Mesoscale emotion circuits related to medial pulvinar revealed by INS-fMRI in macaque monkeys
Poster No:
2
Submission Type:
Abstract Submission
Authors:
Yuqi Feng1,2, An Ping3, Songping Yao1,2, Sunhang Shi1,2, Meilan Liu1,2, Henry Evrard4,5,6, Jianbao Wang2,7,8, Anna Roe1,2,8
Institutions:
1College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China, 2Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University, Hangzhou, China, 3Department of Neurosurgery, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, China, 4International Center for Primate Brain Research, Chinese Academy of Sciences, Shanghai, China, 5Werner Reichardt Center for Integrative Neuroscience, Karl Eberhard University of Tübingen, Tübingen, Germany, 6Max Planck Institute for Biological Cybernetics, Tübingen, Germany, 7Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang Univeristy, Hangzhou, China, 8MOE Frontier Science Center for Brain Science and Brain-Machine Integration, Zhejiang University, Hangzhou, China
First Author:
Yuqi Feng
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
Co-Author(s):
An Ping
Department of Neurosurgery, The Second Affiliated Hospital of Zhejiang University School of Medicine
Hangzhou, China
Department of Neurosurgery, The Second Affiliated Hospital of Zhejiang University School of Medicine
Hangzhou, China
Songping Yao
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
Sunhang Shi
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
Meilan Liu
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University
Hangzhou, China|Hangzhou, China
Henry Evrard
International Center for Primate Brain Research, Chinese Academy of Sciences|Werner Reichardt Center for Integrative Neuroscience, Karl Eberhard University of Tübingen|Max Planck Institute for Biological Cybernetics
Shanghai, China|Tübingen, Germany|Tübingen, Germany
International Center for Primate Brain Research, Chinese Academy of Sciences|Werner Reichardt Center for Integrative Neuroscience, Karl Eberhard University of Tübingen|Max Planck Institute for Biological Cybernetics
Shanghai, China|Tübingen, Germany|Tübingen, Germany
Jianbao Wang
Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University|Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang Univeristy|MOE Frontier Science Center for Brain Science and Brain-Machine Integration, Zhejiang University
Hangzhou, China|Hangzhou, China|Hangzhou, China
Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University|Affiliated Mental Health Center & Hangzhou Seventh People's Hospital, Zhejiang Univeristy|MOE Frontier Science Center for Brain Science and Brain-Machine Integration, Zhejiang University
Hangzhou, China|Hangzhou, China|Hangzhou, China
Anna Roe, Phd
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University|MOE Frontier Science Center for Brain Science and Brain-Machine Integration, Zhejiang University
Hangzhou, China|Hangzhou, China|Hangzhou, China
College of Biomedical Engineering and Instrument Science, Zhejiang University|Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University|MOE Frontier Science Center for Brain Science and Brain-Machine Integration, Zhejiang University
Hangzhou, China|Hangzhou, China|Hangzhou, China
Introduction:
In primates, how the experience of emotion (including the feeling of emotion, motor expression, and interoceptive aspects) is integrated in the brain is poorly understood. The medial pulvinar (PM) is a key nucleus that potentially links these multiple limbic modalities into a specific experience (Romanski, 1997; Homman-Ludiye, 2019; Froesel, 2021). Here, we use focal Infrared Neural Stimulation combined with ultra-high-field 7T functional magnetic resonance imaging (INS-fMRI) to map mesoscale functional connectivity (Xu, 2019; Shi, 2021; Yao, 2023) between PM and emotion-related areas in macaque monkeys in vivo, specifically, cingulate cortex (motor expression, Morecraft, 2007), insular cortex (interoception, Evrard, 2019), and amygdala (sensory, cognitive, and physiological axes of emotion, Gothard, 2020).
Methods:
INS in PM: All procedures were approved by the IACUC of Zhejiang University, in accordance with NIH guidelines. In two anesthetized adult macaque monkeys (sufentanil, 1–2 μg/kg/h), an optical fiber (200 μm diameter, 1875 nm light) was inserted into right PM (Fig 1B). Each INS trial consisted of a 9.5 sec stimulus (four 0.5 sec pulse trains of 0.25 ms pulses at 200 hz). At each stimulation site, we conducted 2-3 runs, 15 trials per run (Fig 1F). After testing intensity dependence (0.1 to 0.3 J/cm2), we acquired all at 0.3 J/cm2.
Scanning & Analysis: Using 7T scanner (Siemens Healthineers) and single loop RAPID coil, structural images (0.3 mm isotropic, MPRAGE) and functional images (1.5 mm isotropic, EPI, TR=2000 ms, TE=22 ms) were collected. Using GLM, significant activations (FDR-corrected p<0.005) in the ipsilateral cingulate, insula, and amygdala were identified. Repeat INS runs demonstrated reproducibility.
Scanning & Analysis: Using 7T scanner (Siemens Healthineers) and single loop RAPID coil, structural images (0.3 mm isotropic, MPRAGE) and functional images (1.5 mm isotropic, EPI, TR=2000 ms, TE=22 ms) were collected. Using GLM, significant activations (FDR-corrected p<0.005) in the ipsilateral cingulate, insula, and amygdala were identified. Repeat INS runs demonstrated reproducibility.
Results:
We conducted sequential INS stimulation in PM in two monkeys (Monkeys P, Y). Here, we presented activations evoked by 3 sites in monkey P, embedded in the suborganization of cingulate and insula (Fig 2A). As shown in Fig 2B-2C, activations appeared as small patches (mean diameter: cingulate 1.69 mm, insula 2.15 mm). The distributed patterns of these patches, arising from each site in PM, collectively formed a functional connectivity map with the cingulate and insula.
To study the topographic organization, we color coded patches into red (site 1), green (site 2) and blue (site 3). Patches from different sites were largely non-overlapping (Fig 2D), indicating each PM site has distinct connections with these areas. Patches in Area 24 appeared in 'face-arm-leg' motor clusters (yellow circles in Fig 2B). In insula Id and dorsal Ig, the patches were clustered into different groups, which appeared to coincide with insula functional subdivisions (yellow ovals in Fig 2C).
To further evaluate distinctions between Area 24 and 23, we examined the connectivity of the anterior 'face' cluster (Area 24) and the posterior 'face' cluster (Area 23) using seed-based analysis. We found that anterior cingulate 'face' seeds exhibited strong connectivity with medial prefrontal areas (Areas 32, 25, 10) and not motor areas, while posterior cingulate 'face' seeds correlated strongly with motor areas (Areas F1, F2, F6) and not frontal areas, providing a mesoscale view of previous distinctions between Area 24 and 23 (Rolls, 2019).
To study the topographic organization, we color coded patches into red (site 1), green (site 2) and blue (site 3). Patches from different sites were largely non-overlapping (Fig 2D), indicating each PM site has distinct connections with these areas. Patches in Area 24 appeared in 'face-arm-leg' motor clusters (yellow circles in Fig 2B). In insula Id and dorsal Ig, the patches were clustered into different groups, which appeared to coincide with insula functional subdivisions (yellow ovals in Fig 2C).
To further evaluate distinctions between Area 24 and 23, we examined the connectivity of the anterior 'face' cluster (Area 24) and the posterior 'face' cluster (Area 23) using seed-based analysis. We found that anterior cingulate 'face' seeds exhibited strong connectivity with medial prefrontal areas (Areas 32, 25, 10) and not motor areas, while posterior cingulate 'face' seeds correlated strongly with motor areas (Areas F1, F2, F6) and not frontal areas, providing a mesoscale view of previous distinctions between Area 24 and 23 (Rolls, 2019).
Conclusions:
We found that the connections from sequential INS stimulation sites in PM to cingulate and insula were patchy and clustered, indicating connections were mesoscale and topographically organized. We suggest this reflects a 3-tiered hierarchy of limbic circuit integration: (a) Single sites in PM led to concurrent global activations in cingulate, insula, and amygdala; (b) Single sites in PM led to concurrent activation in multiple modalities within each area; (c) Sequential sites in PM connected to sequences of largely non-overlapping patches within each modality of these three areas. This suggests that emotion-related networks in primate brain are fundamentally quite orderly.
Brain Stimulation:
Deep Brain Stimulation 1
Emotion, Motivation and Social Neuroscience:
Emotion and Motivation Other
Modeling and Analysis Methods:
Connectivity (eg. functional, effective, structural) 2
Keywords:
FUNCTIONAL MRI
Limbic Systems
Thalamus
Other - Pulvinar
1|2Indicates the priority used for review
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Provide references using APA citation style.
Homman‐Ludiye, J. (2019). The medial pulvinar: function, origin and association with neurodevelopmental disorders. Journal of anatomy, 235(3), 507-520.
Froesel, M. (2021). A multisensory perspective onto primate pulvinar functions. Neuroscience & Biobehavioral Reviews, 125, 231-243.
Xu, A. G. (2019). Focal infrared neural stimulation with high-field functional MRI: a rapid way to map mesoscale brain connectomes. Science advances, 5(4), eaau7046.
Shi, S. (2021). Infrared neural stimulation with 7T fMRI: A rapid in vivo method for mapping cortical connections of primate amygdala. NeuroImage, 231, 117818.
Yao, S. (2023). Functional topography of pulvinar–visual cortex networks in macaques revealed by INS–fMRI. Journal of Comparative Neurology, 531(6), 681-700.
Morecraft, R. J. (2007). Amygdala interconnections with the cingulate motor cortex in the rhesus monkey. Journal of Comparative Neurology, 500(1), 134-165.
Evrard, H. C. (2019). The organization of the primate insular cortex. Frontiers in neuroanatomy, 13, 43.
Gothard, K. M. (2020). Multidimensional processing in the amygdala. Nature Reviews Neuroscience, 21(10), 565-575.
Rolls, E. T. (2019). The cingulate cortex and limbic systems for emotion, action, and memory. Brain Structure and Function, 224(9), 3001-3018.