Asymmetries In Nonhuman Primates Research Articles

Cerebral asymmetry in adult Macaca fascicularis as revealed by voxel-based MRI and DTI analysis

Investigating cerebral asymmetries in non-human primates would facilitate to understand the evolutional traits of the human brain specialization related to language and other high-level cognition. However, brain asymmetrical studies of monkeys produced controversial results. Here, we investigated the cerebral asymmetries using a combination of the optimized voxel-based morphometry (VBM) and tract-based spatial statistics (TBSS) protocols in monkeys. The study-specific MRI and DTI-based templates were created in 66 adult Macaca fascicularis, and the asymmetrical index of grey and white matter was subsequently examined. The VBM analysis detected the well-known frontal and occipital petalias and confirmed the presence of leftward asymmetry in the ventral frontal cortex. A marked leftward asymmetry of anterior superior temporal gyrus but not posterior portion were found. We also identified grey matter asymmetries in some regions that were not previously reported including rightward anterior cingulate, insular cortex and thalamus, and leftward caudate. In contrast, the results of TBSS analysis for the first time revealed the robust leftwards asymmetries of corpus callosum (splenium and body), internal/external capsule, and white matter in middle temporal gyrus, adjacent thalamus and amygdala whereas the rightwards in uncinate fasciculus, posterior thalamic radiation and cerebral peduncle. These findings provide robust evidence of grey and white matter asymmetries in the brain of monkeys, which may extend the understanding of brain evolution in cerebral specialization.

Neuroanatomical asymmetries in nonhuman primates in the homologs to Broca's and Wernicke's areas: a mini-review.

Population-level lateralization in structure and function is a fundamental measure of the human nervous system. To what extent nonhuman primates exhibit similar patterns of asymmetry remains a topic of considerable scientific interest. In this mini-review, a brief summary of findings on brain asymmetries in nonhuman primates in brain regions considered to the homolog's to Broca's and Wernicke's area are presented. Limitations of existing and directions for future studies are discussed in the context of facilitating comparative investigations in primates.

Endocranial asymmetry in New World monkeys: a comparative phylogenetic analysis of morphometric data.

Brain lateralization is a widespread phenomenon although its expression across primates is still controversial due to the reduced number of species analyzed and the disparity of methods used. To gain insight into the diversification of neuroanatomical asymmetries in non-human primates we analyze the endocasts, as a proxy of external brain morphology, of a large sample of New World monkeys and test the effect of brain size, home range and group sizes in the pattern and magnitude of shape asymmetry. Digital endocasts from 26 species were obtained from MicroCT scans and a set of 3D coordinates was digitized on endocast surfaces. Results indicate that Ateles, Brachyteles, Callicebus and Cacajao tend to have a rightward frontal and a leftward occipital lobe asymmetry, whereas Aotus, Callitrichinae and Cebinae have either the opposite pattern or no directional asymmetry. Such differences in the pattern of asymmetry were associated with group and home range sizes. Conversely, its magnitude was significantly associated with brain size, with larger-brained species showing higher inter-hemispheric differences. These findings support the hypothesis that reduction in inter-hemispheric connectivity in larger brains favors the lateralization and increases the structural asymmetries, whereas the patterns of shape asymmetry might be driven by socio-ecological differences among species.

Social buffering of cortisol release and tympanic temperature asymmetries during novelty and isolation stress in marmoset monkeys

Novel environments induce a conflicting emotional approach-withdrawal state that triggers stress-related reactions. Social support through the presence of a highly familiar conspecific buffers the individual against such challenges. Although aversive events seem to be predominantly processed by the right hemisphere, this is still under debate and little is known about functional cerebral asymmetries in nonhuman primates during novelty stress, isolation and social buffering. Here we isolated adult marmoset monkeys in a new open-field arena or in their familiar home-cages to establish hemisphere activity and whether the pairmate’s presence buffers the response. Monkeys socially isolated in either location had higher circulating cortisol levels than non-isolated marmosets, but different hemisphere activity patterns indicated by changes in baseline tympanic membrane temperatures (TMT). The bilateral increase in the monkeys that were isolated in the unfamiliar location may reflect an approach-withdrawal conflict. The left-sided increase in the home-cage isolation group was negatively related to cortisol release, this being potentially associated with a more proactive/approach-prone temperament. Interestingly, TMT and cortisol were unaltered when the pairmate was present. Thus, positive social interaction reduces the perceived intensity of the threat, alters hemisphere asymmetries and blocks the hormonal response to novelty stress, consistent with a buffering effect.

Mapping hemispheric asymmetries of the macaque cerebral cortex during early brain development

Studying cortical hemispheric asymmetries during the dynamic early postnatal stages in macaque monkeys (with close phylogenetic relationship to humans) would increase our limited understanding on the possible origins, developmental trajectories, and evolutional mechanisms of brain asymmetries in nonhuman primates, but remains a blind spot to the community. Via cortical surface‐based morphometry, we comprehensively analyze hemispheric structural asymmetries in 134 longitudinal MRI scans from birth to 20 months of age from 32 healthy macaque monkeys. We reveal that most clusters of hemispheric asymmetries of cortical properties, such as surface area, cortical thickness, sulcal depth, and vertex positions, expand in the first 4 months of life, and evolve only moderately thereafter. Prominent hemispheric asymmetries are found at the inferior frontal gyrus, precentral gyrus, posterior temporal cortex, superior temporal gyrus (STG), superior temporal sulcus (STS), and cingulate cortex. Specifically, the left planum temporale and left STG consistently have larger area and thicker cortices than those on the right hemisphere, while the right STS, right cingulate cortex, and right anterior insula are consistently deeper than the left ones, partially consistent with the findings in human infants and adults. Our results thus provide a valuable reference in studying early brain development and evolution.

Baboon (Papio anubis) chimeric face processing by human (Homo sapiens) judges: Influence of stimuli complexity on the perception of oro-facial asymmetries.

Two methodologies have traditionally been used to measure hemispheric specialization for perception and expression of emotions in human and nonhuman primates. The first refers to objective measures, that is, measures of area and length of facial features, and the second concerns subjective "measures," that is, assessment of chimeric faces by human judges. We proposed a refined approach to the subjective assessment of hemispheric specializations, which aims at delimiting methodological issues in the study of orofacial asymmetries. The study focused on a baboon threat orofacial expression, which has led to discordant results according to the methodology used (Wallez & Vauclair, 2011, 2013). We presented human participants with two sets of chimeric stimuli varying the regions of the face likely to be processed. The whole face set was composed of classical chimeric faces, and the upper face set was made of chimeric faces for which the lower part was blurred. The purpose of this new procedure was to shed light on the perception process of baboon faces by human participants during a free-viewing chimeric task. Results showed a concomitant influence of the chimera structure depending on the order of the presentation of the set, revealing a training effect in our human judges. These factors combined together allowed the appearance of an overall left-left chimeric choice by human judges (i.e., which indicates a right hemisphere involvement in baboon threat expression). These findings bring novel insights into the study of orofacial asymmetries in nonhuman primates by human judgments. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Division of Labour:A Democratic Approach towards Understanding Manual Asymmetries in Non-Human Primates

A consequence of the 'gold rush'-like hunch for human-like handedness in non-human primates has been that researchers have been continually analysing observations at the level of the population, ignoring the analysis at the level of an individual and, consequently, have potentially missed revelations on the forms and functions of manual asymmetries. Recently, consecutive studies on manual asymmetries in bonnet macaques, Macaca radiata revealed both the functional and adaptive significance of manual asymmetries respectively, and pointed towards the division of labour as being the general principle underlying the observed hand-usage patterns. We review the studies on manual asymmetries in capuchin monkeys, Cebus spp. and argue that the observed hand-usage patterns might reflect specialization of the two hands for accomplishing tasks that require different dexterity types (i.e. manoeuvring in three-dimensional space or physical strength). To this end, we do a step-by-step analysis of the various tasks used in the studies on manual asymmetries in capuchin monkeys. We then describe the division of labour as a general principle underlying manual asymmetries in non-human primates and propose experimental designs that would elaborate the forms and functions of manual asymmetries in non-human primates and the associated adaptive value.

Behavioral and brain asymmetries in primates: a preliminary evaluation of two evolutionary hypotheses.

Contrary to many historical views, recent evidence suggests that species-level behavioral and brain asymmetries are evident in nonhuman species. Here, we briefly present evidence of behavioral, perceptual, cognitive, functional, and neuroanatomical asymmetries in nonhuman primates. In addition, we describe two historical accounts of the evolutionary origins of hemispheric specialization and present data from nonhuman primates that address these specific theories. Specifically, we first discuss the evidence that genes play specific roles in determining left-right differences in anatomical and functional asymmetries in primates. We next consider and present data on the hypothesis that hemispheric specialization evolved as a by-product of increasing brain size relative to the surface area of the corpus callosum in different primate species. Last, we discuss some of the challenges in the study of hemispheric specialization in primates and offer some suggestions on how to advance the field.

What can atypical language hemispheric specialization tell us about cognitive functions?

Recent studies have made substantial progress in understanding the interactions between cognitive functions, from language to cognitive control, attention, and memory. However, dissociating these functions has been hampered by the close proximity of regions involved, as in the case in the prefrontal and parietal cortex. In this article, we review a series of studies that investigated the relationship between language and other cognitive functions in an alternative way - by examining their functional (co-)lateralization. We argue that research on the hemispheric lateralization of language and its link with handedness can offer an appropriate starting-point to shed light on the relationships between different functions. Besides functional interactions, anatomical asymmetries in non-human primates and those underlying language in humans can provide unique information about cortical organization. Finally, some open questions and criteria are raised for an ideal theoretical model of the cortex based on hemispheric specialization.

Contrast of hemispheric lateralization for oro-facial movements between learned attention-getting sounds and species-typical vocalizations in chimpanzees: Extension in a second colony

Studies involving oro-facial asymmetries in nonhuman primates have largely demonstrated a right hemispheric dominance for communicative signals and conveyance of emotional information. A recent study on chimpanzee reported the first evidence of significant left-hemispheric dominance when using attention-getting sounds and rightward bias for species-typical vocalizations (Losin, Russell, Freeman, Meguerditchian, Hopkins & Fitch, 2008). The current study sought to extend the findings from Losin et al. (2008) with additional oro-facial assessment in a new colony of chimpanzees. When combining the two populations, the results indicated a consistent leftward bias for attention-getting sounds and a right lateralization for species-typical vocalizations. Collectively, the results suggest that both voluntary-controlled oro-facial and gestural communication might share the same left-hemispheric specialization and might have coevolved into a single integrated system present in a common hominid ancestor.

Variability and asymmetry of the sulcal contours defining Broca's area homologue in the chimpanzee brain

There has been recent motivation to search for neuroanatomical asymmetries in nonhuman primates in order to provide comparative information on how the human brain is structurally organized to support specific cognitive capabilities, such as language functions. We took the opportunity to study Broca's area homologue in a novel sample of 80 preserved postmortem chimpanzee (Pan troglodytes) cerebral hemispheres. Consistent with the only prior study documenting the morphology of Broca's area homologue in the chimpanzee (Sherwood et al. [2003] Anat Rec 271:276–285), we report great interindividual variation in the structure and connections of the sulci investigated, most notably a left-sided bias in the bifurcation of the inferior precentral sulcus, an anatomical feature that occurs much more frequently in chimpanzees relative to humans. Consistent with our recent neuroimaging report (Keller et al. [2009b] J Neurosci 29:14607–14616), no population-based interhemispheric asymmetries of sulcal length existed that could be considered markers of the size of Broca's area homologue. With strict anatomical guidelines, we report that the diagonal sulcus was present in 25% left and 20% right chimpanzee hemispheres studied, which is substantially less that the general prevalence in humans. Through the presentation of schematic drawings, photographs, morphological recordings and sulcal length metrics, our data illustrate the interindividual variability of Broca's area homologue in the chimpanzee and support the notion of no macroscopic asymmetry of this important homologous language brain region in one of the closest evolutionary ancestor to modern humans.

Right hemisphere dominance for emotion processing in baboons

Asymmetries of emotional facial expressions in humans offer reliable indexes to infer brain lateralization and mostly revealed right hemisphere dominance. Studies concerned with oro-facial asymmetries in nonhuman primates largely showed a left-sided asymmetry in chimpanzees, marmosets and macaques. The presence of asymmetrical oro-facial productions was assessed in Olive baboons in order to determine the functional cerebral asymmetries. Two affiliative behaviors (lipsmack, copulation call) and two agonistic ones (screeching, eyebrow-raising) were recorded. For screeching, a strong and significant left hemimouth bias was found, but no significant bias was observed for the other behaviors. These results are discussed in the light of the available literature concerning asymmetrical oro-facial productions in nonhuman primates. In addition, these findings suggest that human hemispheric specialization for emotions has precursors in primate evolution.

Cerebral volumetric asymmetries in non-human primates: A magnetic resonance imaging study

Magnetic resonance images (MRI) were collected in a sample of 23 apes, 14 Old World monkeys, and 8 New World monkeys. The total area or volume of the anterior and posterior cerebral regions of each hemisphere of the brain was measured. The results indicated that a rightward frontal and leftward occipital pattern of asymmetry was present at a population level in the great ape sample. Population-level cerebral asymmetries were not revealed in the sample of New or Old World monkeys. The total area or volume of the planum temporale, which was localised only in the great apes, was also measured in both hemispheres. A leftward planum temporale asymmetry was evident at the population level in the great apes. It was hypothesised that the rightward frontal and leftward occipital asymmetries would correlate with leftward planum temporale asymmetries. This hypothesis was based on the assumption that, similar to development of the human brain, the nonhuman primate brain “torques” during development due to a growth gradient which progresses anterior to posterior, ventral to dorsal, and right to left. The results of this study confirmed the predicted relationship between cerebral volume and the planum temporale asymmetries. This supports the hypothesis that the great ape brain may develop in a “torquing” manner, producing similar anatomical asymmetries as reported in humans.

Cerebral volumetric asymmetries in non-human primates: A magnetic resonance imaging study

Cerebral volumetric asymmetries in non-human primates: A magnetic resonance imaging study

Sylvian Fissure Asymmetries in Nonhuman Primates Revisited: A Comparative MRI Study

Magnetic resonance images (MRI) were collected in a sample of 28 apes, 16 Old World monkeys and 8 New World monkeys. The length of the sylvian fissure (SF) and the superior temporal sulcus (STS) was traced in each hemisphere from three regions of the cerebral cortex. These three regions were labeled according to their position on the sagittal plane as lateral, medial and insular. It was hypothesized that the length and asymmetry of these fissures would be dependent on the region of measurement and that a leftward asymmetry in the SF and STS would be more robust in the great ape sample than for the monkeys. The results indicated within the ape sample a population-level leftward asymmetry in the medial and insular regions of the SF. Within the Old and New World monkey samples, the SF was leftward in the medial region at the population level, but not at the insular region. Additionally, the Old World monkeys exhibited a population-level rightward lateral SF and a rightward lateral STS. No other families exhibited population-level asymmetries in the lateral region of the SF or in any region of the STS. These results are consistent with findings reported in apes and, to a lesser extent, monkeys. MRI has excellent potential for comparing neuroanatomy across taxonomic families that will help future investigations.

Cranial asymmetry in Ceboid primates: The emissary foramina

AbstractUntil the last decade or so, relatively little was known of cranial asymmetries in nonhuman primates. Data are slowly, but surely, accumulating for such features as transverse sinus flow, sylvian point angle differences, external brain morphology, etc. Cranial asymmetries are being analyzed and related to such diverse problems as “handedness” and phylogenetic systematics. It has been known for over 200 years that cranial asymmetry exists in some of the cerebral blood flow patterns in man, particularly the internal jugular pathway. Although earlier anatomists assumed this was only characteristic of “higher primates” (meaning man and the great apes), little quantitative data have been available to either support or deny this belief. There is a particular dearth of information for New World primates. The aim of this study is to contribute to the growing literature on cerebral asymmetries by partially filling in this gap in our knowledge of New World primate biology.