Strengths and challenges of longitudinal non-human primate neuroimaging

Song, Xiaowei; García-Saldivar, Pamela; Kindred, Nathan; Wang, Yujiang; Merchant, Hugo; Meguerditchian, Adrien; Yang, Yihong; Stein, Elliot A.; Bradberry, Charles W.; Hamed, Suliann Ben; Jedema, Hank P.; Poirier, Colline

doi:10.1016/j.neuroimage.2021.118009

Cited by 13 publications

(8 citation statements)

References 117 publications

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“…Recent work found few differences between adolescent and adult NHP using an ICA-based comparison of resting-state data (22); our finegrained FC analyses identified several specific neural circuits associated with adolescent development, while also illuminating large-scale organizational differences between adolescents and adults. Our longitudinal approach allowed for the identification of true aging effects by capturing the development process as a within-subject effect and potentially allowing the investigation of individual variability over three time points covering the adolescence period (68). Together, these findings provide specificity in our understanding of the development of functional brain circuits during and into late adolescence.…”

Section: Discussionmentioning

confidence: 99%

Age-related development in prefrontal-subcortical resting-state functional connectivity in nonhuman primates

Deshpande

Kohut

2023

Preprint

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Introduction: Understanding age related changes in functional connectivity (FC) with regards to the maturation trajectories of cortical subcortical circuits is critical for identifying biomarkers for disease vulnerability. The present study investigated resting state FC in adolescent and adult nonhuman primates to characterize developmentally sensitive functional brain circuits. Methods: Resting-state fMRI data were acquired in adolescent (33.3 (sd=1.59) months; n=22) and adult (117.29 (sd=2.86) months; n=15) squirrel monkeys and FC was compared in seven prefrontal and ten subcortical regions of interest (ROIs). The effect of subject age on FC between each pair of ROIs was evaluated to identify nodes with the most age sensitive connections (hubs) which were then used in seed-to-whole brain FC analyses. A subset of adolescents (n=7) was also assessed over 3 longitudinal scans to track changes in hub connectivity throughout adolescence. Results: A significant effect of age on ROI to ROI FC was found for adolescent (p<0.001), but not adult, subjects (p=0.8). Evaluation of parameter estimates (beta) for each ROI to ROI pair found three within-prefrontal (dorsolateral (dlPFC), dorsomedial (dmPFC), and medial orbitofrontal cortices), two within-subcortical (R amygdala and L hippocampus), and three between prefrontal-subcortical (dlPFC, dmPFC, L caudate) hubs with the highest number of age-related connections. Large scale organizational differences were also observed between the adolescent and adult groups. Longitudinal scans found within subject changes in FC consistent with group effect. Conclusions: The relationship between changes in FC and age during adolescence indicates dynamic maturation of several prefrontal to subcortical circuits in nonhuman primates. These findings provide specificity in our understanding of the development of functional brain circuits during and into late adolescence.

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Section: Discussionmentioning

confidence: 99%

Age-related development in prefrontal-subcortical resting-state functional connectivity in nonhuman primates

Deshpande

Kohut

2023

Preprint

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“…This suggests the intriguing possibility that the storage location of WM representations and site of top-down control signals can occur in the same area depending on learning and task demands. Future work using longitudinal paradigms in NHP studies might also clarify the importance of training, spatial scale, and species differences on WM maintenance processes (Badre et al, 2015; Milham et al, 2018; Song et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Long-term learning transforms prefrontal cortex representations during working memory

Miller

Tambini

Kiyonaga

et al. 2022

Preprint

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The lateral prefrontal cortex (lPFC) is reliably active during working memory (WM) across human and animal models, but the role of lPFC in successful WM is under debate. For instance, non-human primate (NHP) electrophysiology research finds that lPFC circuitry stores WM representations. Human neuroimaging instead suggests that lPFC plays a control function over WM content that is stored in sensory cortices. These seemingly incompatible WM accounts are often confounded by differences in the amount of task training and stimulus exposure across studies (i.e., NHPs tend to be trained extensively). Here, we test the possibility that such long-term training may alter the role of lPFC in WM maintenance. We densely sampled WM-related activity across learning, in three human participants, using a longitudinal functional MRI (fMRI) protocol. Over three months, participants trained on (1) a serial reaction time (SRT) task, wherein complex fractal stimuli were embedded within probabilistic sequences, and (2) a delayed recognition task probing WM for trained or novel stimuli. Participants were scanned frequently throughout training, to track how WM activity patterns change with repeated stimulus exposure and long-term associative learning. WM task performance improved for trained (but not novel) fractals and, neurally, delay activity significantly increased in distributed lPFC voxels across learning. Pattern similarity analyses also found that item-level WM representations emerged within lPFC, but not in sensory cortices, and lPFC delay activity increasingly reflected sequence relationships from the SRT task, even though that information was task-irrelevant for WM. These findings demonstrate that human lPFC develops stimulus-selective WM responses with learning and WM representations are shaped by long-term experience. Influences from training and long-term memory may reconcile competing accounts of lPFC function during WM.

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“…Yet, the necessity to increase NHP subjects to address limits in statistical power faces ethical aspects related to animal welfare in the case of invasive neuroimaging studies. The development of fNIRS (Debracque et al 2021) and longitudinal studies in comparative neuroscience (Song et al 2021) would thus allow answering parts of these challenges.…”

Section: Discussionmentioning

confidence: 99%

Cerebral activity in monkeys Papio anubis during the perception of conspecific and heterospecific agonistic vocalizations: A functional Near Infrared Spectroscopy study

Debracque

Gruber

Lacoste

et al. 2022

Preprint

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Are conspecific emotional vocalizations special? Although often investigated in non-human primates using functional magnetic resonance imaging or positron emission tomography, it remains unclear whether the listening of conspecific vocal emotions leads to similar or different cerebral activations when compared to heterospecific calls (i.e. expressed by another primate species). Using a neuroimaging technique rarely employed in monkeys so far, functional Near Infrared Spectroscopy (fNIRS), the present study investigated cortical temporal activities during exposure to both conspecific and heterospecific calls in three female adult baboons (Papio anubis). The three subjects were lightly anesthetized and passively exposed to agonistic baboon and chimpanzee (Pan troglodytes) vocalizations, as well as energy matched white noises in order to control for this low-level acoustic feature. Despite inter-individual variabilities, permutation test analyses on the extracted OxyHemoglobin signal revealed for two subjects out of three significant differences between the passive listening of baboon versus chimpanzee stimuli. Additionally, in one subject, a modulation of the left temporal cortex activity was found for the perception of baboon calls contrasted to chimpanzee vocalizations as well as for the passive listening of baboon white noises compared to chimpanzee ones. Although the lack of generalization of those findings in all three subjects prevents us to drawn any conclusion and that more subjects would be needed, the hypothesis that baboons’ cortical temporal regions may be more sensitive to the processing of conspecific sounds compared to heterospecific stimuli is not excluded. Our study highlights that fNIRS may be a promising alternative to further investigate the auditory mechanisms at play in the right and left baboons’ temporal cortices for the processing of emotional vocalizations.

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Strengths and challenges of longitudinal non-human primate neuroimaging

Cited by 13 publications

References 117 publications

Age-related development in prefrontal-subcortical resting-state functional connectivity in nonhuman primates

Age-related development in prefrontal-subcortical resting-state functional connectivity in nonhuman primates

Long-term learning transforms prefrontal cortex representations during working memory

Cerebral activity in monkeys Papio anubis during the perception of conspecific and heterospecific agonistic vocalizations: A functional Near Infrared Spectroscopy study

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