Volume electron microscopy for genetically and molecularly defined neural circuits.
Nobuhiko Ohno, Fuyuki Karube, Fumino Fujiyama
Neuroscience research, 22 Jun. 2024, [International Magazine]
English, Scientific journal, The brain networks responsible for adaptive behavioral changes are based on the physical connections between neurons. Light and electron microscopy have long been used to study neural projections and the physical connections between neurons. Volume electron microscopy has recently expanded its scale of analysis due to methodological advances, resulting in complete wiring maps of neurites in a large volume of brain tissues and even entire nervous systems in a growing number of species. However, structural approaches frequently suffer from inherent limitations in which elements in images are identified solely by morphological criteria. Recently, an increasing number of tools and technologies have been developed to characterize cells and cellular components in the context of molecules and gene expression. These advancements include newly developed probes for visualization in electron microscopic images as well as correlative integration methods for the same elements across multiple microscopic modalities. Such approaches advance our understanding of interactions between specific neurons and circuits and may help to elucidate novel aspects of the basal ganglia network involving dopamine neurons. These advancements are expected to reveal mechanisms for processing adaptive changes in specific neural circuits that modulate brain functions.

descSPIM: an affordable and easy-to-build light-sheet microscope optimized for tissue clearing techniques.
Kohei Otomo, Takaki Omura, Yuki Nozawa, Steven J Edwards, Yukihiko Sato, Yuri Saito, Shigehiro Yagishita, Hitoshi Uchida, Yuki Watakabe, Kiyotada Naitou, Rin Yanai, Naruhiko Sahara, Satoshi Takagi, Ryohei Katayama, Yusuke Iwata, Toshiro Shiokawa, Yoku Hayakawa, Kensuke Otsuka, Haruko Watanabe-Takano, Yuka Haneda, Shigetomo Fukuhara, Miku Fujiwara, Takenobu Nii, Chikara Meno, Naoki Takeshita, Kenta Yashiro, Juan Marcelo Rosales Rocabado, Masaru Kaku, Tatsuya Yamada, Yumiko Oishi, Hiroyuki Koike, Yinglan Cheng, Keisuke Sekine, Jun-Ichiro Koga, Kaori Sugiyama, Kenichi Kimura, Fuyuki Karube, Hyeree Kim, Ichiro Manabe, Tomomi Nemoto, Kazuki Tainaka, Akinobu Hamada, Hjalmar Brismar, Etsuo A Susaki
Nature communications, 15, 1, 4941, 4941, 12 Jun. 2024, [International Magazine]
English, Scientific journal, Despite widespread adoption of tissue clearing techniques in recent years, poor access to suitable light-sheet fluorescence microscopes remains a major obstacle for biomedical end-users. Here, we present descSPIM (desktop-equipped SPIM for cleared specimens), a low-cost ($20,000-50,000), low-expertise (one-day installation by a non-expert), yet practical do-it-yourself light-sheet microscope as a solution for this bottleneck. Even the most fundamental configuration of descSPIM enables multi-color imaging of whole mouse brains and a cancer cell line-derived xenograft tumor mass for the visualization of neurocircuitry, assessment of drug distribution, and pathological examination by false-colored hematoxylin and eosin staining in a three-dimensional manner. Academically open-sourced ( https://github.com/dbsb-juntendo/descSPIM ), descSPIM allows routine three-dimensional imaging of cleared samples in minutes. Thus, the dissemination of descSPIM will accelerate biomedical discoveries driven by tissue clearing technologies.

Pre- and Postembedding Immunoelectron Microscopy to Analyze the Central Nervous System
Fumino Fujiyama, Fuyuki Karube
Methods in Molecular Biology, 45, 62, Springer US, 18 Apr. 2024
In book

Anterograde trans-neuronal labeling of striatal interneurons in relation to dopamine neurons in the substantia nigra pars compacta
Fuyuki Karube, Yang Yang, Kenta Kobayashi, Fumino Fujiyama
Frontiers in Neuroanatomy, 18, Frontiers Media SA, 28 Feb. 2024
Scientific journal, Recent advances in neural tracing have unveiled numerous neural circuits characterized by brain region and cell type specificity, illuminating the underpinnings of specific functions and behaviors. Dopaminergic (DA) neurons in the midbrain are highly heterogeneous in terms of gene and protein expression and axonal projections. Different cell types within the substantia nigra pars compacta (SNc) tend to project to the striatum in a cell-type-dependent manner characterized by specific topography. Given the wide and dense distribution of DA axons, coupled with a combination of synaptic and volume transmission, it remains unclear how DA release is spatially and temporally regulated, to appropriately achieve specific behaviors and functions. Our hypothesis posits that hidden rules governing synapse formation between pre-synaptic DA neuron types and striatal neuron types may modulate the effect of DA at a single-cell level. To address this conjecture, we employed adeno-associated virus serotype 1 (AAV1) to visualize the neural circuitry of DA neurons. AAV1 has emerged as a potent anatomical instrument capable of labeling and visualizing pre- and post-synaptic neurons simultaneously through anterograde trans-synaptic labeling. First, AAV1-Cre was injected into the SNc, resulting in Cre expression in both medium spiny neurons and interneurons in the striatum. Due to the potential occurrence of the retrograde transfer of AAV1, only striatal interneurons were considered for trans-synaptic or trans-neuronal labeling. Interneuron types expressing parvalbumin, choline acetyltransferase, somatostatin, or nitrogen oxide synthase exhibited Cre expression. Using a combination of AAV1-Cre and Cre-driven fluorophore expressing AAVs, striatal interneurons and the axons originating from the SNc were visualized in distinct colors. Using immunofluorescence against neurotransmitter transporters, almost all axons in the striatum visualized using this approach were confirmed to be dopaminergic. Moreover, individual DA axons established multiple appositions on the somata and proximal dendrites of interneurons. This finding suggests that irrespective of the extensive and widespread axonal arborization of DA neurons, a particular DA neuron may exert a significant influence on specific interneurons. Thus, AAV1-based labeling of the DA system can be a valuable tool to uncover the concealed rules governing these intricate relationships.

Globus pallidus is not independent from striatal direct pathway neurons: an up-to-date review
Fumino Fujiyama, Fuyuki Karube, Yasuharu Hirai
Mol Brain, 17, 34, 2024, [Peer-reviewed]
English, Scientific journal

Empagliflozin attenuates arrhythmogenesis in diabetic cardiomyopathy by normalizing intracellular Ca2+ handling in ventricular cardiomyocytes.
Takahide Kadosaka, Masaya Watanabe, Hiroyuki Natsui, Takuya Koizumi, Motoki Nakao, Taro Koya, Hikaru Hagiwara, Rui Kamada, Taro Temma, Fuyuki Karube, Fumino Fujiyama, Toshihisa Anzai
American journal of physiology. Heart and circulatory physiology, 324, 3, H341-H354, 06 Jan. 2023, [International Magazine]
English, Scientific journal, Diabetic cardiomyopathy has been reported to increase the risk of fatal ventricular arrhythmia. The beneficial effects of the selective sodium-glucose co-transporter 2 inhibitor have not been fully examined in the context of anti-arrhythmic therapy, especially its direct cardioprotective effects despite the negligible SGLT2 expression in cardiomyocytes. We aimed to examine the anti-arrhythmic effects of empagliflozin (EMPA) treatment on diabetic cardiomyocytes, with a special focus on Ca2+ handling. We conducted echocardiography and hemodynamic studies and studied electrophysiology, Ca2+ handling, and protein expression in C57BLKS/J-leprdb/db mice (db/db mice) and their non-diabetic lean heterozygous Leprdb/+ littermates (db/+ mice). Preserved systolic function with diastolic dysfunction was observed in 16-week-old db/db mice. During arrhythmia induction, db/db mice had significantly increased premature ventricular complexes (PVCs) than controls, which was attenuated by EMPA. In protein expression analyses, calmodulin-dependent protein kinase II (CaMKII) Thr287 autophosphorylation and CaMKII-dependent RyR2 phosphorylation (S2814) were significantly increased in diabetic hearts, which were inhibited by EMPA. Additionally, global O-GlcNAcylation significantly decreased with EMPA treatment. Furthermore, EMPA significantly inhibited ventricular cardiomyocyte glucose uptake. Diabetic cardiomyocytes exhibited increased spontaneous Ca2+ events and decreased sarcoplasmic reticulum (SR) Ca2+ content, along with impaired Ca2+ transient, all of which normalized with EMPA treatment. Notably, most EMPA-induced improvements in Ca2+ handling were abolished by the addition of an O-GlcNAcase (OGA) inhibitor. In conclusion, EMPA attenuated ventricular arrhythmia inducibility by normalizing the intracellular Ca2+ handling, and we speculated that this effect was, at least partly, due to the inhibition of O-GlcNAcylation via the suppression of glucose uptake into cardiomyocytes.

Conservation of the Direct and Indirect Pathway Dichotomy in Mouse Caudal Striatum With Uneven Distribution of Dopamine Receptor D1- and D2-Expressing Neurons
Kumiko Ogata, Fuko Kadono, Yasuharu Hirai, Ken-ichi Inoue, Masahiko Takada, Fuyuki Karube, Fumino Fujiyama
Frontiers in Neuroanatomy, 16, Frontiers Media SA, 04 Feb. 2022, [Peer-reviewed], [Corresponding author]
English, Scientific journal, The striatum is one of the key nuclei for adequate control of voluntary behaviors and reinforcement learning. Two striatal projection neuron types, expressing either dopamine receptor D1 (D1R) or dopamine receptor D2 (D2R) constitute two independent output routes: the direct or indirect pathways, respectively. These pathways co-work in balance to achieve coordinated behavior. Two projection neuron types are equivalently intermingled in most striatal space. However, recent studies revealed two atypical zones in the caudal striatum: the zone in which D1R-neurons are the minor population (D1R-poor zone) and that in which D2R-neurons are the minority (D2R-poor zone). It remains obscure as to whether these imbalanced zones have similar properties on axonal projections and electrophysiology compared to other striatal regions. Based on morphological experiments in mice using immunofluorescence, in situ hybridization, and neural tracing, here, we revealed that the poor zones densely projected to the globus pallidus and substantia nigra pars lateralis, with a few collaterals in substantia nigra pars reticulata and compacta. Similar to that in other striatal regions, D1R-neurons were the direct pathway neurons. We also showed that the membrane properties of projection neurons in the poor zones were largely similar to those in the conventional striatum using in vitro electrophysiological recording. In addition, the poor zones existed irrespective of the age or sex of mice. We also identified the poor zones in the common marmoset as well as other rodents. These results suggest that the poor zones in the caudal striatum follow the conventional projection patterns irrespective of the imbalanced distribution of projection neurons. The poor zones could be an innate structure and common in mammals. The unique striatal zones possessing highly restricted projections could relate to functions different from those of motor-related striatum.

Acetylcholine from the nucleus basalis magnocellularis facilitates the retrieval of well-established memory
Shogo Soma, Naofumi Suematsu, Akinori Y Sato, Keisuke Tsunoda, Allen Bramian, Anish Reddy, Koki Takabatake, Fuyuki Karube, Fumino Fujiyama, Satoshi Shimegi
Neurobiology of Learning and Memory, 183, 107484, 107484, Elsevier BV, Sep. 2021, [Peer-reviewed]
Scientific journal

Modulatory Effects of Monoamines and Perineuronal Nets on Output of Cerebellar Purkinje Cells
Moritoshi Hirono, Fuyuki Karube, Yuchio Yanagawa
Frontiers in Neural Circuits, 15, Frontiers Media SA, 14 Jun. 2021, [Peer-reviewed]
Scientific journal, Classically, the cerebellum has been thought to play a significant role in motor coordination. However, a growing body of evidence for novel neural connections between the cerebellum and various brain regions indicates that the cerebellum also contributes to other brain functions implicated in reward, language, and social behavior. Cerebellar Purkinje cells (PCs) make inhibitory GABAergic synapses with their target neurons: other PCs and Lugaro/globular cells via PC axon collaterals, and neurons in the deep cerebellar nuclei (DCN) via PC primary axons. PC-Lugaro/globular cell connections form a cerebellar cortical microcircuit, which is driven by serotonin and noradrenaline. PCs’ primary outputs control not only firing but also synaptic plasticity of DCN neurons following the integration of excitatory and inhibitory inputs in the cerebellar cortex. Thus, strong PC-mediated inhibition is involved in cerebellar functions as a key regulator of cerebellar neural networks. In this review, we focus on physiological characteristics of GABAergic transmission from PCs. First, we introduce monoaminergic modulation of GABAergic transmission at synapses of PC-Lugaro/globular cell as well as PC-large glutamatergic DCN neuron, and a Lugaro/globular cell-incorporated microcircuit. Second, we review the physiological roles of perineuronal nets (PNNs), which are organized components of the extracellular matrix and enwrap the cell bodies and proximal processes, in GABA release from PCs to large glutamatergic DCN neurons and in cerebellar motor learning. Recent evidence suggests that alterations in PNN density in the DCN can regulate cerebellar functions.

Motor cortex can directly drive the globus pallidus neurons in a projection neuron type-dependent manner in the rat
Fuyuki Karube, Susumu Takahashi, Kenta Kobayashi, Fumino Fujiyama
eLife, 8, e49511, eLife Sciences Publications, Ltd, 12 Nov. 2019, [Peer-reviewed], [Lead author]
English, Scientific journal, The basal ganglia are critical for the control of motor behaviors and for reinforcement learning. Here, we demonstrate in rats that primary and secondary motor areas (M1 and M2) make functional synaptic connections in the globus pallidus (GP), not usually thought of as an input site of the basal ganglia. Morphological observation revealed that the density of axonal boutons from motor cortices in the GP was 47% and 78% of that in the subthalamic nucleus (STN) from M1 and M2, respectively. Cortical excitation of GP neurons was comparable to that of STN neurons in slice preparations. FoxP2-expressing arkypallidal neurons were preferentially innervated by the motor cortex. The connection probability of cortico-pallidal innervation was higher for M2 than M1. These results suggest that cortico-pallidal innervation is an additional excitatory input to the basal ganglia, and that it can affect behaviors via the cortex-basal ganglia-thalamus motor loop.

Thalamostriatal projections and striosome-matrix compartments.
Fujiyama F, Unzai T, KARUBE F
Neurochemistry International, 125, 67, 73, Jan. 2019, [Peer-reviewed], [Last author]
English, Scientific journal

Supramammillary Nucleus Afferents to the Dentate Gyrus Co-release Glutamate and GABA and Potentiate Granule Cell Output.
Hashimotodani Y, Karube F, Yanagawa Y, Fujiyama F, Kano M
Cell Reports, 25, 2704, 2715, Nov. 2018, [Peer-reviewed]
English, Scientific journal

Parvalbumin-producing striatal interneurons receive excitatory inputs onto proximal dendrites from the motor thalamus in male mice.
Yasutake Nakano, Fuyuki Karube, Yasuharu Hirai, Kenta Kobayashi, Hiroyuki Hioki, Shinichiro Okamoto, Hiroshi Kameda, Fumino Fujiyama
Journal of neuroscience research, 96, 7, 1186, 1207, Jul. 2018, [Peer-reviewed], [International Magazine]
English, Scientific journal, In rodents, the dorsolateral striatum regulates voluntary movement by integrating excitatory inputs from the motor-related cerebral cortex and thalamus to produce contingent inhibitory output to other basal ganglia nuclei. Striatal parvalbumin (PV)-producing interneurons receiving this excitatory input then inhibit medium spiny neurons (MSNs) and modify their outputs. To understand basal ganglia function in motor control, it is important to reveal the precise synaptic organization of motor-related cortical and thalamic inputs to striatal PV interneurons. To examine which domains of the PV neurons receive these excitatory inputs, we used male bacterial artificial chromosome transgenic mice expressing somatodendritic membrane-targeted green fluorescent protein in PV neurons. An anterograde tracing study with the adeno-associated virus vector combined with immunodetection of pre- and postsynaptic markers visualized the distribution of the excitatory appositions on PV dendrites. Statistical analysis revealed that the density of thalamostriatal appositions along the dendrites was significantly higher on the proximal than distal dendrites. In contrast, there was no positional preference in the density of appositions from axons of the dorsofrontal cortex. Population observations of thalamostriatal and corticostriatal appositions by immunohistochemistry for pathway-specific vesicular glutamate transporters confirmed that thalamic inputs preferentially, and cortical ones less preferentially, made apposition on proximal dendrites of PV neurons. This axodendritic organization suggests that PV neurons produce fast and reliable inhibition of MSNs in response to thalamic inputs and process excitatory inputs from motor cortices locally and plastically, possibly together with other GABAergic and dopaminergic dendritic inputs, to modulate MSN inhibition.

Perineuronal Nets in the Deep Cerebellar Nuclei Regulate GABAergic Transmission and Delay Eyeblink Conditioning.
Hirono M, Watanabe S, Karube F, Fujiyama F, Kawahara S, Nagao S, Yanagawa Y, Misonou H
The Journal of neuroscience : the official journal of the Society for Neuroscience, 38, 27, 6130, 6144, Jul. 2018, [Peer-reviewed]

Using a novel PV-Cre rat model to characterize pallidonigral cells and their terminations
Yoon-Mi Oh, Fuyuki Karube, Susumu Takahashi, Kenta Kobayashi, Masahiko Takada, Motokazu Uchigashima, Masahiko Watanabe, Kayo Nishizawa, Kazuto Kobayashi, Fumino Fujiyama
BRAIN STRUCTURE & FUNCTION, 222, 5, 2359, 2378, Dec. 2017, [Peer-reviewed]
English, Scientific journal

Substance P effects exclusively on prototypic neurons in mouse globus pallidus
Kazuko Mizutani, Susumu Takahashi, Shinichiro Okamoto, Fuyuki Karube, Fumino Fujiyama
BRAIN STRUCTURE & FUNCTION, 222, 9, 4089, 4110, Dec. 2017, [Peer-reviewed]
English, Scientific journal

Axon topography of layer 6 spiny cells to orientation map in the primary visual cortex of the cat (area 18)
Fuyuki Karube, Katalin Sari, Zoltan F. Kisvarday
BRAIN STRUCTURE & FUNCTION, 222, 3, 1401, 1426, Apr. 2017, [Peer-reviewed]
English, Scientific journal

Perineuronal nets in the deep cerebellar nuclei regulate GABAergic transmission and delay eyeblink conditioning　　　　　　　　　　　　　　　
Hirono M, Watanabe S, Karube F, Fujiyama F, Kawahara S, Nagao S, Yanagawa Y, Misonou H
J Neurosci, 291, 51, 2017, [Peer-reviewed]

Neuronal circuits and physiological roles of the basal ganglia in terms of transmitters, receptors and related disorders
Katsuya Yamada, Susumu Takahashi, Fuyuki Karube, Fumino Fujiyama, Kazuto Kobayashi, Akinori Nishi, Toshihiko Momiyama
JOURNAL OF PHYSIOLOGICAL SCIENCES, 66, 6, 435, 446, Nov. 2016, [Peer-reviewed]
English

The Diversity of Cortical Inhibitory Synapses
Yoshiyuki Kubota, Fuyuki Karube, Masaki Nomura, Yasuo Kawaguchi
FRONTIERS IN NEURAL CIRCUITS, 10, 27, Apr. 2016, [Peer-reviewed]
English, Scientific journal

Functional effects of distinct innervation styles of pyramidal cells by fast spiking cortical interneurons
Yoshiyuki Kubota, Satoru Kondo, Masaki Nomura, Sayuri Hatada, Noboru Yamaguchi, Alsayed A. Mohamed, Fuyuki Karube, Joachim Luebke, Yasuo Kawaguchi
ELIFE, 4, Jul. 2015, [Peer-reviewed]
English, Scientific journal

Morphological elucidation of basal ganglia circuits contributing reward prediction
Fumino Fujiyama, Susumu Takahashi, Fuyuki Karube
Frontiers in Neuroscience, 9, 6, Frontiers Research Foundation, 2015, [Peer-reviewed]
English

Long-lasting single-neuron labeling by in vivo electroporation without microscopic guidance
Kei Oyama, Shinya Ohara, Sho Sato, Fuyuki Karube, Fumino Fujiyama, Yoshikazu Isomura, Hajime Mushiake, Toshio Iijima, Ken-Ichiro Tsutsui
Journal of Neuroscience Methods, 218, 2, 139, 147, 15 Sep. 2013, [Peer-reviewed]
English, Scientific journal

Specialized Cortical Subnetworks Differentially Connect Frontal Cortex to Parahippocampal Areas
Yasuharu Hirai, Mieko Morishima, Fuyuki Karube, Yasuo Kawaguchi
JOURNAL OF NEUROSCIENCE, 32, 5, 1898, 1913, Feb. 2012, [Peer-reviewed]
English, Scientific journal

Conserved properties of dendritic trees in four cortical interneuron subtypes
Yoshiyuki Kubota, Fuyuki Karube, Masaki Nomura, Allan T. Gulledge, Atsushi Mochizuki, Andreas Schertel, Yasuo Kawaguchi
SCIENTIFIC REPORTS, 1, 89, doi:10.1038/srep00089, Sep. 2011, [Peer-reviewed]
English, Scientific journal

Selective Coexpression of Multiple Chemical Markers Defines Discrete Populations of Neocortical GABAergic Neurons
Yoshiyuki Kubota, Naoki Shigematsu, Fuyuki Karube, Akio Sekigawa, Satoko Kato, Noboru Yamaguchi, Yasuharu Hirai, Mieko Morishima, Yasuo Kawaguchi
CEREBRAL CORTEX, 21, 8, 1803, 1817, Aug. 2011, [Peer-reviewed]
English, Scientific journal

Axon Topography of Layer IV Spiny Cells to Orientation Map in the Cat Primary Visual Cortex (Area 18)
Fuyuki Karube, Zoltan F. Kisvarday
CEREBRAL CORTEX, 21, 6, 1443, 1458, Jun. 2011, [Peer-reviewed]
English, Scientific journal

Dendritic dimensions and signal conduction properties of cortical nonpyramidal cells
Kubota Yoshiyuki, Karube Fuyuki, Nomura Masaki, Gulledge Allan T, Mochizuki Atsushi, Kawaguchi Yasuo
NEUROSCIENCE RESEARCH, 68, E12, 2010, [Peer-reviewed]

Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
Giorgio A. Ascoli, Lidia Alonso-Nanclares, Stewart A. Anderson, German Barrionuevo, Ruth Benavides-Piccione, Andreas Burkhalter, Gyoergy Buzsaki, Bruno Cauli, Javier DeFelipe, Alfonso Fairen, Dirk Feldmeyer, Gord Fishell, Yves Fregnac, Tamas F. Freund, Daniel Gardner, Esther P. Gardner, Jesse H. Goldberg, Moritz Helmstaedter, Shaul Hestrin, Fuyuki Karube, Zoltan F. Kisvarday, Bertrand Lambolez, David A. Lewis, Oscar Marin, Henry Markram, Alberto Munoz, Adam Packer, Carl C. H. Petersen, Kathleen S. Rockland, Jean Rossier, Bernardo Rudy, Peter Somogyi, Jochen F. Staiger, Gabor Tamas, Alex M. Thomson, Maria Toledo-Rodriguez, Yun Wang, David C. West, Rafael Yuste
NATURE REVIEWS NEUROSCIENCE, 9, 7, 557, 568, Jul. 2008, [Peer-reviewed]
English

Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats
Masakazu Uematsu, Yasuharu Hirai, Fuyuki Karube, Satoe Ebihara, Megumi Kato, Kuniya Abe, Kunihiko Obata, Sachiko Yoshida, Masumi Hirabayashi, Yuchio Yanagawa, Yasuo Kawaguchi
CEREBRAL CORTEX, 18, 2, 315, 330, Feb. 2008, [Peer-reviewed]
English, Scientific journal

Dendritic dimensions of cortical nonpyramidal cells
Kubota Yoshiyuki, Karube Fuyuki, Nomura Masaki, Aoyagi Toshio, Mochizuki Atsushi, Kawaguchi Yasuo
NEUROSCIENCE RESEARCH, 58, S73, 2007, [Peer-reviewed]

Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents
Yoshiyuki Kubota, Sayuri Hatada, Satoru Kondo, Fuyuki Karube, Yasuo Kawaguchi
JOURNAL OF NEUROSCIENCE, 27, 5, 1139, 1150, Jan. 2007, [Peer-reviewed]
English, Scientific journal

Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells
Y Kawaguchi, F Karube, Y Kubota
CEREBRAL CORTEX, 16, 5, 696, 711, May 2006, [Peer-reviewed]
English, Scientific journal

Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes
F Karube, Y Kubota, Y Kawaguchi
JOURNAL OF NEUROSCIENCE, 24, 12, 2853, 2865, Mar. 2004, [Peer-reviewed]
English, Scientific journal

Combinative Stimulation Inactivates Sex Pheromone Production in the Silkworm Moth, Bombyx mori
Fuyuki Karube, Masahiko Kobayashi
Archives of Insect Biochemistry and Physiology, 42, 2, 111, 118, John Wiley and Sons Ltd, 1999, [Peer-reviewed]
English, Scientific journal

Presence of eupyrene spermatozoa in vestibulum accelerates oviposition in the silkworm moth, Bombyx mori
Fuyuki Karube, Masahiko Kobayashi
Journal of Insect Physiology, 45, 10, 947, 957, Elsevier Ltd, 1999, [Peer-reviewed]
English, Scientific journal

structure and function of basal ganglia　　　　　　　　　　　　　　　
藤山文乃, 高橋晋, 苅部冬紀, Clinical Neuroscience, 35, 268, 270, 2017, [Invited]

Morphological elucidation of basal ganglia circuits contributing reward prediction
Fumino Fujiyama, Susumu Takahashi, Fuyuki Karube, FRONTIERS IN NEUROSCIENCE, 9, Feb. 2015
English, Book review

Topographical organization of layer 4 and 6 spiny neurons over functional maps for visual signals in cat area 18
Fuyuki Karube, Zoltan F. Kisvarday, NEUROSCIENCE RESEARCH, 68, E152, E152, 2010
English, Summary international conference

Cerebral Cortex: Inhibitory Cells
Y. Kawaguchi, F. Karube, Encyclopedia of Neuroscience, 775, 783, 2010
Elsevier Ltd, English

Dendritic shape and EPSP conduction of cortical nonpyramidal cells
Yoshiyuki Kubota, Fuyuki Karube, Masaki Nomura, Toshio Aoyagi, Yasuo Kawaguchi, NEUROSCIENCE RESEARCH, 65, S84, S84, 2009
English, Summary international conference

DENDRITIC MORPHOLOGIY AND SIGNAL CONDUCTION PROPERTY OF CORTICAL NONPYRAMIDAL CELLS
Yoshiyuki Kubota, Fuyuki Karube, Masaki Nomura, Toshio Aoyagi, Yasuo Kawaguchi, JOURNAL OF PHYSIOLOGICAL SCIENCES, 59, 77, 77, 2009
English, Summary international conference

大脳皮質棘突起への興奮性入力と抑制性入力の二重支配　　　　　　　　　　　　　　　
窪田 芳之, 畑田 さゆり, 根東 覚, 苅部 冬紀, 川口 泰雄, 解剖学雑誌, 82, Suppl., 225, 225, Mar. 2007
(一社)日本解剖学会, Japanese

大脳基底核 意志と行動の狭間にある神経回路　　　　　　　　　　　　　　　
苅部 冬紀, 高橋 晋, 藤山 文乃
共立出版, Jul. 2019, [Joint work]

脳科学辞典：錐体細胞　　　　　　　　　　　　　　　
2012

"Structures and Circuits: Cerebral Cortex, Inhibitory cells". In The New Encyclopedia of Neuroscience (ed Squire L)　　　　　　　　　　　　　　　
Elsevier, Oxford, UK., 2008