Enclosure-Based Behavioral and Wireless Neural Recording Setup for Unrestrained Rhesus Macaques.

Electrophysiological studies with behaving nonhuman primates often require the separation of animals from their social group as well as partial movement restraint to perform well-controlled experiments. When the research goal per se does not mandate constraining the animals' movements, there are often still experimental needs imposed by tethered data acquisition. Recent technological advances meanwhile allow wireless neurophysiological recordings at high band-width in limited-size enclosures. Here, we demonstrate wireless neural recordings at single unit resolution from unrestrained rhesus macaques while they performed self-paced, structured visuomotor tasks on our custom-built, stand-alone touchscreen system [eXperimental Behavioral Instrument (XBI)] in their home environment. We were able to successfully characterize neural tuning to task parameters, such as visuo-spatial selectivity during movement planning and execution, as expected from existing findings obtained via setup-based neurophysiology recordings. We conclude that when movement restraint and/or a highly controlled, insulated environment are not necessary for scientific reasons, cage-based wireless neural recordings are a viable option. We propose an approach that allows the animals to engage in a self-paced manner with our XBI device, both for fully automatized training and cognitive testing, as well as neural data acquisition in their familiar environment, maintaining auditory and sometimes visual contact with their conspecifics.

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

In recent years, the utility and efficiency of automated procedures for cognitive assessment in psychology and neuroscience have been demonstrated in non-human primates (NHP). This approach mimics conventional shaping principles of breaking down a final desired behavior into smaller components that can be trained in a staircase manner. When combined with home-cage-based approaches, this could lead to a reduction in human workload, enhancement in data quality, and improvement in animal welfare. However, to our knowledge, there are no reported attempts to develop automated training and testing protocols for long-tailed macaques (Macaca fascicularis), a ubiquitous NHP model in neuroscience and pharmaceutical research. In the current work, we present the results from 6 long-tailed macaques that were trained using an automated unsupervised training (AUT) protocol for introducing the animals to the basics of a two-alternative choice (2 AC) task where they had to discriminate a conspecific vocalization from a pure tone relying on images presented on a touchscreen to report their response. We found that animals (1) consistently engaged with the device across several months; (2) interacted in bouts of high engagement; (3) alternated peacefully to interact with the device; and (4) smoothly ascended from step to step in the visually guided section of the procedure, in line with previous results from other NHPs. However, we also found (5) that animals' performance remained at chance level as soon as the acoustically guided steps were reached; and (6) that the engagement level decreased significantly with decreasing performance during the transition from visual to acoustic-guided sections. We conclude that with an autonomous approach, it is possible to train long-tailed macaques in their social group using computer vision techniques and without dietary restriction to solve a visually guided discrimination task but not an acoustically guided task. We provide suggestions on what future attempts could take into consideration to instruct acoustically guided discrimination tasks successfully.

Assessing cognitive flexibility in humans and rhesus macaques with visual motion and neutral distractors.

Introduction: Cognitive flexibility is the ability of an individual to make behavioral adjustments in response to internal and/or external changes. While it has been reported in a wide variety of species, established paradigms to assess cognitive flexibility vary between humans and non-human animals, making systematic comparisons difficult to interpret. Methods: We developed a computer-based paradigm to assess cognitive flexibility in humans and non-human primates. Our paradigm (1) uses a classical reversal learning structure in combination with a set-shifting approach (4 stimuli and 3 rules) to assess flexibility at various levels; (2) it employs the use of motion as one of three possible contextual rules; (3) it comprises elements that allow a foraging-like and random interaction, i.e., instances where the animals operate the task without following a strategy, to potentially minimize frustration in favor of a more positive engagement. Results and Discussion: We show that motion can be used as a feature dimension (in addition to commonly used shape and color) to assess cognitive flexibility. Due to the way motion is processed in the primate brain, we argue that this dimension is an ideal candidate in situations where a non-binary rule set is needed and where participants might not be able to fully grasp other visual information of the stimulus (e.g., quantity in Wisconsin Card Sorting Test). All participants in our experiment flexibly shifted to and from motion-based rules as well as color- and shape-based rules, but did so with different proficiencies. Overall, we believe that with such approach it is possible to better characterize the evolution of cognitive flexibility in primates, as well as to develop more efficient tools to diagnose and treat various executive function deficits.

Sustained spatial attention accounts for the direction bias of human microsaccades.

Small ballistic eye movements, so called microsaccades, occur even while foveating an object. Previous studies using covert attention tasks have shown that shortly after a symbolic spatial cue, specifying a behaviorally relevant location, microsaccades tend to be directed toward the cued location. This suggests that microsaccades can serve as an index for the covert orientation of spatial attention. However, this hypothesis faces two major challenges: First, effects associated with visual spatial attention are hard to distinguish from those that associated with the contemplation of foveating a peripheral stimulus. Second, it is less clear whether endogenously sustained attention alone can bias microsaccade directions without a spatial cue on each trial. To address the first issue, we investigated the direction of microsaccades in human subjects while they attended to a behaviorally relevant location and prepared a response eye movement either toward or away from this location. We find that directions of microsaccades are biased toward the attended location rather than towards the saccade target. To tackle the second issue, we verbally indicated the location to attend before the start of each block of trials, to exclude potential visual cue-specific effects on microsaccades. Our results indicate that sustained spatial attention alone reliably produces the microsaccade direction effect. Overall, our findings demonstrate that sustained spatial attention alone, even in the absence of saccade planning or a spatial cue, is sufficient to explain the direction bias observed in microsaccades.