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Executive function (EF) is a complex construct that reflects multiple higher-order cognitive processes such as planning, updating, inhibiting and set-shifting. Decline in these functions is a hallmark of cognitive ageing in humans, and age differences and changes in EF correlate with age-related differences and changes in association cortices, particularly the prefrontal areas. Here, we review evidence for age-related decline in EF and associated neurobiological changes in prosimians, New World and Old World monkeys, apes and humans. While EF declines with age in all primate species studied, the relationship of this decline with age-related alterations in the prefrontal cortex remains unclear, owing to the scarcity of neurobiological studies focusing on the ageing brain in most primate species. In addition, the influence of sex, vascular and metabolic risk, and hormonal status has rarely been considered. We outline several methodological limitations and challenges with the goal of producing a comprehensive integration of cognitive and neurobiological data across species and elucidating how ageing shapes neurocognitive trajectories in primates with different life histories, lifespans and brain architectures. Such comparative investigations are critical for fostering translational research and understanding healthy and pathological ageing in our own species. This article is part of the theme issue ‘Evolution of the primate ageing process’.

The claustrum and the insula are closely juxtaposed in the brain of the prosimian primate, the gray mouse lemur (Microcebus murinus). Whether the claustrum has closer affinities with the cortex or the striatum has been debated for many decades. Our observation of histological sections from primate brains and genomic data in the mouse suggest former. Given this, the present study compares the connections of the two structures in Microcebus using high angular resolution diffusion imaging (HARDI, with 72 directions), with a very small voxel size (90 micra), and probabilistic fiber tractography. High angular and spatial resolution diffusion imaging is non-destructive, requires no surgical interventions, and the connection of each and every voxel can be mapped, whereas in conventional tract tracer studies only a few specific injection sites can be assayed. Our data indicate that despite the high genetic and spatial affinities between the two structures, their connectivity patterns are very different. The claustrum connects with many cortical areas and the olfactory bulb; its strongest probabilistic connections are with the entorhinal cortex, suggesting that the claustrum may have a role in spatial memory and navigation. By contrast, the insula connects with many subcortical areas, including the brainstem and thalamic structures involved in taste and visceral feelings. Overall, the connections of the Microcebus claustrum and insula are similar to those of the rodents, cat, macaque, and human, validating our results. The insula in the Microcebus connects with the dorsolateral frontal cortex in contrast to the mouse insula, which has stronger connections with the ventromedial frontal lobe, yet this is consistent with the dorsolateral expansion of the frontal cortex in primates. In addition to revealing the connectivity patterns of the Microcebus brain, our study demonstrates that HARDI, at high resolutions, can be a valuable tool for mapping fiber pathways for multiple sites in fixed brains in rare and difficult-to-obtain species.

Mouse lemurs Microcebus spp. are small, nocturnal primates endemic to Madagascar. The genus is extraordinarily diverse, with 25 extant species, several of which have been described recently. The Endangered Claire's mouse lemur Microcebus mamiratra was first described in 2006, but, similarly to other newly described mouse lemurs, remains understudied, and estimates of its population size are unavailable, hampering effective conservation management. We conducted line transect distance sampling surveys of M. mamiratra across several habitat types in and around Lokobe National Park on the island of Nosy Be in north-western Madagascar. Using a systematic random design we surveyed 15 transects over a 6-week period in 2023, recording 92 detections from a total survey effort of 46.5 km. We estimate the density of M. mamiratra on Nosy Be to be 125.1 individuals/km2, which extrapolates to an estimate of c. 4,700 individuals across the forested areas of its range on the island. Our results indicate that Nosy Be harbours moderately high densities of M. mamiratra, with the highest encounter rates in the unprotected secondary and degraded forests around Lokobe National Park. Our population estimate will inform future conservation status assessments and conservation planning for this range-restricted species and provide a baseline for monitoring population changes over time. We present recommendations for the conservation of M. mamiratra and highlight the potential for lemur watching, sustained by the strong tourism industry on Nosy Be, to help protect lemur habitat and generate economic opportunities for local communities.

Systematic genetic studies of a handful of diverse organisms over the past 50 years have transformed our understanding of biology. However, many aspects of primate biology, behavior, and disease are absent or poorly modeled in any of the current genetic model organisms including mice. We surveyed the animal kingdom to find other animals with advantages similar to mice that might better exemplify primate biology, and identified mouse lemurs (Microcebus spp.) as the outstanding candidate. Mouse lemurs are prosimian primates, roughly half the genetic distance between mice and humans. They are the smallest, fastest developing, and among the most prolific and abundant primates in the world, distributed throughout the island of Madagascar, many in separate breeding populations due to habitat destruction. Their physiology, behavior, and phylogeny have been studied for decades in laboratory colonies in Europe and in field studies in Malagasy rainforests, and a high quality reference genome sequence has recently been completed. To initiate a classical genetic approach, we developed a deep phenotyping protocol and have screened hundreds of laboratory and wild mouse lemurs for interesting phenotypes and begun mapping the underlying mutations, in collaboration with leading mouse lemur biologists. We also seek to establish a mouse lemur gene “knockout” library by sequencing the genomes of thousands of mouse lemurs to identify null alleles in most genes from the large pool of natural genetic variants. As part of this effort, we have begun a citizen science project in which students across Madagascar explore the remarkable biology around their schools, including longitudinal studies of the local mouse lemurs. We hope this work spawns a new model organism and cultivates a deep genetic understanding of primate biology and health. We also hope it establishes a new and ethical method of genetics that bridges biological, behavioral, medical, and conservation disciplines, while providing an example of how hands-on science education can help transform developing countries.

The rodent visual system has attracted great interest in recent years due to its experimental tractability, but the fundamental mechanisms used by the mouse to represent the visual world remain unclear. In the primate, researchers have argued from both behavioral and neural evidence that a key step in visual representation is ‘figure-ground segmentation’, the delineation of figures as distinct from backgrounds. To determine if mice also show behavioral and neural signatures of figure-ground segmentation, we trained mice on a figure-ground segmentation task where figures were defined by gratings and naturalistic textures moving counterphase to the background. Unlike primates, mice were severely limited in their ability to segment figure from ground using the opponent motion cue, with segmentation behavior strongly dependent on the specific carrier pattern. Remarkably, when mice were forced to localize naturalistic patterns defined by opponent motion, they adopted a strategy of brute force memorization of texture patterns. In contrast, primates, including humans, macaques, and mouse lemurs, could readily segment figures independent of carrier pattern using the opponent motion cue. Consistent with mouse behavior, neural responses to the same stimuli recorded in mouse visual areas V1, RL, and LM also did not support texture-invariant segmentation of figures using opponent motion. Modeling revealed that the texture dependence of both the mouse’s behavior and neural responses could be explained by a feedforward neural network lacking explicit segmentation capabilities. These findings reveal a fundamental limitation in the ability of mice to segment visual objects compared to primates.

•Glutamate, a critical amino acid for the brain, can be detected by gluCEST imaging.•Whole brain gluCEST maps were recorded at high field (11.7T) MRI in a primate.•Regional differences of gluCEST contrast strongly reflect glutamate pathways.•gluCEST imaging highlights regional age-related alterations.•gluCEST imaging highlights age-related alterations in large-scale networks. Glutamate is the amino acid with the highest cerebral concentration. It plays a central role in brain metabolism. It is also the principal excitatory neurotransmitter in the brain and is involved in multiple cognitive functions. Alterations of the glutamatergic system may contribute to the pathophysiology of many neurological disorders. For example, changes of glutamate availability are reported in rodents and humans during Alzheimer's and Huntington's diseases, epilepsy as well as during aging. Most studies evaluating cerebral glutamate have used invasive or spectroscopy approaches focusing on specific brain areas. Chemical Exchange Saturation Transfer imaging of glutamate (gluCEST) is a recently developed imaging technique that can be used to study relative changes in glutamate distribution in the entire brain with higher sensitivity and at higher resolution than previous techniques. It thus has strong potential clinical applications to assess glutamate changes in the brain. High field is a key condition to perform gluCEST images with a meaningful signal to noise ratio. Thus, even if some studies started to evaluate gluCEST in humans, most studies focused on rodent models that can be imaged at high magnetic field. In particular, systematic characterization of gluCEST contrast distribution throughout the whole brain has never been performed in humans or non-human primates. Here, we characterized for the first time the distribution of the gluCEST contrast in the whole brain and in large-scale networks of mouse lemur primates at 11.7 Tesla. Because of its small size, this primate can be imaged in high magnetic field systems. It is widely studied as a model of cerebral aging or Alzheimer's disease. We observed high gluCEST contrast in cerebral regions such as the nucleus accumbens, septum, basal forebrain, cortical areas 24 and 25. Age-related alterations of this biomarker were detected in the nucleus accumbens, septum, basal forebrain, globus pallidus, hypophysis, cortical areas 24, 21, 6 and in olfactory bulbs. An age-related gluCEST contrast decrease was also detected in specific neuronal networks, such as fronto-temporal and evaluative limbic networks. These results outline regional differences of gluCEST contrast and strengthen its potential to provide new biomarkers of cerebral function in primates. [Display omitted]

•Mouse lemur, one of the smallest primates, was imaged with high field 11.7T MRI.•First functional atlas of mouse lemur brain.•First characterization of its brain networks and comparison with human networks.•High-level cortical networks of lemurs are not homologous to human ones.•Hubs are grouped in lemurs while they are split into clusters in humans. Measures of resting-state functional connectivity allow the description of neuronal networks in humans and provide a window on brain function in normal and pathological conditions. Characterizing neuronal networks in animals is complementary to studies in humans to understand how evolution has modelled network architecture. The mouse lemur (Microcebus murinus) is one of the smallest and more phylogenetically distant primates as compared to humans. Characterizing the functional organization of its brain is critical for scientists studying this primate as well as to add a link for comparative animal studies. Here, we created the first functional atlas of mouse lemur brain and describe for the first time its cerebral networks. They were classified as two primary cortical networks (somato-motor and visual), two high-level cortical networks (fronto-parietal and fronto-temporal) and two limbic networks (sensory-limbic and evaluative-limbic). Comparison of mouse lemur and human networks revealed similarities between mouse lemur high-level cortical networks and human networks as the dorsal attentional (DAN), executive control (ECN), and default-mode networks (DMN). These networks were however not homologous, possibly reflecting differential organization of high-level networks. Finally, cerebral hubs were evaluated. They were grouped along an antero-posterior axis in lemurs while they were split into parietal and frontal clusters in humans. [Display omitted]

Primates show a range of reproductive seasonality patterns, from year-round to strictly seasonal breeding. Seasonality depends on several factors, such as food availability, which dictates patterns of optimal and nonoptimal periods for reproduction, and is usually triggered by photoperiod in high latitudes. Photorefractoriness is a state of unresponsiveness to the prevailing photoperiod, characterized by spontaneous gonadal regression at the end of the breeding season and spontaneous anticipated gonadal development at the end of the resting season, preventing reproduction from occurring at the wrong time. Despite its importance in understanding primate reproductive physiology and adaptation to seasonal changes, photorefractoriness has been described in only one highly seasonal primate species so far: the gray mouse lemur (Microcebus murinus). In this study, we assessed the time required for male and female mouse lemurs to recover photosensitivity to short-day (SD) and long-day (LD) photoperiods. To test the recovery of photosensitivity to SD, we transferred 25 females and 40 males to SD after 4, 6, 8, 10, or 22 weeks in LD. To test the recovery of photosensitivity to LD, we applied the opposite protocol with 4, 6, 8, 10, or 14 weeks in SD. We monitored body mass, testosterone plasma levels and estrus every 2 weeks. We found that refractoriness in body mass lasted 10 weeks in both sexes, whereas females regained reproductive function in 4 weeks and males did so in 8 weeks. These results highlight that body mass and reproductive functions demonstrate distinct and sex-specific responses to photoperiod in mouse lemurs.

Detecting the risk of infection and minimizing parasite exposure represent the first lines of host defence against parasites. Individuals differ in the expression of these behavioural defences, but causes of such variation have received little empirical attention. We therefore experimentally investigated the effects of several individual and environmental factors on the expression level of faecal avoidance in the context of feeding, drinking, sleeping and defecating in a wild primate population. We found a strong sex bias in the expression level of anti-parasite behaviours of grey mouse lemurs ( Microcebus murinus ), with only females strongly avoiding contaminated food, water and nests, and exhibiting selective defecation. Our results further suggest that individuals adapted their protective behaviours according to variation in intrinsic and ecological factors that may influence the cost–benefit balance of behavioural defences. Overall, individuals exhibited high consistency of investment in protective behaviours across behavioural contexts and time, suggesting that grey mouse lemurs exhibit different hygienic personalities. Finally, the global hygienic score was negatively correlated with faecal–orally transmitted parasite richness, suggesting that variation in behavioural defence has fitness consequences. We suggest that integrating inter-individual variation in behavioural defences in epidemiological studies should improve our ability to model disease spread within populations.

The gray mouse lemur (Microcebus murinus) is a small prosimian of growing interest for studies of primate biology and evolution, and notably as a model organism of brain aging. As brain atlases are essential tools for brain investigation, the objective of the current work was to create the first 3D digital atlas of the mouse lemur brain. For this, a template image was constructed from in vivo magnetic resonance imaging (MRI) data of 34 animals. This template was then manually segmented into 40 cortical, 74 subcortical and 6 cerebro-spinal fluid (CSF) regions. Additionally, we generated probability maps of gray matter, white matter and CSF. The template, manual segmentation and probability maps, as well as imaging tools used to create and manipulate the template, can all be freely downloaded. The atlas was first used to automatically assess regional age-associated cerebral atrophy in a cohort of mouse lemurs previously studied by voxel based morphometry (VBM). Results based on the atlas were in good agreement with the VBM ones, showing age-associated atrophy in the same brain regions such as the insular, parietal or occipital cortices as well as the thalamus or hypothalamus. The atlas was also used as a tool for comparative neuroanatomy. To begin with, we compared measurements of brain regions in our MRI data with histology-based measures from a reference article largely used in previous comparative neuroanatomy studies. We found large discrepancies between our MRI-based data and those of the reference histology-based article. Next, regional brain volumes were compared amongst the mouse lemur and several other mammalian species where high quality volumetric MRI brain atlases were available, including rodents (mouse, rat) and primates (marmoset, macaque, and human). Unlike those based on histological atlases, measures from MRI atlases indicated similar cortical to cerebral volume indices in all primates, including in mouse lemurs, and lower values in mice. On the other hand, white matter to cerebral volume index increased from rodents to small primates (mouse lemurs and marmosets) to macaque, reaching their highest values in humans. [Display omitted] •The mouse lemur primate is an original model for neuroscience studies and comparative anatomy.•We present an anatomical brain template, constructed from in vivo MRI scans of 34 mouse lemurs.•We created the first high resolution 3D atlas of the mouse lemur brain (120 regions encompassing each voxel of the template).•The template, code developed to create and manipulate the template as well as segmentation maps are freely available.•The atlas was used to characterize age-related atrophy and to compare the mouse lemur brain with brains from other mammals.