Individual Differences in Scanpaths Correspond with Serotonin Transporter Genotype and Behavioral Phenotype in Rhesus Monkeys (Macaca mulatta)

Scanpaths (the succession of fixations and saccades during spontaneous viewing) contain information about the image but also about the viewer. To determine the viewer-dependent factors in the scanpaths of monkeys, we trained three adult males (Macaca mulatta) to look for 3 s at images of conspecific facial expressions with either direct or averted gaze. The subjects showed significant differences on four basic scanpath parameters (number of fixations, fixation duration, saccade length, and total scanpath length) when viewing the same facial expression/gaze direction combinations. Furthermore, we found differences between monkeys in feature preference and in the temporal order in which features were visited on different facial expressions. Overall, the between-subject variability was larger than the within- subject variability, suggesting that scanpaths reflect individual preferences in allocating visual attention to various features in aggressive, neutral, and appeasing facial expressions. Individual scanpath characteristics were brought into register with the genotype for the serotonin transporter regulatory gene (5-HTTLPR) and with behavioral characteristics such as expression of anticipatory anxiety and impulsiveness/hesitation in approaching food in the presence of a potentially dangerous object

A context-dependent switch from sensing to feeling in the primate amygdala

The skin transmits affective signals that integrate into our social vocabulary. As the socio-affective aspects of touch are likely processed in the amygdala, we compare neural responses to social grooming and gentle airflow recorded from the amygdala and the primary somatosensory cortex of non-human primates. Neurons in the somatosensory cortex respond to both types of tactile stimuli. In the amygdala, however, neurons do not respond to individual grooming sweeps even though grooming elicits autonomic states indicative of positive affect. Instead, many show changes in baseline firing rates that persist throughout the grooming bout. Such baseline fluctuations are attributed to social context because the presence of the groomer alone can account for the observed changes in baseline activity. It appears, therefore, that during grooming, the amygdala stops responding to external inputs on a short timescale but remains responsive to social context (or the associated affective states) on longer time scales

Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala

Neurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing

Infrared neural stimulation with 7T fMRI: A rapid in vivo method for mapping cortical connections of primate amygdala

We have previously shown that INS-fMRI is a rapid method for mapping mesoscale brain networks in the macaque monkey brain. Focal stimulation of single cortical sites led to the activation of connected cortical locations, resulting in a global connectivity map. Here, we have extended this method for mapping brainwide networks following stimulation of single subcortical sites. As a testbed, we focused on the basal nucleus of the amygdala in the macaque monkey. We describe methods to target basal nucleus locations with submillimeter precision, pulse train stimulation methods, and statistical tests for assessing non-random nature of activations. Using these methods, we report that stimulation of precisely targeted loci in the basal nucleus produced sparse and specific activations in the brain. Activations were observed in the insular and sensory association cortices as well as activations in the cingulate cortex, consistent with known anatomical connections. What is new here is that the activations were focal and, in some cases, exhibited shifting topography with millimeter shifts in stimulation site. The precision of the method enables networks mapped from different nearby sites in the basal nucleus to be distinguished. While further investigation is needed to improve the sensitivity of this method, our analyses do support the reproducibility and non-random nature of some of the activations. We suggest that INS-fMRI is a promising method for mapping large-scale cortical and subcortical networks at high spatial resolution. © 2021 The Author(s)Open access articleThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

A framework and resource for global collaboration in non-human primate neuroscience

As science and technology evolve, there is an increasing need for promotion of international scientific exchange. Collaborations, while offering substantial opportunities for scientists and benefit to society, also present challenges for those working with animal models, such as non-human primates (NHPs). Diversity in regulation of animal research is sometimes mistaken for the absence of common international welfare standards. Here, the ethical and regulatory protocols for 13 countries that have guidelines in place for biomedical research involving NHPs were assessed with a focus on neuroscience. Review of the variability and similarity in trans-national NHP welfare regulations extended to countries in Asia, Europe and North America. A tabulated resource was established to advance solution-oriented discussions and scientific collaborations across borders. Our aim is to better inform the public and other stakeholders. Through cooperative efforts to identify and analyze information with reference to evidence-based discussion, the proposed key ingredients may help to shape and support a more informed, open framework. This framework and resource can be expanded further for biomedical research in other countries

Multidimensional Neural Selectivity in the Primate Amygdala

The amygdala contributes to multiple functions including attention allocation, sensory processing, decision-making, and the elaboration of emotional behaviors. The diversity of functions attributed to the amygdala is reflected in the response selectivity of its component neurons. Previous work claimed that subsets of neurons differentiate between broad categories of stimuli (e.g., objects vs faces, rewards vs punishment), while other subsets are narrowly specialized to respond to individual faces or facial features (e.g., eyes). Here we explored the extent to which the same neurons contribute to more than one neural subpopulation in a task that activated multiple functions of the amygdala. The subjects (Macaca mulatta) watched videos depicting conspecifics or inanimate objects, and learned by trial and error to choose the individuals or objects associated with the highest rewards. We found that the same neurons responded selectively to two or more of the following task events or stimulus features: (1) alerting, task-related stimuli (fixation icon, video start, and video end); (2) reward magnitude; (3) stimulus categories (social vs nonsocial); and (4) stimulus-unique features (faces, eyes). A disproportionate number of neurons showed selectivity for all of the examined stimulus features and task events. These results suggest that neurons that appear specialized and uniquely tuned to specific stimuli (e.g., face cells, eye cells) are likely to respond to multiple other types of stimuli or behavioral events, if/when these become behaviorally relevant in the context of a complex task. This multidimensional selectivity supports a flexible, context-dependent evaluation of inputs and subsequent decision making based on the activity of the same neural ensemble.United States Department of Health & Human Services National Institutes of Health (NIH) - USA [P50-MH100023]Open access journalThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

Decision of Learning Status Based on Modeling of the Information Measurement of Social Behavioral Tasks in Rhesus Monkeys

We are interested in identifying the learning status of the social behavioral tasks in the rhesus monkey. In addition, we define the characteristic of stimulus with a numerical quantification. We allow monkeys to interact with individuals of different social status, while we monitor the viewer monkey's behavior by tracking its scan paths. With these observations, we can understand the learning status of this animal via looking behavior analysis on the stimulus. First, the viewer monkey shows different looking patterns among six different classes. Therefore, we can generate different data descriptors of these classes and observe the classification performance of the machine learning algorithm. Second, we design the ground truth model based on the characteristic of each stimulus. We define the distribution of information from the ratio of the face, body, and background area in the stimulus. Lastly, we link them to figure out whether the viewer monkey learned enough about the information in the stimulus.NIHImmediate accessThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]