Phenotypic and genetic associations between gray matter covariation and tool use skill in chimpanzees (Pan troglodytes): Repeatability in two genetically isolated populations.

Humans and chimpanzees both exhibit a diverse set of tool use skills which suggests selection for tool manufacture and use occurred in the common ancestors of the two species. Our group has previously reported phenotypic and genetic associations between tool use skill and gray matter covariation, as quantified by source-based morphometry (SBM), in chimpanzees. As a follow up study, here we evaluated repeatability in heritability in SBM components and their phenotypic association with tool use skill in two genetically independent chimpanzee cohorts. Within the two independent cohorts of chimpanzees, we identified 8 and 16 SBM components, respectively. Significant heritability was evident for multiple SBM components within both cohorts. Further, phenotypic associations between tool use performance and the SBM components were largely consistent between the two cohorts; the most consistent finding being an association between tool use performance and an SBM component including the posterior superior temporal sulcus (STS) and superior temporal gyrus (STG), and the interior and superior parietal regions (p < 0.05). These findings indicate that the STS, STG, and parietal cortices are phenotypically and genetically implicated in chimpanzee tool use abilities.

Age- and sex-related differences in baboon (Papio anubis) gray matter covariation.

Age-related changes in cognition, brain morphology, and behavior are exhibited in several primate species. Baboons, like humans, naturally develop Alzheimer's disease-like pathology and cognitive declines with age and are an underutilized model for studies of aging. To determine age-related differences in gray matter covariation of 89 olive baboons (Papio anubis), we used source-based morphometry (SBM) to analyze data from magnetic resonance images. We hypothesized that we would find significant age effects in one or more SBM components, particularly those which include regions influenced by age in humans and other nonhuman primates (NHPs). A multivariate analysis of variance revealed that individual weighted gray matter covariation scores differed across the age classes. Elderly baboons contributed significantly less to gray matter covariation components including the brainstem, superior parietal cortex, thalamus, and pallidum compared to juveniles, and middle and superior frontal cortex compared to juveniles and young adults (p < 0.05). Future studies should examine the relationship between the changes in gray matter covariation reported here and age-related cognitive decline.

Termite fishing laterality in the Fongoli savanna chimpanzees (Pan troglodytes verus): further evidence of a left hand preference.

Whether nonhuman primates show population-level handedness is a topic of much scientific debate. A previous study of handedness for termite fishing reported population-level left handedness in the chimpanzees from Gombe National Park, Tanzania. In the current study, we examined whether similar hand preferences were evident in a savanna-dwelling chimpanzee population with regards to termite fishing. Hand preference data were collected for 27 chimpanzees from February 2007 through July 2008 and November 2011 through January 2012 in southeastern Senegal. Overall, the Fongoli chimpanzees demonstrate a trend toward population-level handedness, though the results did not reach conventional levels of statistical significance likely due to the limited sample size. Fongoli chimpanzees showed the same pattern of left hand preference as reported at Gombe and the two populations did not differ significantly. When the data were combined across all studies, wild chimpanzees showed a population-level left hand preference for termite fishing.

A neuroanatomical predictor of mirror self-recognition in chimpanzees.

The ability to recognize one's own reflection is shared by humans and only a few other species, including chimpanzees. However, this ability is highly variable across individual chimpanzees. In humans, self-recognition involves a distributed, right-lateralized network including frontal and parietal regions involved in the production and perception of action. The superior longitudinal fasciculus (SLF) is a system of white matter tracts linking these frontal and parietal regions. The current study measured mirror self-recognition (MSR) and SLF anatomy in 60 chimpanzees using diffusion tensor imaging. Successful self-recognition was associated with greater rightward asymmetry in the white matter of SLFII and SLFIII, and in SLFIII's gray matter terminations in Broca's area. We observed a visible progression of SLFIII's prefrontal extension in apes that show negative, ambiguous, and compelling evidence of MSR. Notably, SLFIII's terminations in Broca's area are not right-lateralized or particularly pronounced at the population level in chimpanzees, as they are in humans. Thus, chimpanzees with more human-like behavior show more human-like SLFIII connectivity. These results suggest that self-recognition may have co-emerged with adaptations to frontoparietal circuitry.

The influence of AVPR1A genotype on individual differences in behaviors during a mirror self-recognition task in chimpanzees (Pan troglodytes).

The mark/rouge test has been used to assess mirror self-recognition (MSR) in many species. Despite consistent evidence of MSR in great apes, genetic or non-genetic factors may account for the individual differences in behavioral responses that have been reported. We examined whether vasopressin receptor gene (AVPR1A) polymorphisms are associated with MSR-related behaviors in chimpanzees since vasopressin has been implicated in the development and evolution of complex social relations and cognition and chimpanzees are polymorphic for the presence of the RS3-containing DupB region. We compared a sample of DupB+/- and DupB-/- chimpanzees on a mark test to assess its role on social behavior toward a mirror. Chimpanzees were administered two, 10-min sessions where frequencies of mirror-guided self-directed behaviors, contingent actions and other social behaviors were recorded. Approximately one-third showed evidence of MSR and these individuals exhibited more mirror-guided self-exploratory behaviors and mouth contingent actions than chimpanzees not classified as passers. Moreover, DupB+/- males exhibited more scratching and agonistic behaviors than other male and female cohorts. Our findings support previous studies demonstrating individual differences in MSR abilities in chimpanzees and suggest that AVPR1A partly explains individual differences in MSR by influencing the behavioral reactions of chimpanzees in front of a mirror.

DUF1220 protein domains drive proliferation in human neural stem cells and are associated with increased cortical volume in anthropoid primates.

Genome sequences encoding DUF1220 protein domains show a burst in copy number among anthropoid species and especially humans, where they have undergone the greatest human lineage-specific copy number expansion of any protein coding sequence in the genome. While DUF1220 copy number shows a dosage-related association with brain size in both normal populations and in 1q21.1-associated microcephaly and macrocephaly, a function for these domains has not yet been described. Here we provide multiple lines of evidence supporting the view that DUF1220 domains function as drivers of neural stem cell proliferation among anthropoid species including humans. First, we show that brain MRI data from 131 individuals across 7 anthropoid species shows a strong correlation between DUF1220 copy number and multiple brain size-related measures. Using in situ hybridization analyses of human fetal brain, we also show that DUF1220 domains are expressed in the ventricular zone and primarily during human cortical neurogenesis, and are therefore expressed at the right time and place to be affecting cortical brain development. Finally, we demonstrate that in vitro expression of DUF1220 sequences in neural stem cells strongly promotes proliferation. Taken together, these data provide the strongest evidence so far reported implicating DUF1220 dosage in anthropoid and human brain expansion through mechanisms involving increasing neural stem cell proliferation.

Hemispheric specialization for local and global processing of hierarchical visual stimuli in chimpanzees (Pan troglodytes).

This study examined laterality in global and local processing of hierarchical compound stimuli in seven chimpanzees (Pan troglodytes). A divided visual half-field paradigm was used that allowed for unilateral presentation of compound stimuli to either the left or right hemisphere. Comparison stimuli differing on the basis of their global configuration, local elements or both features followed sample stimulus presentation. Subjects were required to accurately discriminate the comparison stimuli on the basis of these features relative to the sample stimulus. No laterality effects were found for accuracy; however, for reaction time, a significant interaction was found between visual field and processing mode. An overall right visual field advantage was found for local processing but no visual field differences for global processing. The overall results are consistent with previous findings in humans and suggests homologous lateralization in chimpanzees and humans.

The effect of situational factors on hand preferences for feeding in 177 captive chimpanzees (Pan troglodytes).

This study examined the effect of situational factors on hand use for feeding in a sample of captive chimpanzees. Lateral bias in hand use was tested in biased and unbiased testing circumstances to assess strength and consistency in hand preference. For both unbiased and biased testing conditions, population-level right hand preferences were found for the sample. In the biased condition, subjects were more likely to overcome positional factors in order to feed with their right hand contrasted with the left. Overall, hand use in the biased and unbiased testing conditions was significantly positively correlated. In terms of strength of hand use, juveniles were found to be less lateralized than sub-adults and adults. Moreover, juvenile females were found to be more lateralized than juvenile males. Taken together, the data suggest that chimpanzee hand preferences for feeding are not constrained by situational factors and are relatively consistent in biased and unbiased testing conditions.

Asymmetries in cerebral width in nonhuman primate brains as revealed by magnetic resonance imaging (MRI).

A comparative study of asymmetries in cerebral width was conducted in a sample of great apes, Old World and New World monkeys. The brains of all subjects were scanned using magnetic resonance imaging (MRI) and the first axial slice above the third ventricle was identified. Measures of cerebral width were taken at distances of 10% and 30% of the length from the occipital and frontal poles. Cerebral widths were measured from the midline to the lateral surface of the brain for each area. The great apes exhibited a right-frontal and left-occipital directional asymmetry in cerebral width. In contrast, no significant mean directional asymmetries were found in either the Old or New World monkeys. The results in the great apes are consistent with previous reports of petalia asymmetries and suggest that the use of MRI is a valid approach to the assessment of neuroanatomical asymmetries in primates.

Birth order and left-handedness revisited: some recent findings in chimpanzees (Pan troglodytes) and their implications for developmental and evolutionary models of human handedness.

This paper examines the relationship between parity, pregnancy outcome, and handedness in a sample of captive chimpanzees (Pan troglodytes). The relation between parity, maternal age and positive or negative pregnancy outcome was assessed from life history data for 536 chimpanzees housed at the Yerkes Regional Primate Research Center. The incidences of negative pregnancy outcome (notably spontaneous abortions and stillbirths) were significantly higher in parities of 8 or higher compared to all other parities. In a sub-sample of 165 chimpanzees, the relation between parity, maternal age and handedness was assessed to determine whether left handedness may serve as a marker of prenatal pathology. These analyses indicated that left-handedness was more prevalent in 1st and 8 or higher parities compared to parities between 2 and 7, respectively. Possible prenatal hormonal and periparturitional factors are discussed as possible mechanisms for the observed findings.

Haptic discrimination in capuchin monkeys (Cebus apella): evidence of manual specialization.

Two experiments investigated the effects of haptic and visual discrimination on hand preference in 22 brown capuchin monkeys (Cebus apella). The percentage of left-handed subjects in Experiment 1 were 63.6%, 45.5%, and 18.2% for haptic, bipedal, and quadrupedal reaching, respectively. In Experiment 2, the haptic demands of the task were manipulated by using additional food types and another tactile medium. Left-hand preferences were further strengthened when reaching into water compared to pineshavings in Experiment 1. Reaching with no tactile interference resulted in equal numbers of lateralized and nonlateralized subjects. These results show that when reaching demands the use of haptic cues, as opposed to visual ones, monkeys shift towards greater left hand use. This is consistent with what is known about right hemisphere superiority for haptic discrimination in humans.

Mirror-image matching and mental rotation problem solving by baboons (Papio papio): unilateral input enhances performance.

Three experiments, using a matching-to-sample procedure, were conducted to examine hemispheric specialization in mirror-image discrimination and mental rotation in baboons (Papio papio). In Experiment 1, no significant difference was found in discrimination of mirror-image and asymmetric pattern stimuli. In Experiment 2, orientation discrimination was assessed within the left (LVF) and right (RVF) visual half-fields. An RVF advantage was found in accuracy for asymmetric patterns, whereas an LVF advantage was found for discrimination of mirror-image stimuli. No significant relation was found between angular disparity of the stimuli and response time. Experiment 3 examined the effect of bilateral visual input on accuracy and response time. Significantly lower accuracy and longer response times were found for bilateral compared with unilateral visual input.

Evidence for asymmetrical hemispheric priming using known and unknown warning stimuli in two language-trained chimpanzees (Pan troglodytes).

In this article results are reported from 3 warning stimulus-priming experiments that assessed hemisphere-specific activation and lateralization in 2 language-trained chimpanzees (Pan troglodytes). Results from Experiment 1 indicated a right visual field advantage in priming for meaningful warning stimuli presented in blocks of 36 trials. In Experiments 2 and 3, randomized presentations of meaningful, familiar, and meaningless stimuli resulted in right visual field advantages for meaningful warning stimuli. No visual half-field differences were found for familiar or meaningless warning stimuli. The findings are similar to those found in human subjects using known-unknown symbol paradigms; they suggest that basic phylogenetic neuropsychological systems related to activation and priming processes may link nonhuman primate and human studies of lateralization.

Spontaneous symbol acquisition and communicative use by pygmy chimpanzees (Pan paniscus).

Two pygmy chimpanzees (Pan paniscus) have spontaneously begun to use symbols to communicate with people. In contrast to common chimpanzees (Pan troglodytes) using the same communicative system, the pygmy chimpanzees did not need explicit training in order to form referential symbol-object associations. Instead, they acquired symbols by observing others use these symbols in daily communications with them. In addition, the pygmy chimpanzees have begun to comprehend spoken English words and can readily identify lexigrams upon hearing the spoken words. By contrast, common chimpanzees who received similar exposure to spoken English are unable to do so. The older pygmy chimpanzee has begun to form requests of the form agent-verb-recipient in which he is neither the agent nor the recipient. By contrast, similarly aged common chimpanzees limited their requests to simple verbs, in which the agent was always presumed to be the addressee and the chimpanzee itself was always the recipient, thus they had no need to indicate a specific agent or recipient. These results suggest that these pygmy chimpanzees exhibit symbolic and auditory perceptual skills that are distinctly different from those of common chimpanzees.

Asymmetries in spontaneous head orientation in infant chimpanzees (Pan troglodytes).

Behavioral laterality in head orientation while sleeping in either a supine or prone posture was examined in 43 chimpanzees (Pan troglodytes) for the first 3 months of life. An overall significant right-side lateral bias was found for head orientation in the supine posture. A trend toward greater right-side bias in females compared with males was observed but failed to reach significance. These data suggest that asymmetries in head orientation are present early in life in chimpanzees, and they may be correlated with functional asymmetries observed in adulthood.

Laterality for visual-spatial processing in two language-trained chimpanzees (Pan troglodytes).

Most reviews of laterality in nonhuman primates indicate that hemispheric asymmetries, similar to those found in humans, are not evident. With the growing evidence for cognitive processes germane to language in apes, in addition to their phylogenetic similarity to humans, they appear to be useful candidates for studies of laterality. Laterality for visual-spatial processing in two language-trained chimpanzees (Pan troglodytes) was investigated with a visual half-field paradigm. Initially, the chimpanzees were taught to manipulate a joystick that controlled the movement of a cursor on a computer monitor to a central fixation point. Subjects were then taught a visual discrimination based on the location of a short line contained within a geometric form. Testing consisted of systematic presentation rates of 15, 122, and 226 ms to the left and right visual fields. For half of the trials, subjects used their left hand to respond and, alternately, used the right hand for the remaining trials. Accuracy and reaction time were the dependent measures. One subject demonstrated significantly faster reaction times to stimuli presented to the left visual field (LVF) regardless of which hand was used to respond. The other subject demonstrated a significant LVF bias when using the left hand to respond. The results are discussed in the context of current theories on the evolution of laterality and its relation to linguistic functioning.

A comparative MRI study of the relationship between neuroanatomical asymmetry and interhemispheric connectivity in primates: implication for the evolution of functional asymmetries.

The authors tested the theory that hemispheric specialization evolved as a consequence of reduced interhemispheric connectivity by examining whether neuroanatomical asymmetries were associated with variation in the ratio of corpus callosum size to brain volume (CC:VOL) and to neocortical surface area (CC:NEO) in human and nonhuman primates. Magnetic resonance images were collected in a sample of 45 primates including 8 New World monkeys, 10 Old World monkeys, 4 lesser apes, 17 great apes, and 6 humans. CC:VOL and CC:NEO were determined and correlated with measures of brain asymmetry. The results indicate that brain asymmetry significantly predicted CC:VOL and CC:NEO. Subsequent analyses revealed that species variation in functional asymmetries in the form of handedness are also inversely related to CC:NEO. Taken together, these results support the hypothesis that leftward brain asymmetries may have evolved as a consequence of reduced interhemispheric connectivity.

Lateralized changes in tympanic membrane temperature in relation to different cognitive tasks in chimpanzees (Pan troglodytes).

Lateralized changes in tympanic membrane (TM) temperature were assessed in chimpanzees. Subjects were engaged in 1 of 3 different cognitive tasks, including matching-to-sample, visual-spatial discrimination, and a motor task. During execution of each task, TM temperatures were taken from each ear over a 20-min time period. The TM temperatures at each time interval were subtracted from a baseline measure to assess relative change in blood flow. For the matching-to-sample and visual-spatial discrimination tasks, significant lateralized changes in TM temperature were found, with left-ear temperature increasing and right-ear temperature decreasing. No laterality effects were found for the motor or control tasks. These data provide the first evidence of laterality in physiological functioning in chimpanzees and suggest that transient asymmetries in cognitive functions are associated with changes in cerebral blood flow as assessed by TM temperature change.

Neuroanatomical localization of the motor hand area with magnetic resonance imaging: the left hemisphere is larger in great apes.

Magnetic resonance images of the brain were obtained from 2 gorillas (Gorilla gorilla gorilla), 4 orangutans (Pongo pygmaeus), 14 chimpanzees (Pan troglodytes), and 4 bonobos (Pan paniscus). The region on the motor cortex of humans identified as responsible for motor skill of the hand (the "knob") was identified in this sample on consecutive 1-mm axial scans. The shape of the knob area was traced on each scan from both hemispheres, and the area from all scans was summed to calculate the knob volume. The width of the knob was also measured and correlated highly with knob volume. A significant population-level leftward asymmetry in the volume and width of the knob was revealed (p < .05). Species differences in knob asymmetry and overall volume were not significant, but the variability in overall volume between species was substantial. Selection for the evolution of a neuroanatomical representation of the hand in primates and an evolutionary trend toward population-level right handedness are discussed.