My Publications

  1. Charbonneau JA, Davis B, Raven EP, Patwardhan B, Grebosky C, Halteh L, Bennett JL, Bliss-Moreau E (2024). Evaluation of registration-based vs. manual segmentation of rhesus macaque brain MRIs. Brain Structure and Function.

  2. Charbonneau JA, Raven EP, Katsumi Y, Santistevan AC, Taylor C, Bliss-Moreau E (2024). Intrinsic functional and structural network organization in the macaque insula. Imaging Neuroscience.

  3. Charbonneau JA, Santistevan AC, Raven EP, Bennett JL, Russ BE, Bliss-Moreau E (2024). Evolutionarily conserved neural responses to affective touch in monkeys transcend consciousness and change with age. Proceedings of the National Academy of Sciences.

  4. Santistevan AC, Fiske O, Moadab G, Charbonneau JA, Isaacowitz DM, Bliss-Moreau E (2024). See no evil: Attentional bias towards threat is diminished in aged monkeys. Emotion.

  5. Charbonneau JA, Bennett JL, Chau K, Bliss-Moreau E (2022). Reorganization in the macaque interoceptive-allostatic network following anterior cingulate cortex damage. Cerebral Cortex.

  6. Charbonneau JA, Maister L, Tsakiris M, Bliss-Moreau E (2022). Rhesus monkeys have an interoceptive sense of their beating hearts. Proceedings of the National Academy of Sciences.

  7. Charbonneau JA, Amaral DG, Bliss-Moreau E (2022). Social housing status impacts rhesus monkeys’ affective responses in classic threat processing tasks. Scientific Reports.

  8. Charbonneau JA, Bennett JL, Bliss-Moreau E (2022). Amygdala or hippocampus damage only minimally impacts affective responding to threat. Behavioral Neuroscience.

  9. Paraouty N, Charbonneau JA, Sanes DH (2020). Social learning exploits the available auditory or visual cues. Scientific Reports.

Abstracts are provided chronologically below.

Evaluation of registration-based vs. manual segmentation of rhesus macaque brain MRIs

Charbonneau JA, Davis B, Raven EP, Patwardhan B, Grebosky C, Halteh L, Bennett JL, Bliss-Moreau E (in press)

Brain Structure and Function

With increasing numbers of magnetic resonance imaging (MRI) datasets becoming publicly available, researchers and clinicians alike have turned to automated methods of segmentation to enable population-level analyses of these data. Although prior research has evaluated the extent to which automated methods recapitulate “gold standard” manual segmentation methods in the human brain, such an evaluation has not yet been carried out for segmentation of MRIs of the macaque brain. Macaques offer the important opportunity to bridge gaps between microanatomical studies using invasive methods like tract tracing, neural recordings, and high-resolution histology and non-invasive macroanatomical studies using methods like MRI. As such, it is important to evaluate whether automated tools derive data of sufficient quality from macaque MRIs to bridge these gaps. We tested the relationship between automated registration-based segmentation using an open source and actively maintained NHP imaging analysis pipeline (AFNI) and gold standard manual segmentation of 4 structures (2 cortical: anterior cingulate cortex and insula; 2 subcortical: amygdala and caudate) across 37 rhesus macaques (Macaca mulatta). We identified some variability in the strength of correlation between automated and manual segmentations across neural regions and differences in relationships with demographic variables like age and sex between the two techniques.

Intrinsic functional and structural network organization in the macaque insula

Charbonneau JA, Raven EP, Katsumi Y, Santistevan AC, Taylor C, Bliss-Moreau E (in press)

Imaging Neuroscience

In recent decades in vivo magnetic resonance imaging (MRI) studies have provided previously inaccessible insights into the structure and function of healthy and pathological human brains in the laboratory and the clinic. However, the correlational nature of this work and relatively low resolution means that ground truth neuroanatomical studies and causal manipulations of neural circuitry must still occur in animal models offering greater tractability and higher resolution, rendering a scale and species gap in translation. Here, we bridge this gap with a detailed, multimodal investigation of the macaque insula in vivo. Using both functional and diffusion MRI—tools available for use in humans—we demonstrate a neural architecture in the macaque insula with clear correspondence to prior in vivo MRI findings in humans and post mortem cytoarchitectural and tract tracing studies in monkeys. Results converged across analysis methods and imaging modalities, supporting the translational potential of the macaque model.

Evolutionarily conserved neural responses to affective touch in monkeys transcend consciousness and change with age

Charbonneau JA, Santistevan AC, Raven EP, Bennett JL, Russ BE, Bliss-Moreau E (2024)

Proceedings of the National Academy of Sciences

Affective touch—a slow, gentle, and pleasant form of touch—activates a different neural network than which is activated during discriminative touch in humans. Affective touch perception is enabled by specialized low threshold mechanoreceptors in the skin with unmyelinated fibers called C tactile (CT) afferents. These CT afferents are conserved across mammalian species, including macaque monkeys. However, it is unknown whether neural representation of affective touch is the same across species and whether affective touch’s capacity to activate the hubs of the brain that compute socioaffective information requires conscious perception. Here, we used functional magnetic resonance imaging (fMRI) to assess the preferential activation of neural hubs by slow (affective) vs. fast (discriminative) touch in anesthetized rhesus monkeys (Macaca mulatta). Insula, anterior cingulate cortex (ACC), amygdala, and secondary somatosensory cortex were all significantly more active during slow touch relative to fast touch, suggesting homologous activation of the interoceptive-allostatic network across primate species during affective touch. Further, we found that neural responses to affective vs. discriminative touch in insula and ACC (the primary cortical hubs for interoceptive processing) changed significantly with age. Insula and ACC in younger animals differentiated between slow and fast touch, while activity was comparable between conditions for aged monkeys (equivalent to >70 years in humans). These results, together with prior studies establishing conserved peripheral nervous system mechanisms of affective touch transduction, suggest that neural responses to affective touch are evolutionarily conserved in monkeys, significantly impacted in old age, and do not necessitate conscious experience of touch.

See no evil: Attentional bias towards threat is diminished in aged monkeys

Santistevan AC, Fiske O, Moadab G, Charbonneau JA, Isaacowitz D, Bliss-Moreau E (2024)

Emotion

Prior evidence demonstrates that relative to younger adults, older human adults exhibit attentional biases towards positive and/or away from negative socioaffective stimuli (i.e., the age-related positivity effect). Whether or not the effect is phylogenetically conserved is currently unknown and its biopsychosocial origins are debated. To address this gap, we evaluated how visual processing of socioaffective stimuli differs in aged, compared to middle-aged, rhesus monkeys (Macaca mulatta) using eye-tracking in two experimental designs that are directly comparable to those historically used for evaluating attentional biases in humans. Results of our study demonstrate that while younger rhesus possess robust attentional biases towards threatening pictures of conspecifics’ faces, aged animals evidence no such bias. Critically, these biases emerged only when threatening faces were paired with neutral and not ostensibly ‘positive’ faces, suggesting social context modifies the effect. Results of our study suggest evolutionarily shared mechanisms drive age-related decline in visual biases towards negative stimuli in aging across primate species.

Reorganization in the macaque interoceptive-allostatic network following anterior cingulate cortex damage

Charbonneau JA, Bennett JL, Chau K, Bliss-Moreau E (2022)

Cerebral Cortex

Accumulating evidence indicates that the adult brain is capable of significant structural change following damage—a capacity once thought to be largely limited to developing brains. To date, most existing research on adult plasticity has focused on how exteroceptive sensorimotor networks compensate for damage to preserve function. Interoceptive networks—those that represent and process sensory information about the body’s internal state—are now recognized to be critical for a wide range of physiological and psychological functions from basic energy regulation to maintaining a sense of self, but the extent to which these networks remain plastic in adulthood has not been established. In this report we used detailed histological analyses to pinpoint precise changes to gray matter volume in the interoceptive-allostatic network in adult rhesus monkeys (Macaca mulatta) who received neurotoxic lesions of the anterior cingulate cortex and neurologically intact control monkeys. Relative to controls, monkeys with anterior cingulate cortex lesions had significant and selective unilateral expansion of the ventral anterior insula and significant relative bilateral expansion of the lateral nucleus of the amygdala. This work demonstrates the capacity for neuroplasticity in the interoceptive-allostatic network which, given that changes included expansion rather than atrophy, is likely to represent an adaptive response following damage.

Rhesus monkeys have an interoceptive sense of their beating hearts

Charbonneau JA, Maister L, Tsakiris M, Bliss-Moreau E (2022)

Proceedings of the National Academy of Sciences

The sensation of internal bodily signals, like when your stomach is contracting or your heart is beating, plays a critical role in broad biological and psychological functions, ranging from homeostasis to emotional experience and self-awareness. The evolutionary origins of this capacity and, thus, the extent to which it is present in nonhuman animals remains unclear. Here, we show that rhesus monkeys (Macaca mulatta) spend significantly more time viewing stimuli presented asynchronously, as compared to synchronously, with their heartbeats. This is consistent with evidence previously shown in human infants using a nearly identical experimental paradigm, suggesting that rhesus monkeys have a human-like capacity to integrate interoceptive signals from the heart with exteroceptive audiovisual information. As no prior work has demonstrated behavioral evidence of innate cardiac interoceptive ability in nonhuman animals, these results have important implications for our understanding of the evolution of this ability and for establishing rhesus monkeys as an animal model for human interoceptive function and dysfunction. We anticipate that this work may also provide an important model for future psychiatric research, as disordered interoceptive processing is implicated in a wide variety of psychiatric conditions.

Social housing status impacts rhesus monkeys’ affective responding in classic threat processing tasks

Charbonneau JA, Amaral DG, Bliss-Moreau E (2022)

Scientific Reports

Individuals’ social contexts are broadly recognized to impact both their psychology and neurobiology. These effects are observed in people and in nonhuman animals who are the subjects for comparative and translational science. The social contexts in which monkeys are reared have long been recognized to have significant impacts on affective processing. Yet, the social contexts in which monkeys live as adults are often ignored and could have important consequences for interpreting findings, particularly those related to biopsychiatry and behavioral neuroscience studies. The extant nonhuman primate neuropsychological literature has historically tested individually-housed monkeys, creating a critical need to understand how social context might impact the outcomes of such experiments. We evaluated affective responding in adult rhesus monkeys living in four different social contexts using two classic threat processing tasks—a test of responsivity to objects and a test of responsivity to an unfamiliar human. These tasks have been commonly used in behavioral neuroscience for decades. Relative to monkeys with full access to a social partner, individually-housed monkeys had blunted reactivity to threat and monkeys who had limited contact with their partner were more reactive to some threatening stimuli. These results indicate that monkeys’ social housing contexts impact affective reactivity and point to the potential need to reconsider inferences drawn from prior studies in which the impacts of social context have not been considered.

Amygdala or hippocampus damage only minimally impacts affective responding to threat

Charbonneau JA, Bennett JL, Bliss-Moreau E (2021)

Behavioral Neuroscience

Decades of research studying the behavioral effects of damage to structures in medial temporal lobe of rhesus monkeys have documented that such damage, particularly damage to the amygdala, causes animals to become hyporesponsive to threat and hyper-social. This phenotype, a subset of the behaviors known as “Klüver-Bucy Syndrome,” is one of the most well-known phenomena in behavioral neuroscience. Carrying on the tradition of evaluating hyposensitivity to threat in monkeys with temporal lobe lesions, we evaluated the responses of rhesus monkeys with bilateral ibotenic acid lesions of the amygdala or hippocampus and procedure-matched control animals to the presentation of an unfamiliar human intruder and threatening objects of varying complexity. All animals behaved as expected—calibrating their responses to the ostensible threat value of the stimuli such that they were most responsive to the most potent stimuli and least responsive to the least potent stimuli. Contrary to an earlier report (Mason et al., 2006), lesion status did not impact the pattern of responses across multiple dependent measures (overt behaviors, position in cage, etc.). The only lesion induced difference consistent with hyposensitivity to threat was that monkeys with amygdala lesions retrieved food rewards placed near reptile-like objects more rapidly than did control animals. These findings call into question the assumption that amygdala damage causes robust, stereotyped changes to affective behavior. They also highlight the importance of replication in neuroscientific studies using nonhuman primates.

Social learning exploits the available auditory or visual cues

Paraouty N, Charbonneau JA, Sanes DH (2020)

Scientific Reports

The ability to acquire a behavior can be facilitated by exposure to a conspecific demonstrator. Such social learning occurs under a range of conditions in nature. Here, we tested the idea that social learning can benefit from any available sensory cue, thereby permitting learning under different natural conditions. The ability of naïve gerbils to learn a sound discrimination task following 5 days of exposure adjacent to a demonstrator gerbil was tested in the presence or absence of visual cues. Naïve gerbils acquired the task significantly faster in either condition, as compared to controls. We also found that exposure to a demonstrator was more potent in facilitating learning, as compared to exposure to the sounds used to perform the discrimination task. Therefore, social learning was found to be flexible and equally efficient in the auditory or visual domains.

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