Early life adversity in primates: Behavioral, endocrine, and neural effects.

BACKGROUND: Evidence suggests that early life adversity is associated with maladaptive behaviors and is commonly an antecedent of stress-related psychopathology. This is particularly relevant to rearing in primate species as infant primates depend on prolonged, nurturant rearing by caregivers for normal development. To further understand the consequences of early life rearing adversity, and the relation among alterations in behavior, physiology and brain function, we assessed young monkeys that had experienced maternal separation followed by peer rearing with behavioral, endocrine and multimodal neuroimaging measures. METHODS: 50 young rhesus monkeys were studied, half of which were rejected by their mothers and peer reared, and the other half were reared by their mothers. Assessments were performed at approximately 1.8 years of age and included: threat related behavioral and cortisol responses, cerebrospinal fluid (CSF) measurements of oxytocin and corticotropin releasing hormone (CRH), and multimodal neuroimaging measures (anatomical scans, resting functional connectivity, diffusion tensor imaging, and threat-related regional glucose metabolism). RESULTS: The results demonstrated alterations across behavioral, endocrine, and neuroimaging measures in young monkeys that were reared without their mothers. At a behavioral level in response to a potential threat, peer reared animals engaged in significantly less freezing behavior (p = 0.022) along with increased self-directed behaviors (p < 0.012). Levels of oxytocin in the CSF, but not plasma, were significantly reduced in the peer reared animals (p = 0.019). No differences in plasma cortisol or CSF CRH were observed. Diffusion tensor imaging revealed significantly decreased white matter density across the brain. Exploratory correlational and permutation analyses suggest that the impact of peer rearing on behavior, endocrine and brain structural alterations are mediated by separate parallel mechanisms. CONCLUSIONS: Taken together, these results demonstrate in NHPs the importance of maternal rearing on the development of brain, behavior and hormonal systems that are linked to social functioning and adaptive responses. The findings suggest that the effects of maternal deprivation are mediated via multiple independent pathways which may account for the heterogeneity in behavioral and biological alterations observed in individuals that have experienced this early life adversity.

Configuration of the action observation network depends on the goals of the observer.

Observing the actions of others engages a core action observation network (AON) that includes the bilateral inferior frontal cortex (IFC), posterior superior temporal sulcus (pSTS) and inferior parietal lobule (IPL) (Caspers et al., 2010). Each region in the AON has functional properties that are heterogeneous and include representing the perceptual properties of action, predicting action outcomes and making inferences as to the goals of the actor. Critically, recent evidence shows that neural representations within the pSTS are sharpened when attending to the kinematics of the actor, such that the top-down guided attention reshapes underlying neural representations. In this study we evaluate how attention alters network connectivity within the AON as a system. Cues directed participant's attention to the goal, kinematics, or identity depicted in short action animations while brain responses were measured by fMRI. We identified those parcels within the AON with functional connectivity modulated by task. Results show that connectivity between the right pSTS and right IFC, and bilateral extended STS (STS+) were modulated during action observation such that connections were strengthened when the participant was attending to the action than goal. This finding is contrasted by the univariate results, which no univariate modulations in these brain regions except for right IFC. Using the functional networks defined by Yeo et al. (2011), we identified the parcels that are modulated by the attention to consist mainly of the fronto-parietal control network and default mode networks. These results are consistent with models of top-down feedback from executive system in the IFC to pSTS and implicates a right lateralized dual pathway model for action observation when focused on whole-body kinematics.

Category-specific activations depend on imaging mode, task demand, and stimuli modality: An ALE meta-analysis.

The cortical organization of the semantic network has been examined extensively in neuropsychological and neuroimaging studies; however, after decades of research, several issues remain controversial. A comprehensive and systematic investigation is needed to characterize the consistent patterns of category-specific activations as well as to examine factors that contribute to the varying findings across numerous neuroimaging studies. In this study, we reviewed 113 published papers that reported category-specific activations for living or nonliving concepts from the past two decades. Using the Activation Likelihood Estimate (ALE) method, we characterized the brain regions associated with living and nonliving concepts and revealed how the observed patterns were heavily influenced by methodological factors including imaging mode, task demand, and stimuli modality. Our findings provided the most comprehensive summary of category-specific activations for living and nonliving concepts and critically revealed that these activation patterns are highly contextually dependent. This work advanced our knowledge about the organization of the cortical semantic network and provided important insights into theoretical accounts and future research directions.

Top-Down Attention Guidance Shapes Action Encoding in the pSTS.

The posterior superior temporal sulcus (pSTS) is a brain region characterized by perceptual representations of human body actions that promote the understanding of observed behavior. Increasingly, action observation is recognized as being strongly shaped by the expectations of the observer (Kilner 2011; Koster-Hale and Saxe 2013; Patel et al. 2019). Therefore, to characterize top-down influences on action observation, we evaluated the statistical structure of multivariate activation patterns from the action observation network (AON) while observers attended to the different dimensions of action vignettes (the action kinematics, goal, or identity of avatars jumping or crouching). Decoding accuracy varied as a function of attention instruction in the right pSTS and left inferior frontal cortex (IFC), with the right pSTS classifying actions most accurately when observers attended to the action kinematics and the left IFC classifying most accurately when observed attended to the actor's goal. Functional connectivity also increased between the right pSTS and right IFC when observers attended to the actions portrayed in the vignettes. Our findings are evidence that the attentive state of the viewer modulates sensory representations in the pSTS, consistent with proposals that the pSTS occupies an interstitial zone mediating top-down context and bottom-up perceptual cues during action observation.