A comprehensive macaque fMRI pipeline and hierarchical atlas.

Functional neuroimaging research in the non-human primate (NHP) has been advancing at a remarkable rate. The increase in available data establishes a need for robust analysis pipelines designed for NHP neuroimaging and accompanying template spaces to standardize the localization of neuroimaging results. Our group recently developed the NIMH Macaque Template (NMT), a high-resolution population average anatomical template and associated neuroimaging resources, providing researchers with a standard space for macaque neuroimaging . Here, we release NMT v2, which includes both symmetric and asymmetric templates in stereotaxic orientation, with improvements in spatial contrast, processing efficiency, and segmentation. We also introduce the Cortical Hierarchy Atlas of the Rhesus Macaque (CHARM), a hierarchical parcellation of the macaque cerebral cortex with varying degrees of detail. These tools have been integrated into the neuroimaging analysis software AFNI to provide a comprehensive and robust pipeline for fMRI processing, visualization and analysis of NHP data. AFNI's new @animal_warper program can be used to efficiently align anatomical scans to the NMT v2 space, and afni_proc.py integrates these results with full fMRI processing using macaque-specific parameters: from motion correction through regression modeling. Taken together, the NMT v2 and AFNI represent an all-in-one package for macaque functional neuroimaging analysis, as demonstrated with available demos for both task and resting state fMRI.

The Subcortical Atlas of the Rhesus Macaque (SARM) for neuroimaging.

Digitized neuroanatomical atlases that can be overlaid onto functional data are crucial for localizing brain structures and analyzing functional networks identified by neuroimaging techniques. To aid in functional and structural data analysis, we have created a comprehensive parcellation of the rhesus macaque subcortex using a high-resolution ex vivo structural imaging scan. This anatomical scan and its parcellation were warped to the updated NIMH Macaque Template (NMT v2), an in vivo population template, where the parcellation was refined to produce the Subcortical Atlas of the Rhesus Macaque (SARM) with 210 primary regions-of-interest (ROIs). The subcortical parcellation and nomenclature reflect those of the 4th edition of the Rhesus Monkey Brain in Stereotaxic Coordinates (Paxinos et al., in preparation), rather than proposing yet another novel atlas. The primary ROIs are organized across six spatial hierarchical scales from small, fine-grained ROIs to broader composites of multiple ROIs, making the SARM suitable for analysis at different resolutions and allowing broader labeling of functional signals when more accurate localization is not possible. As an example application of this atlas, we have included a functional localizer for the dorsal lateral geniculate (DLG) nucleus in three macaques using a visual flickering checkerboard stimulus, identifying and quantifying significant fMRI activation in this atlas region. The SARM has been made openly available to the neuroimaging community and can easily be used with common MRI data processing software, such as AFNI, where the atlas has been embedded into the software alongside cortical macaque atlases.

CIVET-Macaque: An automated pipeline for MRI-based cortical surface generation and cortical thickness in macaques.

The MNI CIVET pipeline for automated extraction of cortical surfaces and evaluation of cortical thickness from in-vivo human MRI has been extended for processing macaque brains. Processing is performed based on the NIMH Macaque Template (NMT), as the reference template, with the anatomical parcellation of the surface following the D99 and CHARM atlases. The modifications needed to adapt CIVET to the macaque brain are detailed. Results have been obtained using CIVET-macaque to process the anatomical scans of the 31 macaques used to generate the NMT and another 95 macaques from the PRIME-DE initiative. It is anticipated that the open usage of CIVET-macaque will promote collaborative efforts in data collection and processing, sharing, and automated analyses from which the non-human primate brain imaging field will advance.

U-net model for brain extraction: Trained on humans for transfer to non-human primates.

Brain extraction (a.k.a. skull stripping) is a fundamental step in the neuroimaging pipeline as it can affect the accuracy of downstream preprocess such as image registration, tissue classification, etc. Most brain extraction tools have been designed for and applied to human data and are often challenged by non-human primates (NHP) data. Amongst recent attempts to improve performance on NHP data, deep learning models appear to outperform the traditional tools. However, given the minimal sample size of most NHP studies and notable variations in data quality, the deep learning models are very rarely applied to multi-site samples in NHP imaging. To overcome this challenge, we used a transfer-learning framework that leverages a large human imaging dataset to pretrain a convolutional neural network (i.e. U-Net Model), and then transferred this to NHP data using a small NHP training sample. The resulting transfer-learning model converged faster and achieved more accurate performance than a similar U-Net Model trained exclusively on NHP samples. We improved the generalizability of the model by upgrading the transfer-learned model using additional training datasets from multiple research sites in the Primate Data-Exchange (PRIME-DE) consortium. Our final model outperformed brain extraction routines from popular MRI packages (AFNI, FSL, and FreeSurfer) across a heterogeneous sample from multiple sites in the PRIME-DE with less computational cost (20 s~10 min). We also demonstrated the transfer-learning process enables the macaque model to be updated for use with scans from chimpanzees, marmosets, and other mammals (e.g. pig). Our model, code, and the skull-stripped mask repository of 136 macaque monkeys are publicly available for unrestricted use by the neuroimaging community at https://github.com/HumanBrainED/NHP-BrainExtraction.

Combining brain perturbation and neuroimaging in non-human primates.

Brain perturbation studies allow detailed causal inferences of behavioral and neural processes. Because the combination of brain perturbation methods and neural measurement techniques is inherently challenging, research in humans has predominantly focused on non-invasive, indirect brain perturbations, or neurological lesion studies. Non-human primates have been indispensable as a neurobiological system that is highly similar to humans while simultaneously being more experimentally tractable, allowing visualization of the functional and structural impact of systematic brain perturbation. This review considers the state of the art in non-human primate brain perturbation with a focus on approaches that can be combined with neuroimaging. We consider both non-reversible (lesions) and reversible or temporary perturbations such as electrical, pharmacological, optical, optogenetic, chemogenetic, pathway-selective, and ultrasound based interference methods. Method-specific considerations from the research and development community are offered to facilitate research in this field and support further innovations. We conclude by identifying novel avenues for further research and innovation and by highlighting the clinical translational potential of the methods.

A collaborative resource platform for non-human primate neuroimaging.

Neuroimaging non-human primates (NHPs) is a growing, yet highly specialized field of neuroscience. Resources that were primarily developed for human neuroimaging often need to be significantly adapted for use with NHPs or other animals, which has led to an abundance of custom, in-house solutions. In recent years, the global NHP neuroimaging community has made significant efforts to transform the field towards more open and collaborative practices. Here we present the PRIMatE Resource Exchange (PRIME-RE), a new collaborative online platform for NHP neuroimaging. PRIME-RE is a dynamic community-driven hub for the exchange of practical knowledge, specialized analytical tools, and open data repositories, specifically related to NHP neuroimaging. PRIME-RE caters to both researchers and developers who are either new to the field, looking to stay abreast of the latest developments, or seeking to collaboratively advance the field .

A population MRI brain template and analysis tools for the macaque.

The use of standard anatomical templates is common in human neuroimaging, as it facilitates data analysis and comparison across subjects and studies. For non-human primates, previous in vivo templates have lacked sufficient contrast to reliably validate known anatomical brain regions and have not provided tools for automated single-subject processing. Here we present the "National Institute of Mental Health Macaque Template", or NMT for short. The NMT is a high-resolution in vivo MRI template of the average macaque brain generated from 31 subjects, as well as a neuroimaging tool for improved data analysis and visualization. From the NMT volume, we generated maps of tissue segmentation and cortical thickness. Surface reconstructions and transformations to previously published digital brain atlases are also provided. We further provide an analysis pipeline using the NMT that automates and standardizes the time-consuming processes of brain extraction, tissue segmentation, and morphometric feature estimation for anatomical scans of individual subjects. The NMT and associated tools thus provide a common platform for precise single-subject data analysis and for characterizations of neuroimaging results across subjects and studies.

Adolescent relationship violence: help-seeking and help-giving behaviors among peers.

Young people tend to disclose relationship violence experiences to their peers, if they disclose at all, yet little is known about the nature and frequency of adolescent help-seeking and help-giving behaviors. Conducted within a sample of 1,312 young people from four New York City high schools, this is the first paper to ask adolescent help-givers about the various forms of help they provide and among the first to examine how ethnicity and nativity impact help-seeking behaviors. Relationship violence victims who had ever disclosed (61%) were more likely to choose their friends for informal support. Ethnicity was predictive of adolescent disclosure outlets, whereas gender and nativity were not. Latinos were significantly less likely than non-Latinos to ever disclose to only friends, as compared to disclosing to at least one adult. The likelihood of a young person giving help to their friend in a violent relationship is associated with gender, ethnicity, and nativity, with males being significantly less likely than females to give all forms of help to their friends (talking to their friends about the violence, suggesting options, and taking action). Foreign-born adolescents are less likely to talk or suggest options to friends in violent relationships. This study also found that Latinos were significantly more likely than non-Latinos to report taking action with or on behalf of a friend in a violent relationship. This research shows that adolescents often rely on each other to address relationship violence, underlining the importance of adolescents' receipt of training and education on how to support their friends, including when to seek help from more formal services. To further understand the valuable role played by adolescent peers of victims, future research should explore both which forms of help are perceived by the victim to be most helpful and which are associated with more positive outcomes.

Short-latency preference for faces in primate superior colliculus depends on visual cortex.

Face processing is fundamental to primates and has been extensively studied in higher-order visual cortex. Here, we report that visual neurons in the midbrain superior colliculus (SC) of macaque monkeys display a preference for images of faces. This preference emerges within 40 ms of stimulus onset-well before "face patches" in visual cortex-and, at the population level, can be used to distinguish faces from other visual objects with accuracies of ∼80%. This short-latency face preference in SC depends on signals routed through early visual cortex because inactivating the lateral geniculate nucleus, the key relay from retina to cortex, virtually eliminates visual responses in SC, including face-related activity. These results reveal an unexpected circuit in the primate visual system for rapidly detecting faces in the periphery, complementing the higher-order areas needed for recognizing individual faces.

Short-latency preference for faces in the primate superior colliculus.

Face processing is fundamental to primates and has been extensively studied in higher-order visual cortex. Here we report that visual neurons in the midbrain superior colliculus (SC) display a preference for faces, that the preference emerges within 50ms of stimulus onset - well before "face patches" in visual cortex - and that this activity can distinguish faces from other visual objects with accuracies of ~80%. This short-latency preference in SC depends on signals routed through early visual cortex, because inactivating the lateral geniculate nucleus, the key relay from retina to cortex, virtually eliminates visual responses in SC, including face-related activity. These results reveal an unexpected circuit in the primate visual system for rapidly detecting faces in the periphery, complementing the higher-order areas needed for recognizing individual faces.

Intimate Partner Violence Help-Seeking in the U.S. Transgender Survey.

Research finds that transgender survivors of intimate partner violence (IPV) often face transphobia-related barriers to reaching help. Due partially to a dearth of larger datasets supporting multivariate analyses, it is unclear whether sociodemographic factors can further hinder transgender help-seeking. Addressing these gaps, logistic regression secondary data analyses were conducted with 15,198 transgender IPV survivors from the nationally-representative 2015 U.S. Transgender Survey. Odds of seeking help from survivor agencies were significantly greater for survivors who are trans men, assigned-female-at-birth genderqueer, Alaska Native or American Indian, poorer, transphobia victims, and victims of any IPV type, especially controlling IPV. In addition, odds of not seeking help due fearing transphobic responses were significantly greater for survivors who are trans women, asexual or bisexual, poorer, younger, undocumented, childless, ever homeless, transphobia victims, or victims of any IPV type, particularly sexual IPV. Implications for future research and population-specific service provision are discussed.

Transgender Polyvictimization in the U.S. Transgender Survey.

Relative to cisgender people, transgender individuals not only are at an elevated risk of experiencing at least one form of physical or sexual violence, but also at an increased risk of polyvictimization: that is, exposure to multiple types of violence over the life course. Given that polyvictimization increases vulnerability to adverse mental and physical health sequelae, there is a pressing need to identify which sociodemographic subgroups of transgender people are at greater risk of polyvictimization. Understanding these risk profiles will have important implications for developing transgender-specific models for violence prevention, screening, and intervention. Responding to this need in the literature, the present article offers secondary data analyses of the 2015 U.S. Transgender Survey, the largest study to-date of transgender people in the United States (N = 27,715 transgender adults), with participants selected from all 50 states and Washington, D.C., as well as several U.S. territories and overseas military bases. Multiple variable regressions examine sociodemographic predictors of five distinct forms of violence, as well as how many of these five violence types were experienced. The examined sociodemographic predictors included gender, sexual orientation, race-ethnicity, citizenship status, ever been homeless, has a disability, transgender outness, gender visual conformity, household income, and age. The five assessed violence victimization types included intimate partner violence, nonpartner sexual assault, antitransgender family violence, antitransgender physical violence during Kindergarten through 12th grade, and past-year antitransgender physical violence. With some exceptions, results indicate that more marginalized segments of transgender communities have a greater likelihood of experiencing polyvictimization. Recommendations are discussed for future research and service provision.

The cortical and subcortical correlates of face pareidolia in the macaque brain.

Face detection is a foundational social skill for primates. This vital function is thought to be supported by specialized neural mechanisms; however, although several face-selective regions have been identified in both humans and nonhuman primates, there is no consensus about which region(s) are involved in face detection. Here, we used naturally occurring errors of face detection (i.e. objects with illusory facial features referred to as examples of 'face pareidolia') to identify regions of the macaque brain implicated in face detection. Using whole-brain functional magnetic resonance imaging to test awake rhesus macaques, we discovered that a subset of face-selective patches in the inferior temporal cortex, on the lower lateral edge of the superior temporal sulcus, and the amygdala respond more to objects with illusory facial features than matched non-face objects. Multivariate analyses of the data revealed differences in the representation of illusory faces across the functionally defined regions of interest. These differences suggest that the cortical and subcortical face-selective regions contribute uniquely to the detection of facial features. We conclude that face detection is supported by a multiplexed system in the primate brain.

Transgender Intimate Partner Violence and Help-Seeking Patterns.

Intimate partner violence (IPV) against transgender individuals is highly prevalent and impactful, and thus research is needed to examine the extent to which survivors are able to reach needed assistance and safety. To our knowledge, no U.S.-based quantitative studies have explored transgender utilization patterns and perceptions regarding a broad range of help-giving resources (HGRs). The present article fills this gap in the literature by exploring help-seeking attitudes and behaviors of a convenience sample of 92 transgender adults and 325 cisgender sexual minority adults in the United States. Results from an online questionnaire indicate that, among the subsample experiencing IPV (n = 187), help-seeking rates were significantly higher among transgender survivors (84.1%) than cisgender sexual minority survivors (67.1%). In addition, transgender survivors most commonly sought help from friends (76.7%), followed by mental health care providers (39.5%) and family (30.2%), whereas formal HGRs such as police, IPV telephone hotlines, and survivor shelters had low utilization rates. Among all transgender participants, IPV survivors were significantly less likely than nonsurvivors to perceive family, medical doctors, and survivor hotlines as helpful HGRs for other survivors in general. Finally, transgender survivors were significantly less likely than nonsurvivors to self-report a willingness to disclose any future IPV to family. Although replication with larger, probability samples is needed, these findings suggest that friends often represent the primary line of defense for transgender survivors seeking help, and thus bystander intervention trainings and education should be adapted to address not just cisgender but also transgender IPV. Furthermore, because most formal HGR types appear to be underutilized and perceived more negatively by transgender survivors, renewed efforts are needed to tailor services, service advertising, and provider trainings to the needs of transgender communities. Directions for future research are reviewed.

Separable neuronal contributions to covertly attended locations and movement goals in macaque frontal cortex.

We investigated the spatial representation of covert attention and movement planning in monkeys performing a task that used symbolic cues to decouple the locus of covert attention from the motor target. In the three frontal areas studied, most spatially tuned neurons reflected either where attention was allocated or the planned saccade. Neurons modulated by both covert attention and the motor plan were in the minority. Such dual-purpose neurons were especially rare in premotor and prefrontal cortex but were more common just rostral to the arcuate sulcus. The existence of neurons that indicate where the monkey was attending but not its movement goal runs counter to the idea that the control of spatial attention is entirely reliant on the neuronal circuits underlying motor planning. Rather, the presence of separate neuronal populations for each cognitive process suggests that endogenous attention is under flexible control and can be dissociated from motor intention.

Perceptions of Same-Gender and Different-Gender Intimate Partner Cyber-Monitoring.

There is a paucity of research comparing perceptions of technology-facilitated partner monitoring or stalking between same-gender and different-gender relationships. As such, a randomized vignette study was conducted with 738 undergraduate students at a large Midwestern university, who read one of four stories of intimate partner cyber-monitoring (IPCM): same-gender IPCM with physical violence, same-gender IPCM without physical violence, different-gender IPCM with physical violence, and different-gender IPCM without physical violence. Results show that participants were significantly less likely to recommend the survivor break up with the abuser if the story described a same-gender relationship. If the story involved IPCM alone rather than also physical violence, participants were significantly less likely to label the abuse as "domestic violence," more likely to recommend doing nothing, and less likely to recommend most of the assessed protective actions-including being less likely to recommend asking the survivor to break up with the abuser, seeking help from friends and family, calling a domestic violence hotline, or calling the police. Results also indicate that IPCM is largely perceived to be less serious and less deserving of survivor support than physical intimate partner violence (IPV), for both same-gender and different-gender relationships. Implications for prevention education programming as well as research are discussed.

Bidirectional IPV Among Adolescent Sexual Minorities.

Research repeatedly concludes that lesbian, gay, and bisexual individuals (i.e., sexual minorities) are at increased risk of experiencing abuse in a romantic or sexual relationship. For service providers, a vital but largely unanswered question is how common it is for victims of sexual minority intimate partner violence (SM-IPV) to also have perpetrated IPV, particularly in regard to adolescent relationships. To our knowledge, the present article is only the second in the literature to examine adolescent SM-IPV directionality, and it is the first to compare adolescent SM-IPV directionality and heterosexual IPV (H-IPV) directionality within the same sample. In 25 high schools across three northern New England states, sexual minority (n = 398) and heterosexual (n = 2,687) high school-aged adolescents aged 13 years to 19 years (where sexual orientation is defined indirectly via sexual attraction) completed a questionnaire as part of a broader evaluation study of a bystander-focused violence prevention curriculum (we utilized baseline data in this article). Chi-square tests revealed that experiencing victimization was significantly associated with engaging in perpetration for all forms of IPV assessed for both sexual minority and heterosexual youths. The sole exception was threatening IPV, for which a significant association was found among heterosexual but not sexual minority individuals. Bidirectional IPV rates did not differ substantially by sexual attraction: Verbal abuse was most likely to be bidirectional for both sexual attraction groups and all other assessed IPV forms occurring overwhelmingly in unidirectional patterns. Although replication is needed, study results suggest that adolescent IPV is not generally bidirectional. Directions for future research are discussed, including the need for sampling plans that enable further disaggregation by age and sexual orientations.

Sexual and Gender Minority Intimate Partner Violence and Childhood Violence Exposure.

Limited research on female-assigned-at-birth sexual and gender minorities (FAB SGM) suggests that their risk of psychological, physical, and sexual intimate partner violence (IPV) victimization and perpetration may be linked to childhood violence exposure (CVE), such as experiencing child abuse, or witnessing sibling or interparental abuse. That said, there is a dearth of research in this population examining whether there is typically a violence type match between CVE and IPV (e.g., physical CVE predicting physical IPV), a gender match between those involved in CVE and later IPV (e.g., witnessing the abuse of female parents predicting IPV among women), or an increase in IPV risk commensurate with the number of different CVE types experienced. Addressing these gaps, this article draws on the baseline survey data of FAB400, a merged cohort accelerated longitudinal study of 488 FAB SGM adolescents and young adults. Analyses focused on the subsample of 457 participants with prior intimate relationship experience. Findings revealed that each assessed form of CVE-parental verbal abuse victimization, parental physical maltreatment victimization, childhood sexual abuse victimization, witnessing sibling abuse, and witnessing interparental violence-predicted risk of IPV perpetration and victimization, without evidence of violence type match. Witnessing interparental violence was associated with IPV irrespective of the abused parent's gender. In addition, exposure to a greater number of forms of CVE was associated with an increased risk of all types of IPV victimization and perpetration. Results offer preliminary evidence that the intergenerational transmission of violence is an applicable framework for FAB SGM, and as such this should be considered when screening and intervening for childhood, family, and partner violence in this population. Suggestions for future directions are discussed.

Development and Initial Validation of Three Culturally Sensitive Measures of Intimate Partner Violence for Sexual and Gender Minority Populations.

Measures of intimate partner violence (IPV) have largely been developed and validated in heterosexual, cisgender samples, with little attention to whether these measures are culturally appropriate for sexual and gender minority (SGM) populations. However, rates of IPV are two to three times higher among SGM than heterosexual populations, highlighting the importance of culturally appropriate measures of IPV for SGM populations. In this article, after reviewing key problems with the use of existing IPV measures with SGM samples, we describe the development of a toolkit of new and adapted measures of IPV for use with SGM assigned female at birth (SGM-AFAB) populations, including an adapted version of the Conflict Tactics Scale-Revised, an adapted measure of coercive control, and the newly developed SGM-Specific IPV Tactics Measure. Using data from a sample of 352 SGM-AFAB individuals, we then test the psychometric properties of these three measures, including their factor structures, internal reliability, and convergent/divergent validity. Results provide initial evidence of the reliability and validity of each measure. Together, these three measures comprise a culturally appropriate and psychometrically validated measurement toolkit for studying a broad range of IPV tactics among SGM-AFAB that will help build a foundation for more in-depth research into IPV in SGM populations.

Multitasking of attention and memory functions in the primate prefrontal cortex.

In motor and sensory areas of cortex, neuronal activity often depends on the location of a movement target or a sensory stimulus, with each neuron tuned to a single part of space called a preferred direction (when motor) or a receptive field (when sensory). As we previously reported, some neurons in the monkey prefrontal cortex are tuned to two parts of space, which we interpreted as reflecting attention and working memory, respectively. Monkeys performed a behavioral task in which they attended to a visual stimulus at one location while remembering a second place, and these locations were varied from trial to trial to assess spatial tuning. Most spatially tuned neurons specialized in either attentional or mnemonic processing, but about one-third of the cells showed tuning for both. Here, we show that the latter population, called multitasking neurons, improves the encoding of both the attended and remembered locations. These neurons do so for three reasons: (1) the preferred directions for attention and for working memory usually differ (and often diametrically oppose one another), (2) they have stronger tuning than specialized cells, and (3) pairs of multitasking neurons represent these cognitive parameters more efficiently than pairs that include even a single specialized cell. These findings suggest that multitasking neurons provide a computational advantage for behaviors that place simultaneous demands on two or more cognitive processes.