Preserved neural dynamics across animals performing similar behaviour.

Animals of the same species exhibit similar behaviours that are advantageously adapted to their body and environment. These behaviours are shaped at the species level by selection pressures over evolutionary timescales. Yet, it remains unclear how these common behavioural adaptations emerge from the idiosyncratic neural circuitry of each individual. The overall organization of neural circuits is preserved across individuals1 because of their common evolutionarily specified developmental programme2-4. Such organization at the circuit level may constrain neural activity5-8, leading to low-dimensional latent dynamics across the neural population9-11. Accordingly, here we suggested that the shared circuit-level constraints within a species would lead to suitably preserved latent dynamics across individuals. We analysed recordings of neural populations from monkey and mouse motor cortex to demonstrate that neural dynamics in individuals from the same species are surprisingly preserved when they perform similar behaviour. Neural population dynamics were also preserved when animals consciously planned future movements without overt behaviour12 and enabled the decoding of planned and ongoing movement across different individuals. Furthermore, we found that preserved neural dynamics extend beyond cortical regions to the dorsal striatum, an evolutionarily older structure13,14. Finally, we used neural network models to demonstrate that behavioural similarity is necessary but not sufficient for this preservation. We posit that these emergent dynamics result from evolutionary constraints on brain development and thus reflect fundamental properties of the neural basis of behaviour.

Transcranial magnetic stimulation in non-human primates: A systematic review.

Transcranial magnetic stimulation (TMS) is widely employed as a tool to investigate and treat brain diseases. However, little is known about the direct effects of TMS on the brain. Non-human primates (NHPs) are a valuable translational model to investigate how TMS affects brain circuits given their neurophysiological similarity with humans and their capacity to perform complex tasks that approach human behavior. This systematic review aimed to identify studies using TMS in NHPs as well as to assess their methodological quality through a modified reference checklist. The results show high heterogeneity and superficiality in the studies regarding the report of the TMS parameters, which have not improved over the years. This checklist can be used for future TMS studies with NHPs to ensure transparency and critical appraisal. The use of the checklist would improve methodological soundness and interpretation of the studies, facilitating the translation of the findings to humans. The review also discusses how advancements in the field can elucidate the effects of TMS in the brain.

Coding strategy for surface luminance switches in the primary visual cortex of the awake monkey.

Both surface luminance and edge contrast of an object are essential features for object identification. However, cortical processing of surface luminance remains unclear. In this study, we aim to understand how the primary visual cortex (V1) processes surface luminance information across its different layers. We report that edge-driven responses are stronger than surface-driven responses in V1 input layers, but luminance information is coded more accurately by surface responses. In V1 output layers, the advantage of edge over surface responses increased eight times and luminance information was coded more accurately at edges. Further analysis of neural dynamics shows that such substantial changes for neural responses and luminance coding are mainly due to non-local cortical inhibition in V1's output layers. Our results suggest that non-local cortical inhibition modulates the responses elicited by the surfaces and edges of objects, and that switching the coding strategy in V1 promotes efficient coding for luminance.

Face detection in untrained deep neural networks.

Face-selective neurons are observed in the primate visual pathway and are considered as the basis of face detection in the brain. However, it has been debated as to whether this neuronal selectivity can arise innately or whether it requires training from visual experience. Here, using a hierarchical deep neural network model of the ventral visual stream, we suggest a mechanism in which face-selectivity arises in the complete absence of training. We found that units selective to faces emerge robustly in randomly initialized networks and that these units reproduce many characteristics observed in monkeys. This innate selectivity also enables the untrained network to perform face-detection tasks. Intriguingly, we observed that units selective to various non-face objects can also arise innately in untrained networks. Our results imply that the random feedforward connections in early, untrained deep neural networks may be sufficient for initializing primitive visual selectivity.

Dynamic divisive normalization circuits explain and predict change detection in monkey area MT.

Sudden changes in visual scenes often indicate important events for behavior. For their quick and reliable detection, the brain must be capable to process these changes as independently as possible from its current activation state. In motion-selective area MT, neurons respond to instantaneous speed changes with pronounced transients, often far exceeding the expected response as derived from their speed tuning profile. We here show that this complex, non-linear behavior emerges from the combined temporal dynamics of excitation and divisive inhibition, and provide a comprehensive mathematical analysis. A central prediction derived from this investigation is that attention increases the steepness of the transient response irrespective of the activation state prior to a stimulus change, and irrespective of the sign of the change (i.e. irrespective of whether the stimulus is accelerating or decelerating). Extracellular recordings of attention-dependent representation of both speed increments and decrements confirmed this prediction and suggest that improved change detection derives from basic computations in a canonical cortical circuitry.

The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates.

Life history, brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure (either basal/resting or daily) independent of body mass. We addressed this question by examining the relationship between primate free-living daily energy expenditure (DEE) measured by doubly labeled water method (n = 18 species), life history variables (maximum lifespan, gestation and lactation duration, interbirth interval, litter mass, age at first reproduction), resting metabolic rate (RMR) and brain size. We also analyzed whether the hypometabolic primates of Madagascar (lemurs) make distinct energy allocation tradeoffs compared to other primates (monkeys and apes) with different life history traits and ecological constraints. None of the life-history traits correlated with DEE after controlling for body mass and phylogeny. In contrast, a regression model showed that DEE increased with increasing RMR and decreasing reproductive output (i.e., litter mass/interbirth interval) independent of body mass. Despite their low RMR and smaller brains, lemurs had an average DEE remarkably similar to that of haplorhines. The data suggest that lemurs have evolved energy strategies that maximize energy investment to survive in the unusually harsh and unpredictable environments of Madagascar at the expense of reproduction.

Titi monkey neophobia and visual abilities allow for fast responses to novel stimuli.

The Snake Detection Theory implicates constricting snakes in the origin of primates, and venomous snakes for differences between catarrhine and platyrrhine primate visual systems. Although many studies using different methods have found very rapid snake detection in catarrhines, including humans, to date no studies have examined how quickly platyrrhine primates can detect snakes. We therefore tested in captive coppery titi monkeys (Plecturocebus cupreus) the latency to detect a small portion of visible snake skin. Because titi monkeys are neophobic, we designed a crossover experiment to compare their latency to look and their duration of looking at a snake skin and synthetic feather of two lengths (2.5 cm and uncovered). To test our predictions that the latency to look would be shorter and the duration of looking would be longer for the snake skin, we used survival/event time models for latency to look and negative binomial mixed models for duration of looking. While titi monkeys looked more quickly and for longer at both the snake skin and feather compared to a control, they also looked more quickly and for longer at larger compared to smaller stimuli. This suggests titi monkeys' neophobia may augment their visual abilities to help them avoid dangerous stimuli.

Mechanics of heel-strike plantigrady in African apes.

The initiation of a walking step with a heel strike is a defining characteristic of humans and great apes but is rarely found in other mammals. Despite the considerable importance of heel strike to an understanding of human locomotor evolution, no one has explicitly tested the fundamental mechanical question of why great apes use a heel strike. In this report, we test two hypotheses (1) that heel strike is a function of hip protraction and/or knee extension and (2) that short-legged apes with a midfoot that dorsiflexes at heel lift and long digits for whom digitigrady is not an option use heel-strike plantigrady. This strategy increases hip translation while potentially moderating the cost of redirecting the center of mass ('collisional costs') during stance via rollover along the full foot from the heel to toes. We quantified hind limb kinematics and relative hip translation in ten species of primates, including lemurs, terrestrial and arboreal monkeys, chimpanzees, and gorillas. Chimpanzees and gorillas walked with relatively extended knees but only with moderately protracted hips or hind limbs, partially rejecting the first hypothesis. Nonetheless, chimpanzees attained relative hip translations comparable with those of digitigrade primates. Heel-strike plantigrady may be a natural result of a need for increased hip translations when forelimbs are relatively long and digitigrady is morphologically restricted. In addition, foot rollover from the heel to toe in large, short-legged apes may reduce energetic costs of redirecting the center of mass at the step-to-step transition as it appears to do in humans. Heel strike appears to have been an important mechanism for increasing hip translation, and possibly reducing energetic costs, in early hominins and was fundamental to the evolution of the modern human foot and human bipedalism.

Potential use of actigraphy to measure sleep in monkeys: comparison with behavioral analysis from videography.

Sleep is indispensable for human health, with sleep disorders initiating a cascade of negative consequences. As our closest phylogenetic relatives, non-human primates (NHPs) are invaluable for comparative sleep studies and exhibit tremendous potential for improving our understanding of human sleep and related disorders. Previous work on measuring sleep in NHPs has mostly used electroencephalography or videography. In this study, simultaneous videography and actigraphy were applied to observe sleep patterns in 10 cynomolgus monkeys ( Macaca fascicularis) over seven nights (12 h per night). The durations of wake, transitional sleep, and relaxed sleep were scored by analysis of animal behaviors from videography and actigraphy data, using the same behavioral criteria for each state, with findings then compared. Here, results indicated that actigraphy constituted a reliable approach for scoring the state of sleep in monkeys and showed a significant correlation with that scored by videography. Epoch-by-epoch analysis further indicated that actigraphy was more suitable for scoring the state of relaxed sleep, correctly identifying 97.57% of relaxed sleep in comparison with video analysis. Only 34 epochs (0.13%) and 611 epochs (2.30%) were differently interpreted as wake and transitional sleep compared with videography analysis. The present study validated the behavioral criteria and actigraphy methodology for scoring sleep, which can be considered as a useful and a complementary technique to electroencephalography and/or videography analysis for sleep studies in NHPs.

Explicit memory and cognition in monkeys.

Taxonomies of human memory, influenced heavily by Endel Tulving, make a fundamental distinction between explicit and implicit memory. Humans are aware of explicit memories, whereas implicit memories control behavior even though we are not aware of them. Efforts to understand the evolution of memory, and to use nonhuman animals to model human memory, will be facilitated by better understanding the extent to which this critical distinction exists in nonhuman animals. Work with metacognition paradigms in the past 20 years has produced a strong case for the existence of explicit memory in nonhuman primates and possibly other nonhuman animals. Clear dissociations of explicit and implicit memory by metacognition have yet to be demonstrated in nonhumans, although dissociations between memory systems by other behavioral techniques, and by brain manipulations, suggest that the explicit-implicit distinction applies to nonhumans. Neurobehavioral studies of metamemory are beginning to identify neural substrates for memory monitoring in the frontal cortex of monkeys. We have strong evidence that at least some memory systems are explicit in rhesus monkeys, but we need to learn more about the distribution of explicit processes across cognitive systems within monkeys, and across species.

Preparation for certain and uncertain future outcomes in young children and three species of monkey.

This study examined 3-year old children and monkeys' capacities to prepare for immediate future events. In Study 1, children were presented with several tube apparatuses with two exits. When targets were certain to emerge from both, children tended to prepare to catch them by covering each exit. When it was uncertain where targets would emerge, however, they tended to prepare for only one possibility. These results substantiate the claim that simultaneous preparation for mutually exclusive possibilities develops relatively late. Study 2 found no evidence for such a capacity in monkeys (Ateles geoffroyi, Cebus apella, Papio hamadryas) given the same tasks.

Ontogeny of Orbit Orientation in Primates.

Orbit orientation in primates has been linked to adaptive factors related to activity pattern and size-related variation in structural influences on orbit position. Although differences in circumorbital form between anthropoids and strepsirrhines appear to be related to interspecific disparities in levels of orbital convergence and orbital frontation, there is considerable overlap in convergence between suborders. Unfortunately, putative links between convergence and frontation across primates, and consequent arguments about primate and anthropoid origins, are likely to be influenced by allometry, the size range of a respective sample, and adaptive influences on encephalization and activity patterns. Such a multifarious system is less amenable to interspecific treatment across higher-level clades. An ontogenetic perspective is one way to evaluate transformations from one character state to another, especially as they pertain to allometric effects on phenotypic variation. We characterized the ontogeny of orbital convergence and frontation in 13 anthropoid and strepsirrhine species. In each suborder, correlation and regression analyses were used to test hypotheses regarding the allometric bases of variation in orbital orientation. Growth trajectories were analyzed intra- and inter-specifically. Frontation decreased postnatally in all taxa due to the negative scaling of brain vs. skull size. Further, interspecific variation in relative levels of frontation was linked to corresponding ontogenetic transpositions in encephalization that differed within both suborders. In strepsirrhines, postnatal increases in convergence were largely due to the negative allometry of orbit vs. skull size. In contrast, convergence in anthropoids varied little during growth, being unrelated to ontogenetic variation in either relative orbit or interorbit size. Anat Rec, 302:2093-2104, 2019. © 2019 American Association for Anatomy.

Perturbing low dimensional activity manifolds in spiking neuronal networks.

Several recent studies have shown that neural activity in vivo tends to be constrained to a low-dimensional manifold. Such activity does not arise in simulated neural networks with homogeneous connectivity and it has been suggested that it is indicative of some other connectivity pattern in neuronal networks. In particular, this connectivity pattern appears to be constraining learning so that only neural activity patterns falling within the intrinsic manifold can be learned and elicited. Here, we use three different models of spiking neural networks (echo-state networks, the Neural Engineering Framework and Efficient Coding) to demonstrate how the intrinsic manifold can be made a direct consequence of the circuit connectivity. Using this relationship between the circuit connectivity and the intrinsic manifold, we show that learning of patterns outside the intrinsic manifold corresponds to much larger changes in synaptic weights than learning of patterns within the intrinsic manifold. Assuming larger changes to synaptic weights requires extensive learning, this observation provides an explanation of why learning is easier when it does not require the neural activity to leave its intrinsic manifold.

Middle ear pneumatization in nonhuman primates: A comparative analysis.

OBJECTIVES: We test the effects of body mass and phylogeny on middle ear cavity pneumatization, and the role of pneumatization in hearing function, spanning the anatomical, ecological, and behavioral diversity of nonhuman primates. MATERIALS AND METHODS: All cavities were segmented in middle ear scans of 96 specimens, from 12 strepsirrhine and 15 haplorhine extant species. We measured the tympanic cavity (TC) separately, and all other middle ear spaces together (MES), calculating the degree of pneumatization with the surface area-to-volume ratio. We tested body mass effect with linear regression; we evaluated the phylogenetic signal and selection patterns, using a Kappa statistic test, and Ornstein-Uhlenbeck models (OU). We investigated the link between pneumatization and hearing sensitivity using phylogenetic regression. RESULTS: Testing body mass reveals an allometric pattern for both TC and MES dimensions. Degree of pneumatization in MES is dependent on body mass in haplorhines: larger animals have more pneumatized MES. Differences at various taxonomic ranks were observed for MES, while no phylogenetic influence was observed for TC. Infraorder selection patterns are different. Auditory performance is significantly related to degree of pneumatization, indicating that a pneumatized middle ear is associated with better perception of low frequencies. DISCUSSION: Pneumatization in MES is under differential selective pressure, indicating several optima for this trait. Pneumatization in MES probably modifies hearing sensitivity through pressure regulation mechanisms, auditory bulla size reduction, and frequency modulation. This could explain strepsirrhine adaptation to high-frequency perception, while haplorhine auditory perception is adapted to a broader sound range, including high and low frequencies.

A transgenic monkey model for the study of human brain evolution.

Why humans have large brains with higher cognitive abilities is a question long asked by scientists. However, much remains unknown, especially the underlying genetic mechanisms. With the use of a transgenic monkey model, we showed that human-specific sequence changes of a key brain development gene (primary microcephaly1, MCPH1) could result in detectable molecular and cognitive changes resembling human neoteny, a notable characteristic developed during human evolution.

Intrinsic functional architecture of the non-human primate spinal cord derived from fMRI and electrophysiology.

Resting-state functional MRI (rsfMRI) has recently revealed correlated signals in the spinal cord horns of monkeys and humans. However, the interpretation of these rsfMRI correlations as indicators of functional connectivity in the spinal cord remains unclear. Here, we recorded stimulus-evoked and spontaneous spiking activity and local field potentials (LFPs) from monkey spinal cord in order to validate fMRI measures. We found that both BOLD and electrophysiological signals elicited by tactile stimulation co-localized to the ipsilateral dorsal horn. Temporal profiles of stimulus-evoked BOLD signals covaried with LFP and multiunit spiking in a similar way to those observed in the brain. Functional connectivity of dorsal horns exhibited a U-shaped profile along the dorsal-intermediate-ventral axis. Overall, these results suggest that there is an intrinsic functional architecture within the gray matter of a single spinal segment, and that rsfMRI signals at high field directly reflect this underlying spontaneous neuronal activity.

Embracing in a female-bonded monkey species (Theropithecus gelada).

[Correction Notice: An Erratum for this article was reported online in Journal of Comparative Psychology on May 9 2019 (see record 2019-25503-001). In the article "Embracing in a Female-Bonded Monkey Species (Theropithecus gelada)" by Virginia Pallante, Pier Francesco Ferrari, Marco Gamba, and Elisabetta Palagi (Journal of Comparative Psychology, Advance online publication. March 25, 2019. http://dx.doi.org/10.1037/ com0000173), the title incorrectly read "Embracing in a Female-Bonded Monkey Specie (Theropithecus gelada)" All versions of this article have been corrected.] In several primate species, including humans, embracing predicts the level of affiliation between subjects. To explore the functional meaning of embracing, we selected Theropithecus gelada as a model species. The basic level of the gelada society is the 1-male unit, and the integrity of the group is maintained by the strong bonds between females. In our study group, we observed 3 different kinds of embracing: the frontal and side embraces involving a face-to-face and chest-to-chest interaction and the posterior embrace that consists in putting the arms around conspecifics' back and posing a cheek on it. We verified that the quality of relationships between subjects predicts the type of embracing. Frontal and side embraces were more frequent between females sharing strong bonds. Posterior embracing was randomly distributed. We found a high level of female embracing among the mothers during the first months of lactation. This may improve female cohesiveness against males, thus reducing the risk of infanticide, which is particularly high in geladas. Embracing seems also to act as an ice-breaker favoring grooming. Female embracing could be an affiliative strategy that has evolved to maintain group integrity and high social cohesion among females, especially mothers. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Specialized rainforest hunting by Homo sapiens ~45,000 years ago.

Defining the distinctive capacities of Homo sapiens relative to other hominins is a major focus for human evolutionary studies. It has been argued that the procurement of small, difficult-to-catch, agile prey is a hallmark of complex behavior unique to our species; however, most research in this regard has been limited to the last 20,000 years in Europe and the Levant. Here, we present detailed faunal assemblage and taphonomic data from Fa-Hien Lena Cave in Sri Lanka that demonstrates specialized, sophisticated hunting of semi-arboreal and arboreal monkey and squirrel populations from ca. 45,000 years ago, in a tropical rainforest environment. Facilitated by complex osseous and microlithic technologies, we argue these data highlight that the early capture of small, elusive mammals was part of the plastic behavior of Homo sapiens that allowed it to rapidly colonize a series of extreme environments that were apparently untouched by its hominin relatives.

Menstrual cycle in four New World primates: Poeppig's woolly monkey (Lagothrix poeppigii), red uakari (Cacajao calvus), large-headed capuchin (Sapajus macrocephalus) and nocturnal monkey (Aotus nancymaae).

Genital organs from 33 nocturnal monkeys Aotus namcymaae, 29 Poeppig's woolly monkeys (Lagothrix poeppigii), 21 red uakaris (Cacajao calvus) and 11 large-headed capuchins (Sapajus macrocephalus) were histologically analyzed in order to describe the endometrial changes related to the ovarian cycle. A. nancymaae and S. macrocephalus showed histological evidence of menstrual cycle with the detachment of the most superficial endometrium and the subepithelial reabsorption of the endometrial functional layer, explaining the extensive presence of both hemosiderin and fibrin clusters in the early follicular stages. In L. poeppigii, despite the presence of fibrin clusters promoting the remodeling of the endometrium, we did not observe the detachment of the functional layer of the endometrium, suggesting that this species presents a non-menstruating cycle. Finally, C. calvus showed no histological sign of menstrual phase. This reproductive information is useful to improve assisted reproductive techniques in non-human primates, and give us opportunity for comparative studies on the evolution of animal reproductive biology, including humans.