Dead infant carrying by chimpanzee mothers in the Budongo Forest

It has been suggested that non-human primates (hereafter primates) can respond to deceased conspecifics in ways that suggest they experience psychological states not unlike humans, which would indicate they exhibit some notion of death. Here, we report long-term demographic data from two East African chimpanzee groups. During a combined 40-year observation period we recorded 191 births of which around a third died in infancy, mostly within the first year. We documented the post-mortem behaviour of the mothers and found that Budongo chimpanzee mothers routinely carried deceased infants after their death, usually until the body started to decompose after a few days. However, we also observed three cases of extended carrying lasting for more than 2-weeks, one of which was followed by the unusual extended carrying of a substitute object and another which lasted three months. In each case, the corpses mummified. We discuss these data in view of functional hypotheses of dead infant carrying in primates and regarding the potential proximate mechanisms involved in this behaviour. We suggest that chimpanzees may exhibit psychological processes related to death of conspecifics similar to human grieving.

Characterization of a Novel Splicing Variant in Acylglycerol Kinase (AGK) Associated with Fatal Sengers Syndrome

Mitochondrial functional integrity depends on protein and lipid homeostasis in the mitochondrial membranes and disturbances in their accumulation can cause disease. AGK, a mitochondrial acylglycerol kinase, is not only involved in lipid signaling but is also a component of the TIM22 complex in the inner mitochondrial membrane, which mediates the import of a subset of membrane proteins. AGK mutations can alter both phospholipid metabolism and mitochondrial protein biogenesis, contributing to the pathogenesis of Sengers syndrome. We describe the case of an infant carrying a novel homozygous AGK variant, c.518+1G>A, who was born with congenital cataracts, pielic ectasia, critical congenital dilated myocardiopathy, and hyperlactacidemia and died 20 h after birth. Using the patient’s DNA, we performed targeted sequencing of 314 nuclear genes encoding respiratory chain complex subunits and proteins implicated in mitochondrial oxidative phosphorylation (OXPHOS). A decrease of 96-bp in the length of the AGK cDNA sequence was detected. Decreases in the oxygen consumption rate (OCR) and the OCR:ECAR (extracellular acidification rate) ratio in the patient’s fibroblasts indicated reduced electron flow through the respiratory chain, and spectrophotometry revealed decreased activity of OXPHOS complexes I and V. We demonstrate a clear defect in mitochondrial function in the patient’s fibroblasts and describe the possible molecular mechanism underlying the pathogenicity of this novel AGK variant. Experimental validation using in vitro analysis allowed an accurate characterization of the disease-causing variant.

Rate of infant carrying impacts infant spontaneous motor tempo

Rhythm production is a critical component of human interaction, not least forming the basis of our musicality. Infants demonstrate a spontaneous motor tempo (SMT), or natural rate of rhythmic movement. Here, we ask whether infant SMT is influenced by the rate of locomotion infants experience when being carried. Ten-month-old, non-walking infants were tested using a free drumming procedure before and after 10 min of being carried by an experimenter walking at a slower (98 BPM) or faster (138 BPM) than average tempo. We find that infant SMT is differentially impacted by carrying experience dependent on the tempo at which they were carried: infants in the slow-walked group exhibited a slower SMT from pre-test to post-test, while infants in the fast-walked group showed a faster SMT from pre-test to post-test. Heart rate data suggest that this effect is not due to a general change in the state of arousal. We argue that being carried during caregiver locomotion is a predominant experience for infants throughout the first years of life, and as a source of regular, vestibular, information, may at least partially form the basis of their sense of rhythm.

Delivering Clinically on Our Knowledge of Oxytocin and Sensory Stimulation: The Potential of Infant Carrying in Primary Prevention

Oxytocin (OT) is one of the most intensively researched neuropeptides during the three past decades. In benign social contexts, OT exerts a range of desirable socioemotional, stress-reducing, and immunoregulatory effects in mammals and humans and influences mammalian parenting. Consequentially, research in potential pharmacological applications of OT toward human social deficits/disorders and physical illness has increased substantially. Regrettably, the results from the administration of exogenous OT are still relatively inconclusive. Research in rodent maternal developmental programming has demonstrated the susceptibility of offspring endogenous OT systems to maternal somatosensory stimulation, with consequences for behavioral, epigenetic, cognitive, and neurological outcomes. A translation of this animal research into practically feasible human parenting recommendations has yet to happen, despite the significant prevention potential implied by the maternal developmental programming research. Extended physical contact with full-term healthy infants in the months following birth (infant carrying) might constitute the human equivalent of those specific rodent maternal behaviors, found to positively influence emerging OT systems. Findings from both OT and maternal programming research parallel those found for infants exposed to such extended parental physical contact, whether through skin-to-skin contact or infant carrying. Clinical support of parents to engage in extended physical contact represents a feasible intervention to create optimum conditions for the development of infant OT systems, with potential beneficial long-term health effects.

Rate of infant carrying predicts infant spontaneous motor tempo

Rhythm production is a critical component of human interaction, not least forming the basis of our musicality. Infants demonstrate a Spontaneous Motor Tempo (SMT), or natural rate of rhythmic movement. Here we ask whether infant SMT is influenced by the rate of loco- motion infants experience when being carried. Ten-month-old, non-walking infants were tested using a free drumming procedure before and after ten minutes of being carried by an experimenter walking at a slower (98 BPM) or faster (138 BPM) than average tempo. We find that infant SMT is differentially impacted by carrying experience dependent on the tempo at which they were carried: Infants in the slow-walked group exhibited a slower SMT from pre-test to post-test, whilst infants in the fast-walked group showed a faster SMT from pre-test to post-test. Heart rate data suggest that this effect is not due to a general change in state of arousal. We argue that being carried during caregiver locomotion is a predominant experience for infants throughout the first years of life, and as a source of regular, vestibular, information, may at least partially form the basis of their sense of rhythm.

Challenging infant-directed singing as a credible signal of maternal attention

I challenge Mehr et al.'s contention that ancestral mothers were reluctant to provide all the attention demanded by their infants. The societies in which music emerged likely involved foraging mothers who engaged in extensive infant carrying, feeding, and soothing. Accordingly, their singing was multimodal, its rhythms aligned with maternal movements, with arousal regulatory consequences for singers and listeners.

Oxytocin receptor binding in the titi monkey hippocampal formation is associated with parental status and partner affiliation

Social cognition is facilitated by oxytocin receptors (OXTR) in the hippocampus, a brain region that changes dynamically with pregnancy, parturition, and parenting experience. We investigated the impact of parenthood on hippocampal OXTR in male and female titi monkeys, a pair-bonding primate species that exhibits biparental care of offspring. We hypothesized that in postmortem brain tissue, OXTR binding in the hippocampal formation would differ between parents and non-parents, and that OXTR density would correlate with frequencies of observed parenting and affiliative behaviors between partners. Subjects were 10 adult titi monkeys. OXTR binding in the hippocampus (CA1, CA2/3, CA4, dentate gyrus, subiculum) and presubiculum layers (PSB1, PSB3) was determined using receptor autoradiography. The average frequency of partner affiliation (Proximity, Contact, and Tail Twining) and infant carrying were determined from longitudinal observations (5–6 per day). Analyses showed that parents exhibited higher OXTR binding than non-parents in PSB1 (t(8) = − 2.33, p = 0.048), and that OXTR binding in the total presubiculm correlated negatively with Proximity (r = − 0.88) and Contact (r = − 0.91), but not Tail Twining or infant carrying. These results suggest that OXTR binding in the presubiculum supports pair bonding and parenting behavior, potentially by mediating changes in hippocampal plasticity.

Reactions to infant death by wild vervet monkeys (Chlorocebus pygerythrus) in KwaZulu-Natal, South Africa: prolonged carrying, non-mother carrying, and partial maternal cannibalism

Observations of dead infant carrying have been reported for many primate species, and researchers have proposed several hypotheses to explain this behaviour. However, despite being a relatively well-studied species, reports of dead infant carrying in wild vervet monkeys (Chlorocebus pygerythrus) remain scarce. Here we report 14 observations of dead infant carrying by female vervet monkeys in a population at Mawana Game Reserve, KwaZulu-Natal, South Africa. Most of the females carried the dead infant for a day or less, but one female carried her infant for at least 14 days. In one case the maternal sister of a dead infant carried it after the death of their mother. We also report a case of mother-infant cannibalism: a female consumed part of her deceased infant’s tail. Other post-mortem care-taking behaviours such as grooming, smelling and licking were also recorded. Of 97 recorded infant deaths in this study population since 2010, 14.4% are known to have elicited dead infant carrying, a proportion similar to that reported for other monkey species. We discuss our observations in relation to various hypotheses about this behaviour, including the post-parturition hormones hypothesis, learning to mother hypothesis, and unawareness of death hypothesis.