Earliest evidence of primate captivity and translocation supports gift diplomacy between Teotihuacan and the Maya.

A multimethod archaeometry study (zooarchaeological, isotopic, ancient DNA, paleobotanical, and radiocarbon dating) of a spider monkey sacrificed in the ceremonial center of Teotihuacan, Mexico (1 to 550 CE) is interpreted as a diplomatic gift exchange with neighboring Maya. Not only does this spider monkey provide the earliest known instance of primate translocation and captivity in Mesoamerica, it helps date incipient modes of interregional diplomacy between two major powers during Early Classic Mesoamerica: Teotihuacan and the Maya. Details of human-primate interaction include age at capture and transport (before ∼3 y of age), captive duration (over 2 y), anthropogenic diet (staple was maize, though secondary resources unique to anthropogenic diet including arrowroot and chili pepper were also found), context of sacrifice (tethered and associated with complete golden eagle and an array of other statecrafts), and general site context (including presence of Maya vessels and Maya-style murals). The timing of the spider monkey's sacrifice (250 to 300 CE) and its life history suggest a reconsideration of epigraphically attested militaristic involvement of Teotihuacan at certain Maya sites. We propose that a period of more multilateral and fluid ritual exchange with Maya dignitaries preceded the Teotihuacan state's eventual ascent to prominence.

Gastric emphysema and pneumatosis intestinalis in two common marmosets with duodenal dilation syndrome.

BACKGROUND: Common marmosets (Callithrix jacchus) are widely used as primate experimental models in biomedical research. Duodenal dilation with chronic vomiting in captive common marmosets is a recently described life-threatening syndrome that is problematic for health control. However, the pathogenesis and cause of death are not fully understood. CASE PRESENTATION: We report two novel necropsy cases in which captive common marmosets were histopathologically diagnosed with gastric emphysema (GE) and pneumatosis intestinalis (PI). Marmoset duodenal dilation syndrome was confirmed in each case by clinical observation of chronic vomiting and by gross necropsy findings showing a dilated, gas-filled and fluid-filled descending duodenum that adhered to the ascending colon. A diagnosis of GE and PI was made on the basis of the bubble-like morphology of the gastric and intestinal mucosa, with histological examination revealing numerous vacuoles diffused throughout the lamina propria mucosae and submucosa. Immunostaining for prospero homeobox 1 and CD31 distinguished gas cysts from blood and lymph vessels. The presence of hepatic portal venous gas in case 1 and possible secondary bacteremia-related septic shock in case 2 were suggested to be acute life-threatening abdominal processes resulting from gastric emphysema and pneumatosis intestinalis. CONCLUSIONS: In both cases, the gross and histopathological findings of gas cysts in the GI tract walls matched the features of human GE and PI. These findings contribute to clarifying the cause of death in captive marmosets that have died of gastrointestinal diseases.

Spectral Power in Marmoset Frontal Motor Cortex during Natural Locomotor Behavior.

During primate arboreal locomotion, substrate orientation modifies body axis orientation and biomechanical contribution of fore- and hindlimbs. To characterize the role of cortical oscillations in integrating these locomotor demands, we recorded electrocorticographic activity from left dorsal premotor, primary motor, and supplementary motor cortices of three common marmosets moving across a branch-like small-diameter pole, fixed horizontally or vertically. Animals displayed behavioral adjustments to the task, namely, the horizontal condition mainly induced quadrupedal walk with pronated/neutral forelimb postures, whereas the vertical condition induced walk and bound gaits with supinated/neutral postures. Examination of cortical activity suggests that ß (16-35 Hz) and γ (75-100 Hz) oscillations could reflect different processes in locomotor adjustments. During task, modulation of γ ERS by substrate orientation (horizontal/vertical) and epoch (preparation/execution) suggests close tuning to movement dynamics and biomechanical demands. ß ERD was essentially modulated by gait (walk/bound), which could illustrate contribution to movement sequence and coordination. At rest, modulation of ß power by substrate orientation underlines its role in sensorimotor processes for postural maintenance.

Secondary somatosensory cortex of primates: beyond body maps, toward conscious self-in-the-world maps.

Recent human imaging studies have revealed the involvement of the secondary somatosensory cortex (SII) in processes that require high-level information integration, such as self-consciousness, social relations, whole body representation, and metaphorical extrapolations. These functions are far beyond its known role in the formation of body maps (even in their most complex forms), requiring the integration of different information modalities in addition to somatosensory information. However, no evidence of such complex processing seems to have been detected at the neuronal level in animal experiments, which would constitute a major discrepancy between human and non-human animals. This article scrutinizes this gap, introducing experimental evidence of human and non-human primates' SII functions set in context with their evolutionary significance and mechanisms, functionally situating the human SII as a primate brain. Based on the presented data, a new concept of a somatocentric holistic self is proposed, represented as a more comprehensive body-in-the-world map in the primate SII, taking into account evolutionary aspects that characterize the human SII and its implication in the emergence of self-consciousness. Finally, the idea of projection is introduced from the viewpoint of cognitive science, providing a logical explanation to bridge this gap between observed behavior and neurophysiological data.

Individual identity and affective valence in marmoset calls: in vivo brain imaging with vocal sound playback.

As with humans, vocal communication is an important social tool for nonhuman primates. Common marmosets (Callithrix jacchus) often produce whistle-like 'phee' calls when they are visually separated from conspecifics. The neural processes specific to phee call perception, however, are largely unknown, despite the possibility that these processes involve social information. Here, we examined behavioral and whole-brain mapping evidence regarding the detection of individual conspecific phee calls using an audio playback procedure. Phee calls evoked sound exploratory responses when the caller changed, indicating that marmosets can discriminate between caller identities. Positron emission tomography with [18F] fluorodeoxyglucose revealed that perception of phee calls from a single subject was associated with activity in the dorsolateral prefrontal, medial prefrontal, orbitofrontal cortices, and the amygdala. These findings suggest that these regions are implicated in cognitive and affective processing of salient social information. However, phee calls from multiple subjects induced brain activation in only some of these regions, such as the dorsolateral prefrontal cortex. We also found distinctive brain deactivation and functional connectivity associated with phee call perception depending on the caller change. According to changes in pupillary size, phee calls from a single subject induced a higher arousal level compared with those from multiple subjects. These results suggest that marmoset phee calls convey information about individual identity and affective valence depending on the consistency or variability of the caller. Based on the flexible perception of the call based on individual recognition, humans and marmosets may share some neural mechanisms underlying conspecific vocal perception.

Cortical control of object-specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study.

KEY POINTS: The cortical mechanisms of grasping have been extensively studied in macaques and humans; here, we investigated whether common marmosets could rely on similar mechanisms despite strong differences in hand morphology and grip diversity. We recorded electrocorticographic activity over the sensorimotor cortex of two common marmosets during the execution of different grip types, which allowed us to study cortical activity (power spectrum) and physiologically inferred connectivity (phase-slope index). Analyses were performed in beta (16-35 Hz) and gamma (75-100 Hz) frequency bands and our results showed that beta power varied depending on grip type, whereas gamma power displayed clear epoch-related modulation. Strength and direction of inter-area connectivity varied depending on grip type and epoch. These findings suggest that fundamental control mechanisms are conserved across primates and, in future research, marmosets could represent an adequate model to investigate primate brain mechanisms. ABSTRACT: The cortical mechanisms of grasping have been extensively studied in macaques and humans. Here, we investigated whether common marmosets could rely on similar mechanisms despite striking differences in manual dexterity. Two common marmosets were trained to grasp-and-pull three objects eliciting different hand configurations: whole-hand, finger and scissor grips. The animals were then chronically implanted with 64-channel electrocorticogram arrays positioned over the left premotor, primary motor and somatosensory cortex. Power spectra, reflecting predominantly cortical activity, and phase-slope index, reflecting the direction of information flux, were studied in beta (16-35 Hz) and gamma (75-100 Hz) bands. Differences related to grip type, epoch (reach, grasp) and cortical area were statistically assessed. Results showed that whole-hand and scissor grips triggered stronger beta desynchronization than finger grip. Task epochs clearly modulated gamma power, especially for finger and scissor grips. Considering effective connectivity, finger and scissor grips evoked stronger outflow from primary motor to premotor cortex, whereas whole-hand grip displayed the opposite pattern. These findings suggest that fundamental control mechanisms, relying on adjustments of cortical activity and connectivity, are conserved across primates. Consistently, marmosets could represent a good model to investigate primate brain mechanisms.

Faecal transplantation for the treatment of Clostridium difficile infection in a marmoset.

BACKGROUND: The common marmoset has been used as an experimental animal for various purposes. Because its average weight ranges from 250 to 500 g, weight loss quickly becomes critical for sick animals. Therefore, effective and non-stressful treatment for chronic diseases, including diarrhoea, is essential. CASE PRESENTATION: We report a case in which faecal microbiota transplantation (FMT) led to immediate recovery from chronic and recurrent diarrhoea caused by Clostridium difficile infection. A male common marmoset experienced chronic diarrhoea after antibiotic treatments. The animal experienced severe weight loss, and a faecal sample was confirmed to be C. difficile-positive but was negative for protozoa. Metronidazole was partially effective at the first administration but not after the recurrence of the clinical signs. Then, oral FMT was administered to the subject by feeding fresh faeces from healthy individuals mixed with the marmoset's usual food. We monitored the faeces by categorization into four groups: normal, loose, diarrhoea, and watery. After the first day of FMT treatment, the marmoset underwent a remarkable recovery from diarrhoea, and after the fourth day of treatment, a test for C. difficile was negative. The clinical signs did not recur. The marmoset recovered from sinusitis and bilateral dacryocystitis, which also did not recur, as a by-product of the improvement in its general health caused by the cessation of diarrhoea after the FMT. CONCLUSION: This is the first reported case of successful treatment of a marmoset using oral FMT. As seen in human patients, FMT was effective for the treatment of recurrent C. difficile infection in a captive marmoset.

Visual Responsiveness of Neurons in the Secondary Somatosensory Area and its Surrounding Parietal Operculum Regions in Awake Macaque Monkeys.

Previous neurophysiological studies performed in macaque monkeys have shown that the secondary somatosensory cortex (SII) is essentially engaged in the processing of somatosensory information and no other sensory input has been reported. In contrast, recent human brain-imaging studies have revealed the effects of visual and auditory stimuli on SII activity, which suggest multisensory integration in the human SII. To determine whether multisensory responses of the SII also exist in nonhuman primates, we recorded single-unit activity in response to visual and auditory stimuli from the SII and surrounding regions in 8 hemispheres from 6 awake monkeys. Among 1157 recorded neurons, 306 neurons responded to visual stimuli. These visual neurons usually responded to rather complex stimuli, such as stimulation of the peripersonal space (40.5%), observation of human action (29.1%), and moving-object stimulation outside the monkey's reach (23.9%). We occasionally applied auditory stimuli to visual neurons and found 10 auditory-responsive neurons that exhibited somatosensory responses. The visual neurons were distributed continuously along the lateral sulcus covering the entire SII, along with other somatosensory neurons. These results highlight the need to investigate novel functional roles-other than somesthetic sensory processing-of the SII.

Common therapeutic mechanisms of pallidal deep brain stimulation for hypo- and hyperkinetic movement disorders.

Abnormalities in cortico-basal ganglia (CBG) networks can cause a variety of movement disorders ranging from hypokinetic disorders, such as Parkinson's disease (PD), to hyperkinetic conditions, such as Tourette syndrome (TS). Each condition is characterized by distinct patterns of abnormal neural discharge (dysrhythmia) at both the local single-neuron level and the global network level. Despite divergent etiologies, behavioral phenotypes, and neurophysiological profiles, high-frequency deep brain stimulation (HF-DBS) in the basal ganglia has been shown to be effective for both hypo- and hyperkinetic disorders. The aim of this review is to compare and contrast the electrophysiological hallmarks of PD and TS phenotypes in nonhuman primates and discuss why the same treatment (HF-DBS targeted to the globus pallidus internus, GPi-DBS) is capable of ameliorating both symptom profiles. Recent studies have shown that therapeutic GPi-DBS entrains the spiking of neurons located in the vicinity of the stimulating electrode, resulting in strong stimulus-locked modulations in firing probability with minimal changes in the population-scale firing rate. This stimulus effect normalizes/suppresses the pathological firing patterns and dysrhythmia that underlie specific phenotypes in both the PD and TS models. We propose that the elimination of pathological states via stimulus-driven entrainment and suppression, while maintaining thalamocortical network excitability within a normal physiological range, provides a common therapeutic mechanism through which HF-DBS permits information transfer for purposive motor behavior through the CBG while ameliorating conditions with widely different symptom profiles.

Complex and dynamic expression of cadherins in the embryonic marmoset cerebral cortex.

Cadherin is a cell adhesion molecule widely expressed in the nervous system. Previously, we analyzed the expression of nine classic cadherins (Cdh4, Cdh6, Cdh7, Cdh8, Cdh9, Cdh10, Cdh11, Cdh12, and Cdh20) and T-cadherin (Cdh13) in the developing postnatal common marmoset (Callithrix jacchus) brain, and found differential expressions between mice and marmosets. In this study, to explore primate-specific cadherin expression at the embryonic stage, we extensively analyzed the expression of these cadherins in the developing embryonic marmoset brain. Each cadherin showed differential spatial and temporal expression and exhibited temporally complicated expression. Furthermore, the expression of some cadherins differed from that in rodent brains, even at the embryonic stage. These results suggest the possibility that the differential expressions of diverse cadherins are involved in primate specific cortical development, from the prenatal to postnatal period.

Identification of tool use acquisition-associated genes in the primate neocortex.

Japanese macaques are able to learn how to use rakes to take food after only a few weeks of training. Since tool-use training induced rapid morphological changes in some restricted brain areas, this system will be a good model for studying the neural basis of plasticity in human brains. To examine the mechanisms of tool-use associated brain expansion on the molecular and cellular level, here, we performed comprehensive analysis of gene expressions with microarray. We identified various transcripts showing differential expression between trained and untrained monkeys in the region around the lateral and intraparietal sulci. Among candidates, we focused on genes related to synapse formation and function. Using quantitative reverse transcription-polymerase chain reaction and histochemical analysis, we confirmed at least three genes (ADAM19, SPON2, and WIF1) with statistically different expression levels in neurons and glial cells. Comparative analysis revealed that tool use-associated genes were more obviously expressed in macaque monkeys than marmosets or mice. Thus, our findings suggest that cognitive tasks induce structural changes in the neocortex via gene expression, and that learning-associated genes innately differ with relation to learning ability.

Periostin, a neurite outgrowth-promoting factor, is expressed at high levels in the primate cerebral cortex.

Periostin (POSTN or osteoblast specific factor) is an extracellular matrix protein originally identified as a protein highly expressed in osteoblasts. Recently, periostin has been reported to function in axon regeneration and neuroprotection. In the present study, we focused on periostin function in cortical evolution. We performed a comparative gene expression analysis of periostin between rodents (mice) and primates (marmosets and macaques). Periostin was expressed at higher levels in the primate cerebral cortex compared to the mouse cerebral cortex. Furthermore, we performed overexpression experiments of periostin in vivo and in vitro. Periostin exhibited neurite outgrowth activity in cortical neurons. These results suggested the possibility that prolonged and increased periostin expression in the primate cerebral cortex enhances the cortical plasticity of the mammalian cerebral cortex.

Global dysrhythmia of cerebro-basal ganglia-cerebellar networks underlies motor tics following striatal disinhibition.

Motor tics, a cardinal symptom of Tourette syndrome (TS), are hypothesized to arise from abnormalities within cerebro-basal ganglia circuits. Yet noninvasive neuroimaging of TS has previously identified robust activation in the cerebellum. To date, electrophysiological properties of cerebellar activation and its role in basal ganglia-mediated tic expression remain unknown. We performed multisite, multielectrode recordings of single-unit activity and local field potentials from the cerebellum, basal ganglia, and primary motor cortex using a pharmacologic monkey model of motor tics/TS. Following microinjections of bicuculline into the sensorimotor putamen, periodic tics occurred predominantly in the orofacial region, and a sizable number of cerebellar neurons showed phasic changes in activity associated with tic episodes. Specifically, 64% of the recorded cerebellar cortex neurons exhibited increases in activity, and 85% of the dentate nucleus neurons displayed excitatory, inhibitory, or multiphasic responses. Critically, abnormal discharges of cerebellar cortex neurons and excitatory-type dentate neurons mostly preceded behavioral tic onset, indicating their central origins. Latencies of pathological activity in the cerebellum and primary motor cortex substantially overlapped, suggesting that aberrant signals may be traveling along divergent pathways to these structures from the basal ganglia. Furthermore, the occurrence of tic movement was most closely associated with local field potential spikes in the cerebellum and primary motor cortex, implying that these structures may function as a gate to release overt tic movements. These findings indicate that tic-generating networks in basal ganglia mediated tic disorders extend beyond classical cerebro-basal ganglia circuits, leading to global network dysrhythmia including cerebellar circuits.

Deep brain stimulation reduces Tic-related neural activity via temporal locking with stimulus pulses.

A neurosurgical intervention that has shown potential for treating basal ganglia (BG) mediated motor tics involves high-frequency deep brain stimulation (HF-DBS) targeted to the output nucleus of the BG: the globus pallidus internus (GPi). This study used a nonhuman primate (Macaca fuscata) model of BG-meditated motor tics, and investigated the short-term neuronal mechanism that might underlie the beneficial effects of GPi-HF-DBS. In parallel with behavioral tic expressions, phasic alterations of neuronal activity emerged in the pallidum following focal disinhibition of the striatum with bicuculline. We delivered HF-DBS in the GPi in such a way that on-stimulation and off-stimulation conditions alternated every 30 s. Analysis of electromyographic (EMG) records showed that during on-stimulation, there were significant reductions in tic-related EMG amplitude. Analysis of pallidal activity showed that GPi-HF-DBS induced both sustained and transient patterns of excitation and inhibition in both segments of the GP. Population-scale firing rates were initially raised relative to baseline, but were not significantly different by the time stimulation ceased. Modulation of behavior and neuronal firing rates were associated with the reduction of tic-related phasic activity in pallidal cells. Examination of short-latency responses showed that firing rate changes were strongly associated with locking of the cells' activity with the HF-DBS pulse. This temporal locking often induced multiphasic changes of firing rates in individual cells, which dynamically changed across the stimulation period. These results support clinical studies that reported success in treating motor tics with GPi-HF-DBS, and demonstrate that the underlying local mechanism within the GP is suppression of tic-related activity through temporal locking with the stimulation pulse.

Complementary and dynamic type II cadherin expression associated with development of the primate visual system.

The middle temporal visual area (MT, also known as V5) is a visual association area that is particularly evolved in the primate brain. The MT receives input from the primary visual area (V1), constitutes part of the dorsal visual pathway, and plays an essential role in processing motion. Connections between the MT and V1 in the primate brain are formed after birth, and are related to the maturation of visual system. However, it remains to be determined what molecular mechanisms control the formation and maturation of the visual system. Cadherins are transmembrane proteins, originally isolated as cell adhesion molecules, which have multiple roles in synapse formation and function. To investigate potential involvement of cadherins in development of the primate visual system, we examined type II cadherin expression (cadherin-6, -8, -12) in cortical and thalamic visual areas of pre- and postnatal brains of the common marmoset (Callithrix jacchus). In the prenatal brain, cadherin-6 was dominantly expressed in the pulvino-MT pathway whereas cadherin-8 was dominant in the lateral geniculate nucleus (LGN)-V1 pathway. During postnatal development, there was a downregulation of cadherin-6 and upregulation of cadherin-8 expression in the MT. The timing of this cadherin exchange preceded the development of V1-MT connections. Our results suggest the possibility that changes in cadherin expression are involved in the development of the primate visual system, and that a switch in cadherin expression may be a general mechanism to control neural plasticity of highly cognitive abilities.

Dissociations between the horizontal and dorsoventral axes in body-size perception.

Body size can vary throughout a person's lifetime, inducing plasticity of the internal body representation. Changes in horizontal width accompany those in dorsal-to-ventral thickness. To examine differences in the perception of different body axes, neural correlates of own-body-size perception in the horizontal and dorsoventral directions were compared using functional magnetic resonance imaging. Original and distorted (-30, -10, +10 and +30%) images of the neck-down region of their own body were presented to healthy female participants, who were then asked whether the images were of their own body or not based explicitly on body size. Participants perceived body images distorted by -10% as their own, whereas those distorted by +30% as belonging to others. Horizontal width images yielded slightly more subjective own-body perceptions than dorsoventral thickness images did. Subjective perception of own-body size was associated with bilateral inferior parietal activity. In contrast, other-body judgments showed pre-supplementary motor and superior parietal activity. Expansion in the dorsoventral direction was associated with the left fusiform gyrus and the right inferior parietal lobule, whereas horizontal expansions were associated with activity in the bilateral somatosensory area. These results suggest neural dissociations between the two body axes: dorsoventral images of thickness may require visual processing, whereas bodily sensations are involved in horizontal body-size perception. Somatosensory rather than visual processes can be critical for the assessment of frontal own-body appearance. Visual body thickness and somatosensory body width may be integrated to construct a whole-body representation.

Three-dimensional reconstruction of brain structures of the rodent Octodon degus: a brain atlas constructed by combining histological and magnetic resonance images.

Degus (Octodon degus) are rodents that are becoming more widely used in the neuroscience field. Degus display several more complex behaviors than rats and mice, including complicated social behaviors, vocal communications, and tool usage with superb manual dexterity. However, relatively little information is known about the anatomy of degu brains. Therefore, for these complex behaviors to be correlated with specific brain regions, a contemporary atlas of the degu brain is required. This manuscript describes the construction of a three-dimensional (3D) volume rendered model of the degu brain that combines histological and magnetic resonance images. This atlas provides several advantages, including the ability to visualize the surface of the brain from any angle. The atlas also permits virtual cutting of brain sections in any plane and provides stereotaxic coordinates for all sections, to be beneficial for both experimental surgeries and radiological studies. The reconstructed 3D atlas is freely available online at: http://brainatlas.brain.riken.jp/degu/modules/xoonips/listitem.php?index_id=24 .

Neural response to movement of the hand and mouth in the secondary somatosensory cortex of Japanese monkeys during a simple feeding task.

Neural activity was recorded in the secondary somatosensory cortex (SII) of macaque monkeys during a simple feeding task. Around the border between the representations of the hand and face in SII, we found neurons that became active during both retrieving with the hand and eating; 59% had receptive fields (RFs) in the hand/face and the remaining 41% had no RFs. Neurons that responded to touching objects were rarely found. This suggests their sensorimotor function rather than tactile object recognition.

Modulation of cortical vestibular processing by somatosensory inputs in the posterior insula.

PRIMARY OBJECTIVE: To study the mechanism of somatosensory-vestibular interactions, this study examined the effects of somatosensory inputs on body sway induced by galvanic vestibular stimulation (GVS) in healthy participants and persons with brain injury in the posterior insula, a region constituting a part of the parietoinsular vestibular cortex. RESEARCH DESIGN: This study adopted an experimental, controlled, repeated measures design. METHODS AND PROCEDURES: Participants were 11 healthy individuals, two persons with unilateral posterior insular injury and two age-matched controls. Bipolar GVS was applied to the mastoid processes while participants were sitting with their eyes closed, either lightly touching a stable surface with their index finger or not touching the surface with their index finger. MAIN OUTCOMES AND RESULTS: In healthy participants, tilting was greater with right hemispheric stimulation than with left hemispheric stimulation. Moreover, with right hemispheric stimulation, tilting was greater with a right finger touch than with no touch. The person with right-brain injury showed tilting induced by GVS; however, finger touch had no modulatory effect. In contrast, finger touch enhanced tilting in the person with left-brain injury. CONCLUSIONS: These preliminary results are discussed in light of a hypothesis of right hemispheric dominance of somatosensory-vestibular interactions in the posterior insula.