Thursday 7 November 2024

Common Origins - Marmoset and Human Brain Development


As in humans, infants of common marmosets interact with several caregivers from birth and are thus exposed to intensive social interaction.
Image: Judith Burkart/UZH
Brain Development Marmosets | | UZH

Creationists like to pretend there is nothing in common between humans and the rest of the animal kingdom because humans were magically created as the special creation of a god who made all the 'lower' animals for our use, then gave us dominion over everything. This makes creationists feel really important.

The truth however is that we have very much in common with other animals and particularly with the species to which we are most closely relates and with whom we share the most recent common ancestor as we and they evolved and diversified over the same period of time to arrive at our present state.

This is reflected in the nested hierarchies into which the different branches of the evolutionary tree can be arranged in, anatomy, physiology and DNA and in the way our bodies develop through embryology and continued into childhood.


And yet creationists insist we are not only a different species, but a different 'kind' of animal, even a different category of life altogether, even though none of the difference they insist apply to different taxons as evidence of evolution apply to humans in respect of the other great apes.

The common marmoset, Callithrix jacchus, and their evolutionary relationship to humans. The common marmoset (Callithrix jacchus) is a small primate species native to the forests and scrublands of northeastern Brazil. Known for its expressive face, tufted ears, and squirrel-sized body, it’s a popular species for scientific research, primarily because it shares some interesting genetic and behavioural traits with humans. Here’s an overview of its characteristics, behaviour, and evolutionary relationship with humans.

Physical Characteristics
  • Size: Common marmosets are small, weighing only about 300-400 grams, with a body length of 7-10 inches (18-25 cm) and a long, bushy tail.
  • Appearance: They have a distinctive look with white ear tufts, a small face, and wide eyes. Their fur is mostly brownish-grey with a mix of white and black, allowing them to blend into their arboreal habitat.
  • Hands and Feet: Like other New World monkeys, they have claws on most fingers (rather than flat nails like humans), which helps them cling to trees.

Habitat and Diet
  • Environment: Marmosets thrive in forests, especially in areas with dense foliage where they can find food and avoid predators. They’re highly adaptable and can be found in both natural and urbanized settings in Brazil.
  • Diet: They’re omnivores, feeding on tree sap, insects, fruits, and small animals. They use their specialized incisor teeth to gouge tree bark and access sap, which is a key component of their diet.

Social Structure and Behaviour
  • Social Groups: Marmosets live in family groups typically led by a dominant pair. Groups consist of 5-15 individuals, often including multiple generations, with cooperative care of young by both parents and other group members.
  • Communication: Marmosets are highly social and communicate through vocalizations, scents, and body language. They produce different calls depending on the context, and some sounds are ultrasonic, beyond human hearing range.
  • Reproduction: These primates have a unique reproductive system, where dominant females can suppress the reproduction of other females in the group. They often give birth to twins, and group members assist in raising the young, a rare behaviour in mammals that echoes human familial cooperation.

Relationship to Humans

Marmosets belong to the infraorder Simiiformes, which includes all monkeys and apes, meaning they’re more distantly related to humans than other primates like chimpanzees and gorillas, who are part of the hominoid lineage. However, they still share significant genetic similarities with humans—about 92% of their DNA. They’re one of the smallest primates often studied for insights into human aging, neurological diseases, and genetics because of several interesting parallels:
  • Brain and Behaviour: While their brains are much smaller than humans', they share many structural and functional aspects, including similar regions that govern emotions, memory, and sensory processing.
  • Lifespan and Aging: Marmosets age quickly for a primate, with a lifespan of around 12-16 years. They exhibit aging patterns similar to humans, including changes in the immune system, body mass, and cognitive abilities, which is valuable in studying aging processes.
  • Social and Parenting Behaviours: Cooperative parenting and close social bonds within groups mirror certain aspects of human social structures.

Conservation Status

The common marmoset is currently listed as "Least Concern" by the IUCN, though habitat loss and pet trade are concerns. They adapt well to different environments, which has helped their survival, but their populations are still vulnerable to ecological changes.

In summary, while common marmosets diverged from humans over 40 million years ago, their unique traits and social behaviours make them a valuable species for understanding certain aspects of human biology and psychology, providing insight into genetic, neurological, and social characteristics that bridge the gap between humans and other primates.
Now, as though to drive another nail into the coffin of that primitive superstition, scientists have just shown how the brains of humans and the common marmoset monkey follow parallel development, demonstrating their common origins.

Common marmosets and humans have similar prolonged periods of childhood where child care is shared amongst several adults, so the children experience intense socialisation as they develop juts as human children do, and because their brains are fundamentally the same as human brains, the same areas develop in the same way and at the same stage in their development:
Similarities in Brain Development Between Marmosets and Humans
In common marmosets, the brain regions that process social interactions develop very slowly, extending until early adulthood, like in humans. During this time, all group members are involved in raising the infants, which contributes to the species’ strong socio-cognitive skills.
The development of primate brains is shaped by various inputs. However, these inputs differ between independent breeders, such as great apes, and cooperative breeders, such as the common marmoset (Callithrix jacchus) and humans. In these species, group members other than the parents contribute substantially to raising the infants from birth onwards.

A group of international researchers led by Paola Cerrito from the University of Zurich’s Department of Evolutionary Anthropology studied how such social interactions map onto brain development in common marmosets. The study provides new insights into the relationship between the timing of brain development and the socio-cognitive skills of marmosets, in particular their prosocial and cooperative behaviours.

Prolonged learning from social interactions

The research team analysed brain development using magnetic resonance data and showed that in marmosets, the brain regions involved in the processing of social interactions exhibit protracted development – in a similar way to humans. These brain regions only reach maturity in early adulthood, allowing the animals to learn from social interactions for longer.

Like humans, immature marmosets are surrounded and cared for by multiple caregivers from birth and are therefore exposed to intense social interaction. Feeding is also a cooperative business: the immature animals are fed by group members and as they get older they have to beg for food because their mothers are already busy with the next offspring. According to the study, the need to elicit care from several group members significantly shapes brain development and contributes to the sophisticated socio-cognitive motivation (and observed skills) of these primates.

A model for human evolution

Given their similarities with humans, marmosets are an important model for studying the evolution of social cognition.

Our findings underscore the importance of social experiences to the formation of neural and cognitive networks, not only in primates, but also in humans. This insight could have an impact on various fields, ranging from evolutionary biology to neuroscience and psychology.

Paola Cerrito, first author
Department of Evolutionary Anthropology
University of Zurich, Zürich, Switzerland.

The early-life social inputs that characterize infants’ life in cooperatively breeding species may be a driving force in the development of humans marked social motivation.

Publication:
Abstract
Primate brain development is shaped by inputs received during critical periods. These inputs differ between independent and cooperative breeders: In cooperative breeders, infants interact with multiple caregivers. We study how the neurodevelopmental timing of the cooperatively breeding common marmoset maps onto behavioral milestones. To obtain structure-function co-constructions, we combine behavioral, neuroimaging (anatomical and functional), and neural tracing experiments. We find that brain areas critically involved in observing conspecifics interacting (i) develop in clusters, (ii) have prolonged developmental trajectories, (iii) differentiate during the period of negotiations between immatures and multiple caregivers, and (iv) do not share stronger connectivity than with other regions. Overall, developmental timing of social brain areas correlates with social and behavioral milestones in marmosets and, as in humans, extends into adulthood. This rich social input is likely critical for the emergence of their strong socio-cognitive skills. Because humans are cooperative breeders too, these findings have strong implications for the evolution of human social cognition.

INTRODUCTION
Strong social cognition and prosociality are, from a very young age, hallmarks of the human mind compared to the closest living relatives, the nonhuman great apes (1). Because of our peculiar life history, characterized by early weaning and extensive allomaternal care starting from very early in infancy, human development is embedded in a world filled with other individuals, including parents, siblings, and other family members. Thus, this is the context in which human toddlers’ strong social cognition and prosociality develops (2). It is this same period that is also the most important for the formation of the neural bases of higher-order social, emotional, and communicative functions (3). Not unexpectedly then, several independent lines of evidence, spanning neuroscience, pediatrics, primatology, and psychiatry, point to the fundamental role that the relative timing of brain development and social interactions have for the acquisition of social cognition and prosocial behaviors (4).

During ontogeny, total brain volume increases until reaching its adult levels. This volumetric increase is the product of gray matter (GM) volume (GMV) increase until a peak value is reached in childhood, after which it decreases concurrently with synaptic pruning and white matter volumetric increase (5). In addition, the ontogenetic trajectories of cerebral GM are heterochronous, such that both maximum GMV and GM reduction rate vary across brain regions. The importance of the temporal patterns of brain development in shaping the adult phenotype becomes apparent, for example, in the case of autism spectrum disorder (ASD). Deviations from the normal range of developmental timing of the cortex can profoundly affect socio-cognitive skills and are one of the main factors linked to the occurrence of ASD (3). Specifically, several studies have found that early brain overgrowth during the first years of life strongly correlates with ASD [e.g. (6)] and a meta-analysis of all published magnetic resonance imaging (MRI) data by 2005 revealed that the period of greatest brain enlargement in autism is during early childhood (7), with about a 10% volume increase compared to controls during the first year of life. Hence, individuals affected by ASD present an accelerated early-life brain growth and achieve a final brain volume that is not different from that of controls, but they achieve it earlier than controls. Recent works with human brain organoids has confirmed the accelerated maturation of the cortex in the ASD phenotype, especially interneurons (8, 9). Consequently, given this accelerated early-life brain development, fewer social inputs are available during the period when the GMV reduces to adult size and differentiates via experience-dependent pruning. Accelerated development of functional connectivity between certain brain areas [e.g., amygdala–prefrontal cortex (PFC)] can also be a consequence of early-life stress, which, in turn, can cause adverse physiological conditions such as increased anxiety and cortisol levels (10). Unfortunately, so far, nothing is known regarding the impact of changes in brain developmental timing within nonhuman species. That is, we do not know if, within a given nonhuman species, alterations in ontogenetic trajectories of the brain have an impact on the adult behavioral phenotype. However, comparative studies across species with different ontogenetic trajectories and social behaviors can help us shed light on the relationship between the two.

The importance of social inputs occurring during prolonged brain maturation and slow developmental pace has also been highlighted in the context of human evolutionary studies. The remarkable brain growth and development occurring postnatally in humans arguably allows the brain to be influenced by the social environment outside of the uterus to a greater extent than that seen in other great apes (11), who are not cooperative breeders (12). Hawkes and Finlay (13) show that, in addition to weaning our infants earlier than expected (based on allometric scaling with other life-history variables), human neonates have an especially delayed neural development, which is likely correlated with the energetic trade-offs stemming from the large size and high caloric demand of our brain (14). In addition, we observe that, in humans, compared to other great apes, myelination is much prolonged and continues well into adulthood (15).

Common marmosets (Callithrix jacchus) are cooperatively breeding platyrrhine monkeys. Like humans, but unlike other great apes (12), they rely on extensive allomaternal care and share many life-history traits (e.g., short interbirth intervals and a hiatus between menarche and first reproduction) with humans (16). They also show remarkable prosociality (4, 15) [much more than great apes (16)] and strong socio-cognitive abilities, which have been argued to correlate with cooperative breeding (1720). However, the neurobiological features underlying the socio-cognitive abilities promoting the prosocial behavior are poorly understood. Moreover, experimental research has shown that, in common marmosets (hereafter marmosets), there is a critical period for the development of social behaviors (21), although the relationship between developmental timing of the brain and these early-life social interactions is poorly understood.

Given these similarities with humans, marmosets are becoming an ever-more important model in neuroscience (2225) and particularly in research investigating the neurobiological and neurodevelopmental bases of social cognition. As in humans, immature marmosets are surrounded and cared for by multiple caregivers from the first day on. The entire family is typically present during birth, and oxytocin levels increase not only in mothers but also in all group members (26). Group members contribute appreciably to carrying the infants and, once infants start eating solid food, frequently share food with them. After a peak provisioning period, adults are increasingly less willing to share food with them (2729). During this period, intense and noisy negotiations over food are frequent, with immatures babbling and begging and adults eventually giving in—or not. Intriguingly, when doing so, immatures appear to take into account how willing individual adults are to share and will insist in more and longer attempts with adults who are generally less likely to refuse them. Soon after, immatures have to compete for attention and food not only with their twin sibling but also with the next offspring that are born far before they themselves are independent because, like in humans, marmosets are weaned early and mothers have their next offspring soon after (30). By now, the immatures still have not reached puberty; this only happens shortly before yet another set of younger siblings is born. Typically, with these new arrivals, the immatures start to act as helpers themselves and thus face the developmental task of switching from being a recipient of help to becoming a provider of help and prosocial acts (31). This is thus the developmental context in which marmosets’ socio-cognitive skills develop.

The goal of this study is to map these behavioral milestones specific to a cooperatively breeding primate to its region-specific brain development to better understand the social interactions in which infants engage during the differentiation period of brain regions selectively implicated in processing social stimuli. Our working hypothesis is that, like in humans, social interactions with several caregivers during this critical period profoundly contribute to the co-construction of the marmoset brain, the maturation of socially related associative areas, and therefore the emergence of prosocial behaviors. For that purpose, we sought to determine if there is a relationship between the temporal profile of the developing marmoset brain and the early-life social interactions that may help explain their sophisticated socio-cognitive skills at adulthood.

To compare the timing of brain development to that of these behavioral milestones and developmental tasks of attaining nutritional independence, we focused on brain regions that, in adult marmosets, are selectively activated by the observation of social interactions between conspecifics but not by multiple but independently behaving marmosets, as identified by Cléry et al. (32). We tested if these brain regions share similar developmental trajectories based on the developmental patterns of regional GMV. To potentially reveal a coordinated ontogenetic profile underlying the “tuning” of the social brain in marmosets, we then compared these neurodevelopmental patterns to longitudinal data of infant negotiations with caregivers in relation to food (as measured by the frequency of food begging). Last, because it is known that brain regions whose activations correlate with performance on a given task strengthen and get fine-tuned with age (33, 34), we assessed if there is stronger connectedness between areas that develop according to similar developmental trajectories and share similar response to social interaction stimuli.

We thus combined several types of previously published data from marmosets to provide a unified picture of structural brain development alongside the development of social interactions between infants and multiple caregivers necessary to ensure survival (infant provisioning). These included structural MRI (sMRI) data of GM of 53 cortical areas and 16 subcortical nuclei acquired from a developmental cohort (aged 13 to 104 weeks) of 41 male and female marmosets (35), functional MRI (fMRI) data mapping the brain areas activated by the observation of social interactions in marmosets (32), food sharing interactions in five family groups of marmosets including a total of 26 adults and 14 immatures [from 1 to 60 weeks of age (27)], and cellular-resolution data of corticocortical connectivity in marmosets obtained via 143 retrograde tracer injections in 52 young adult marmosets of both sexes (36).

Overall, we make the following predictions:
  1. P1: Cortical regions that show significantly stronger activation during the observation of social interactions (32) share similar structural neurodevelopmental profiles, which are distinct from those regions showing significantly stronger activation during the observation of nonsocial activities.
  2. P2: That those same brain regions showing a significantly stronger activation during the observation of social interactions exhibit a protracted development, reaching their adult volume later than the other regions.
  3. P3: The developmental trajectory of infant negotiations with caregivers in relation to food (as measured by the frequency of food begging) is more similar to that of brain regions responding more strongly to the observation of social interactions than to the other regions.
  4. P4: Functional connectivity is stronger between regions with similar developmental timing and response strength to the observation of either social or nonsocial behaviors and weaker between regions with different developmental timing and response strength.
If the brains of humans an marmosets are fundamentally similar and develop the same way, perhaps a creationist could explain in what way, apart from their tail and their claws in place of human flat finger nails, marmosets are a different 'kind' to humans, and then explain why the same reasoning doesn't place the great apes in the same 'kind' as humans.

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