Chemogenetic dissection of the primate prefronto-subcortical pathways for working memory and decision-making

Oyama, Kei; Hori, Yukiko; Nagai, Yuji; Miyakawa, Naohisa; Mimura, Koki; Hirabayashi, Toshiyuki; Inoue, Ken; Suhara, Tetsuya; Takada, Masahiko; Higuchi, Makoto; Minamimoto, Takafumi

doi:10.1126/sciadv.abg4246

Cited by 47 publications

(43 citation statements)

References 68 publications

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“…PK, pharmacokinetics study; J, Japanese; R, Rhesus. #229 and #245 were used in our previous studies ( Nagai et al, 2020 ; Oyama et al, 2021 ).…”

Section: Methodsmentioning

confidence: 99%

“…Two monkeys (#229 and #245) received injections of AAV vector into the bilateral PFC (Brodmann's area 46) as described previously ( Nagai et al, 2020 ; Oyama et al, 2021 ). The frontal cortex was exposed by removing a bone flap and reflecting the dura mater.…”

Section: Methodsmentioning

confidence: 99%

“…Importantly, low doses of DCZ exert chemogenetic effects with rapid onset that last several hours in both rodents and nonhuman primates ( Nagai et al, 2020 ). This indicates that DCZ is a promising chemogenetic actuator that can be used for a wide variety of objectives (e.g., Hirabayashi et al, 2021 ; Hori et al, 2021 ; Oyama et al, 2021 ). In particular, its superior efficacy and brain permeability permit its use for oral administration.…”

Section: Introductionmentioning

confidence: 99%

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Chronic Behavioral Manipulation via Orally Delivered Chemogenetic Actuator in Macaques

et al. 2022

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“…PK, pharmacokinetics study; J, Japanese; R, Rhesus. #229 and #245 were used in our previous studies ( Nagai et al, 2020 ; Oyama et al, 2021 ).…”

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Chronic Behavioral Manipulation via Orally Delivered Chemogenetic Actuator in Macaques

et al. 2022

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“…Recent advances in viral vectors that enable targeting specific neurons are likely essential for subsequent studies. These include viral tools targeting neurons with specific projections ( Inoue et al, 2015 ; Oyama et al, 2021 ), or specific interneurons in non-human primates ( Dimidschstein et al, 2016 ; Vormstein-Schneider et al, 2020 ; Mich et al, 2021 ), as well as enhancer-based viral vectors targeting entorhinal excitatory cells ( Nair et al, 2020 ). The cell-type-based global map provided in this study will accelerate the application of these genetic tools in monkeys for better understanding of the role of EC in memory and navigation and will further the translational potential of the experimental observations in monkeys.…”

Section: Discussionmentioning

confidence: 99%

Laminar Organization of the Entorhinal Cortex in Macaque Monkeys Based on Cell-Type-Specific Markers and Connectivity

Ohara

Yoshino

Kimura

et al. 2021

Front. Neural Circuits

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The entorhinal cortex (EC) is a major gateway between the hippocampus and telencephalic structures, and plays a critical role in memory and navigation. Through the use of various molecular markers and genetic tools, neuron types constituting EC are well studied in rodents, and their layer-dependent distributions, connections, and functions have also been characterized. In primates, however, such cell-type-specific understandings are lagging. To bridge the gap between rodents and primates, here we provide the first cell-type-based global map of EC in macaque monkeys. The laminar organization of the monkey EC was systematically examined and compared with that of the rodent EC by using immunohistochemistry for molecular markers which have been well characterized in the rodent EC: reelin, calbindin, and Purkinje cell protein 4 (PCP4). We further employed retrograde neuron labeling from the nucleus accumbens and amygdala to identify the EC output layer. This cell-type-based approach enabled us to apply the latest laminar definition of rodent EC to monkeys. Based on the similarity of the laminar organization, the monkey EC can be divided into two subdivisions: rostral and caudal EC. These subdivisions likely correspond to the lateral and medial EC in rodents, respectively. In addition, we found an overall absence of a clear laminar arrangement of layer V neurons in the rostral EC, unlike rodents. The cell-type-based architectural map provided in this study will accelerate the application of genetic tools in monkeys for better understanding of the role of EC in memory and navigation.

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“…The implementation of multimodal neuroimaging with neurophysiological recordings in NHPs will be critical for characterizing the underlying network principles available in brain networks. In the future, the use of network analysis tools in combination with optogenetic ( Klein et al., 2016 ; Ortiz-Rios et al., 2021 ; Tervo et al., 2016 ) or chemogenetic interrogation techniques ( Inoue et al., 2015 ; Oyama et al., 2021 ) might enable the targeted control of neural circuits via intervention of central nodes, possibly affecting global network states.…”

Section: Discussionmentioning

confidence: 99%

Dynamic reconfiguration of macaque brain networks during natural vision

Ortiz-Rios

Balezeau²,

Haag

et al. 2021

NeuroImage

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Natural vision engages a wide range of higher-level regions that integrate visual information over the large-scale brain network. How interareal connectivity reconfigures during the processing of ongoing natural visual scenes and how these dynamic functional changes relate to the underlaying anatomical links between regions is not well understood. Here, we hypothesized that macaque visual brain regions are poly-functional sharing the capacity to change their configuration state depending on the nature of visual input. To address this hypothesis, we reconstructed networks from in-vivo diffusion-weighted imaging (DWI) and functional magnetic resonance imaging (fMRI) data obtained in four alert macaque monkeys viewing naturalistic movie scenes. At first, we characterized network properties and found greater interhemispheric density and greater inter-subject variability in free-viewing networks as compared to structural networks. From the structural connectivity, we then captured modules on which we identified hubs during free-viewing that formed a widespread visuo-saccadic network across frontal (FEF, 46v), parietal (LIP, Tpt), and occipitotemporal modules (MT, V4, TEm), and that excluded primary visual cortex. Inter-subject variability of well-connected hubs reflected subject-specific configurations that largely recruited occipito-parietal and frontal modules. Across the cerebral hemispheres, free-viewing networks showed higher correlations among long-distance brain regions as compared to structural networks. From these findings, we hypothesized that long-distance interareal connectivity could reconfigure depending on the ongoing changes in visual scenes. Testing this hypothesis by applying temporally resolved functional connectivity we observed that many structurally defined areas (such as areas V4, MT/MST and LIP) were poly-functional as they were recruited as hub members of multiple network states that changed during the presentation of scenes containing objects, motion, faces, and actions. We suggest that functional flexibility in macaque macroscale brain networks is required for the efficient interareal communication during active natural vision. To further promote the use of naturalistic free-viewing paradigms and increase the development of macaque neuroimaging resources, we share our datasets in the PRIME-DE consortium.

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Chemogenetic dissection of the primate prefronto-subcortical pathways for working memory and decision-making

Cited by 47 publications

References 68 publications

Chronic Behavioral Manipulation via Orally Delivered Chemogenetic Actuator in Macaques

Chronic Behavioral Manipulation via Orally Delivered Chemogenetic Actuator in Macaques

Laminar Organization of the Entorhinal Cortex in Macaque Monkeys Based on Cell-Type-Specific Markers and Connectivity

Dynamic reconfiguration of macaque brain networks during natural vision

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