研究等業績 - 原著論文 - 山方 恒宏
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Shun Hiramatsu, Kokoro Saito, Shu Kondo, Hidetaka Katow, Nobuhiro Yamagata, Chun-Fang Wu, Hiromu Tanimoto
eLife ( eLife Sciences Publications, Ltd ) 2024年07月 [査読有り]
研究論文（学術雑誌）
Dopamine can play opposing physiological roles depending on the receptor subtype. In the fruit fly Drosophila melanogaster, Dop1R1 and Dop2R encode the D1- and D2-like receptors, respectively, and are reported to oppositely regulate intracellular cAMP levels. Here, we profiled the expression and subcellular localization of endogenous Dop1R1 and Dop2R in specific cell types in the mushroom body circuit. For cell-type-specific visualization of endogenous proteins, we employed reconstitution of split-GFP tagged to the receptor proteins. We detected dopamine receptors at both presynaptic and postsynaptic sites in multiple cell types. Quantitative analysis revealed enrichment around the active zones, particularly for Dop2R. The presynaptic localization of Dop1R1 and Dop2R in dopamine neurons suggests dual feedback regulation as autoreceptors. Furthermore, we discovered a starvation-dependent, bidirectional modulation of the presynaptic receptor expression in the PAM and PPL1 clusters, two distinct subsets of dopamine neurons, suggesting regulation of appetitive behaviors. Our results highlight the significance of the co-expression of the two antagonizing dopamine receptors in the spatial and conditional regulation of dopamine responses in neurons.
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Aroma nudges in bugs: Sensory perception and memory in insects
Mizunami M, Yamagata N
Current Opinion in Insect Science ( Elsevier ) 61 ( 101165 ) 2024年01月 [査読有り]
研究論文（学術雑誌） 国内共著
Insects are truly remarkable creatures that have evolved highly advanced sensory systems to thrive in diverse environments. From their keen sense of vision to their sophisticated olfactory, gustatory, and auditory abilities, insects possess an exceptional range of sensory skills that allow them to detect, locate, and respond to the world around them. Recent research has uncovered fascinating examples of these abilities, such as the newly discovered capability of cockroaches [1] and flies [2] to detect the spatial distribution of odors. Moreover, insects like fruit flies, honeybees, and crickets exhibit extraordinary learning and memory capabilities that enable them to adapt to ever-changing environments. By studying the neural network mechanisms of learning and memory in fruit flies, we can gain invaluable insights into how these systems work at the single-neuron level 3, 4. Additionally, insect studies can provide crucial information on the adaptive significance of learning and memory [5], which is a vital area of research in ecology and evolutionary biology. In this section, we will delve into the latest breakthroughs in studying olfactory perceptions, learning, and memory in insects.
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Nutrient responding peptide hormone CCHamide-2 consolidates appetitive memory
Yamagata N, Imanishi Y, Wu H, Kondo S, Sano H, Tanimoto H.
Frontiers in Behavioral Neuroscience ( Frontiers in Behavioral Neuroscience ) 16 986064 - 986064 2022年10月 [査読有り]
研究論文（学術雑誌） 国内共著
CCHamide-2 (CCHa2) is a protostome excitatory peptide ortholog known for various arthropod species. In fruit flies, CCHa2 plays a crucial role in the endocrine system, allowing peripheral tissue to communicate with the central nervous system to ensure proper development and the maintenance of energy homeostasis. Since the formation of odor-sugar associative long-term memory (LTM) depends on the nutrient status in an animal, CCHa2 may play an essential role in linking memory and metabolic systems. Here we show that CCHa2 signals are important for consolidating appetitive memory by acting on the rewarding dopamine neurons. Genetic disruption of CCHa2 using mutant strains abolished appetitive LTM but not short-term memory (STM). A post-learning thermal suppression of CCHa2 expressing cells impaired LTM. In contrast, a post-learning thermal activation of CCHa2 cells stabilized STM induced by non-nutritious sugar into LTM. The receptor of CCHa2, CCHa2-R, was expressed in a subset of dopamine neurons that mediate reward for LTM. In accordance, the receptor expression in these dopamine neurons was required for LTM specifically. We thus concluded that CCHa2 conveys a sugar nutrient signal to the dopamine neurons for memory consolidation. Our finding establishes a direct interplay between brain reward and the putative endocrine system for long-term energy homeostasis.
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Presynaptic inhibition of dopamine neurons controls optimistic bias
Yamagata N, Ezaki T, Takahashi T, Wu H, Tanimoto H.
eLife ( eLife ) 10 2021年06月 [査読有り]
研究論文（学術雑誌） 国内共著
Regulation of reward signaling in the brain is critical for appropriate judgement of the environment and self. In <italic>Drosophila</italic>, the protocerebral anterior medial (PAM) cluster dopamine neurons mediate reward signals. Here, we show that localized inhibitory input to the presynaptic terminals of the PAM neurons titrates olfactory reward memory and controls memory specificity. The inhibitory regulation was mediated by metabotropic gamma-aminobutyric acid (GABA) receptors clustered in presynaptic microdomain of the PAM boutons. Cell type-specific silencing the GABA receptors enhanced memory by augmenting internal reward signals. Strikingly, the disruption of GABA signaling reduced memory specificity to the rewarded odor by changing local odor representations in the presynaptic terminals of the PAM neurons. The inhibitory microcircuit of the dopamine neurons is thus crucial for both reward values and memory specificity. Maladaptive presynaptic regulation causes optimistic cognitive bias.
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Mushroom body output differentiates memory processes and distinct memory-guided behaviors
Ichinose T, Kanno M, Wu H, Yamagata N, Sun H, Abe A, Tanimoto H.
Current Biology ( Current Biology ) 31 ( 6 ) 1294 - 1302.e4 2021年03月 [査読有り]
研究論文（学術雑誌） 国内共著
The mushroom body (MB) of Drosophila melanogaster has multiple functions in controlling memory and behavior.1-9 However, circuit mechanisms that generate this functional diversity are largely unclear. Here, we systematically probed the behavioral contribution of each type of MB output neuron (MBON) by blocking during acquisition, retention, or retrieval of reward or punishment memories. We evaluated the contribution using two conditioned responses: memory-guided odor choice and odor source attraction. Quantitative analysis revealed that these conditioned odor responses are controlled by different sets of MBONs. We found that the valence of memory, rather than the transition of memory steps, has a larger impact on the patterns of required MBONs. Moreover, we found that the glutamatergic MBONs forming recurrent circuits commonly contribute to appetitive memory acquisition, suggesting a pivotal role of this circuit motif for reward processing. Our results provide principles how the MB output circuit processes associative memories of different valence and controls distinct memory-guided behaviors.
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Kondo S, Takahashi T, Yamagata N, Imanishi Y, Katow H, Hiramatsu S, Lynn K, Abe A, Kumaraswamy A, Tanimoto H.
Cell Reports ( Cell Reports ) 30 ( 1 ) 284 - 297.e5 2020年01月 [査読有り]
研究論文（学術雑誌） 国際共著
Neurotransmitters often have multiple receptors that induce distinct responses in receiving cells. Expression and localization of neurotransmitter receptors in individual neurons are therefore critical for understanding the operation of neural circuits. Here we describe a comprehensive library of reporter strains in which a convertible T2A-GAL4 cassette is inserted into endogenous neurotransmitter receptor genes of Drosophila. Using this library, we profile the expression of 75 neurotransmitter receptors in the brain. Cluster analysis reveals neurochemical segmentation of the brain, distinguishing higher brain centers from the rest. By recombinase-mediated cassette exchange, we convert T2A-GAL4 into split-GFP and Tango to visualize subcellular localization and activation of dopamine receptors in specific cell types. This reveals striking differences in their subcellular localization, which may underlie the distinct cellular responses to dopamine in different behavioral contexts. Our resources thus provide a versatile toolkit for dissecting the cellular organization and function of neurotransmitter systems in the fly brain.
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Courtship behavior induced by appetitive olfactory memory
Onodera Y, Ichikawa R, Terao K, Tanimoto H, Yamagata N.
Journal of Neurogenetics ( Journal of Neurogenetics ) 33 ( 2 ) 143 - 151 2019年04月 [査読有り]
研究論文（学術雑誌） 国内共著
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Haenicke J, Yamagata N, Zwaka H, Nawrot M, Menzel R.
eNeuro ( eNeuro ) 5 ( 3 ) 2018年05月 [査読有り]
研究論文（学術雑誌） 国際共著
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Behavioral modulation by spontaneous activity of dopamine neurons
Ichinose T, Tanimoto H, Yamagata N.
Frontiers in Systems Neuroscience ( Frontiers in Systems Neuroscience ) 11 88 - 88 2017年12月 [査読有り]
研究論文（学術雑誌） 国内共著
Dopamine modulates a variety of animal behaviors that range from sleep and learning to courtship and aggression. Besides its well-known phasic firing to natural reward, a substantial number of dopamine neurons (DANs) are known to exhibit ongoing intrinsic activity in the absence of an external stimulus. While accumulating evidence points at functional implications for these intrinsic "spontaneous activities" of DANs in cognitive processes, a causal link to behavior and its underlying mechanisms has yet to be elucidated. Recent physiological studies in the model organism Drosophila melanogaster have uncovered that DANs in the fly brain are also spontaneously active, and that this activity reflects the behavioral/internal states of the animal. Strikingly, genetic manipulation of basal DAN activity resulted in behavioral alterations in the fly, providing critical evidence that links spontaneous DAN activity to behavioral states. Furthermore, circuit-level analyses have started to reveal cellular and molecular mechanisms that mediate or regulate spontaneous DAN activity. Through reviewing recent findings in different animals with the major focus on flies, we will discuss potential roles of this physiological phenomenon in directing animal behaviors.
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市之瀬 敏晴, 山方 恒宏
比較生理生化学 ( 日本比較生理生化学会 ) 34 ( 4 ) 108 - 115 2017年 [査読有り] [招待有り]
研究論文（学術雑誌） 国内共著
<p>ドーパミンは睡眠，学習や求愛行動など，動物のさまざまな行動を制御する。中脳ドーパミンニューロンは，報酬刺激に対する一過的なバースト発火を生理学的特徴とするが，その多くは，外界からの刺激がない状態でも内因的な神経活動を示すことが知られている。先行研究により，このドーパミンニューロンの「自発活動」は，学習などの脳機能に重要な役割を果たすことが分かってきた。しかし，行動との因果関係やその作用メカニズムについては，未だ不明な点が多い。近年，モデル生物であるキイロショウジョウバエ<i>Drosophila melanogaster</i>の脳内においてもドーパミンニューロンが自発的な活動を示すことが分かってきた。最新の生理学的手法，および遺伝学的アプローチにより，ショウジョウバエの行動および内的状態がこの自発活動に反映されており，その変化は個体レベルの行動に直接的に影響することが明らかとなりつつある。さらに自発活動の制御に関わる分子やドーパミンニューロンの局所回路も同定されつつある。本総説では，ショウジョウバエを中心とした最新の知見をまとめ，ドーパミンニューロンの自発活動が動物の行動制御において果たす意義について考察したい。</p>
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Suppression of Dopamine Neurons Mediates Reward.
Yamagata, Nobuhiro Hiroi, Makoto Kondo, Shu Abe, Ayako Tanimoto, Hiromu
PLoS Biol ( PLoS Biology ) 14 ( 12 ) e1002586 - e1002586 2016年12月 [査読有り]
研究論文（学術雑誌） 国内共著
Massive activation of dopamine neurons is critical for natural reward and drug abuse. In contrast, the significance of their spontaneous activity remains elusive. In Drosophila melanogaster, depolarization of the protocerebral anterior medial (PAM) cluster dopamine neurons en masse signals reward to the mushroom body (MB) and drives appetitive memory. Focusing on the functional heterogeneity of PAM cluster neurons, we identified that a single class of PAM neurons, PAM-γ3, mediates sugar reward by suppressing their own activity. PAM-γ3 is selectively required for appetitive olfactory learning, while activation of these neurons in turn induces aversive memory. Ongoing activity of PAM-γ3 gets suppressed upon sugar ingestion. Strikingly, transient inactivation of basal PAM-γ3 activity can substitute for reward and induces appetitive memory. Furthermore, we identified the satiety-signaling neuropeptide Allatostatin A (AstA) as a key mediator that conveys inhibitory input onto PAM-γ3. Our results suggest the significance of basal dopamine release in reward signaling and reveal a circuit mechanism for negative regulation.
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Four Individually Identified Paired Dopamine Neurons Signal Reward in Larval Drosophila.
Rohwedder, Astrid Wenz, Nana L Stehle, Bernhard Huser, Annina Yamagata, Nobuhiro Zlatic, Marta Truman, James W Tanimoto, Hiromu Saumweber, Timo Gerber, Bertram Thum, Andreas S
Curr Biol ( Current Biology ) 26 ( 5 ) 661 - 9 2016年03月 [査読有り]
研究論文（学術雑誌）
Dopaminergic neurons serve multiple functions, including reinforcement processing during associative learning [1-12]. It is thus warranted to understand which dopaminergic neurons mediate which function. We study larval Drosophila, in which only approximately 120 of a total of 10,000 neurons are dopaminergic, as judged by the expression of tyrosine hydroxylase (TH), the rate-limiting enzyme of dopamine biosynthesis [5, 13]. Dopaminergic neurons mediating reinforcement in insect olfactory learning target the mushroom bodies, a higher-order "cortical" brain region [1-5, 11, 12, 14, 15]. We discover four previously undescribed paired neurons, the primary protocerebral anterior medial (pPAM) neurons. These neurons are TH positive and subdivide the medial lobe of the mushroom body into four distinct subunits. These pPAM neurons are acutely necessary for odor-sugar reward learning and require intact TH function in this process. However, they are dispensable for aversive learning and innate behavior toward the odors and sugars employed. Optogenetical activation of pPAM neurons is sufficient as a reward. Thus, the pPAM neurons convey a likely dopaminergic reward signal. In contrast, DL1 cluster neurons convey a corresponding punishment signal [5], suggesting a cellular division of labor to convey dopaminergic reward and punishment signals. On the level of individually identified neurons, this uncovers an organizational principle shared with adult Drosophila and mammals [1-4, 7, 9, 10] (but see [6]). The numerical simplicity and connectomic tractability of the larval nervous system [16-19] now offers a prospect for studying circuit principles of dopamine function at unprecedented resolution.
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Reward signal in a recurrent circuit drives appetitive long-term memory formation.
Ichinose, Toshiharu Aso, Yoshinori Yamagata, Nobuhiro Abe, Ayako Rubin, Gerald M Tanimoto, Hiromu
Elife ( eLife ) 4 ( NOVEMBER2015 ) e10719 - e10719 2015年11月 [査読有り]
研究論文（学術雑誌）
Dopamine signals reward in animal brains. A single presentation of a sugar reward to Drosophila activates distinct subsets of dopamine neurons that independently induce short- and long-term olfactory memories (STM and LTM, respectively). In this study, we show that a recurrent reward circuit underlies the formation and consolidation of LTM. This feedback circuit is composed of a single class of reward-signaling dopamine neurons (PAM-α1) projecting to a restricted region of the mushroom body (MB), and a specific MB output cell type, MBON-α1, whose dendrites arborize that same MB compartment. Both MBON-α1 and PAM-α1 neurons are required during the acquisition and consolidation of appetitive LTM. MBON-α1 additionally mediates the retrieval of LTM, which is dependent on the dopamine receptor signaling in the MB α/β neurons. Our results suggest that a reward signal transforms a nascent memory trace into a stable LTM using a feedback circuit at the cost of memory specificity.
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Distinct dopamine neurons mediate reward signals for short- and long-term memories.
Yamagata, Nobuhiro Ichinose, Toshiharu Aso, Yoshinori Placais, Pierre-Yves Friedrich, Anja B Sima, Richard J Preat, Thomas Rubin, Gerald M Tanimoto, Hiromu
Proc Natl Acad Sci U S A ( Proceedings of the National Academy of Sciences of the United States of America ) 112 ( 2 ) 578 - 83 2015年01月 [査読有り]
研究論文（学術雑誌）
Drosophila melanogaster can acquire a stable appetitive olfactory memory when the presentation of a sugar reward and an odor are paired. However, the neuronal mechanisms by which a single training induces long-term memory are poorly understood. Here we show that two distinct subsets of dopamine neurons in the fly brain signal reward for short-term (STM) and long-term memories (LTM). One subset induces memory that decays within several hours, whereas the other induces memory that gradually develops after training. They convey reward signals to spatially segregated synaptic domains of the mushroom body (MB), a potential site for convergence. Furthermore, we identified a single type of dopamine neuron that conveys the reward signal to restricted subdomains of the mushroom body lobes and induces long-term memory. Constant appetitive memory retention after a single training session thus comprises two memory components triggered by distinct dopamine neurons.
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Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila.
Aso, Yoshinori Sitaraman, Divya Ichinose, Toshiharu Kaun, Karla R Vogt, Katrin Belliart-Guerin, Ghislain Placais, Pierre-Yves Robie, Alice A Yamagata, Nobuhiro Schnaitmann, Christopher Rowell, William J Johnston, Rebecca M Ngo, Teri-T B Chen, Nan Korff, Wyatt Nitabach, Michael N Heberlein, Ulrike Preat, Thomas Branson, Kristin M Tanimoto, Hiromu Rubin, Gerald M
Elife ( eLife ) 3 e04580 - e04580 2014年12月 [査読有り]
研究論文（学術雑誌）
Animals discriminate stimuli, learn their predictive value and use this knowledge to modify their behavior. In Drosophila, the mushroom body (MB) plays a key role in these processes. Sensory stimuli are sparsely represented by ∼2000 Kenyon cells, which converge onto 34 output neurons (MBONs) of 21 types. We studied the role of MBONs in several associative learning tasks and in sleep regulation, revealing the extent to which information flow is segregated into distinct channels and suggesting possible roles for the multi-layered MBON network. We also show that optogenetic activation of MBONs can, depending on cell type, induce repulsion or attraction in flies. The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence. We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli. Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.
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Converging circuits mediate temperature and shock aversive olfactory conditioning in Drosophila.
Galili, Dana, Shani Dylla, Kristina V Ludke, Alja Friedrich, Anja B Yamagata, Nobuhiro Wong, Jin Yan, Hilary Ho, Chien Hsien Szyszka, Paul Tanimoto, Hiromu
Curr Biol ( Current Biology ) 24 ( 15 ) 1712 - 22 2014年08月 [査読有り]
研究論文（学術雑誌）
BACKGROUND: Drosophila learn to avoid odors that are paired with aversive stimuli. Electric shock is a potent aversive stimulus that acts via dopamine neurons to elicit avoidance of the associated odor. While dopamine signaling has been demonstrated to mediate olfactory electric shock conditioning, it remains unclear how this pathway is involved in other types of behavioral reinforcement, such as in learned avoidance of odors paired with increased temperature. RESULTS: To better understand the neural mechanisms of distinct aversive reinforcement signals, we here established an olfactory temperature conditioning assay comparable to olfactory electric shock conditioning. We show that the AC neurons, which are internal thermal receptors expressing dTrpA1, are selectively required for odor-temperature but not for odor-shock memory. Furthermore, these separate sensory pathways for increased temperature and shock converge onto overlapping populations of dopamine neurons that signal aversive reinforcement. Temperature conditioning appears to require a subset of the dopamine neurons required for electric shock conditioning. CONCLUSIONS: We conclude that dopamine neurons integrate different noxious signals into a general aversive reinforcement pathway.
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A subset of dopamine neurons signals reward for odour memory in Drosophila.
Liu, Chang Placais, Pierre-Yves Yamagata, Nobuhiro Pfeiffer, Barret D Aso, Yoshinori Friedrich, Anja B Siwanowicz, Igor Rubin, Gerald M Preat, Thomas Tanimoto, Hiromu
Nature ( Nature ) 488 ( 7412 ) 512 - 6 2012年08月 [査読有り]
研究論文（学術雑誌）
Animals approach stimuli that predict a pleasant outcome. After the paired presentation of an odour and a reward, Drosophila melanogaster can develop a conditioned approach towards that odour. Despite recent advances in understanding the neural circuits for associative memory and appetitive motivation, the cellular mechanisms for reward processing in the fly brain are unknown. Here we show that a group of dopamine neurons in the protocerebral anterior medial (PAM) cluster signals sugar reward by transient activation and inactivation of target neurons in intact behaving flies. These dopamine neurons are selectively required for the reinforcing property of, but not a reflexive response to, the sugar stimulus. In vivo calcium imaging revealed that these neurons are activated by sugar ingestion and the activation is increased on starvation. The output sites of the PAM neurons are mainly localized to the medial lobes of the mushroom bodies (MBs), where appetitive olfactory associative memory is formed. We therefore propose that the PAM cluster neurons endow a positive predictive value to the odour in the MBs. Dopamine in insects is known to mediate aversive reinforcement signals. Our results highlight the cellular specificity underlying the various roles of dopamine and the importance of spatially segregated local circuits within the MBs.
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Neural organization and visual processing in the anterior optic tubercle of the honeybee brain.
Mota, Theo Yamagata, Nobuhiro Giurfa, Martin Gronenberg, Wulfila Sandoz, Jean-Christophe
J Neurosci ( Journal of Neuroscience ) 31 ( 32 ) 11443 - 56 2011年08月 [査読有り]
研究論文（学術雑誌）
The honeybee Apis mellifera represents a valuable model for studying the neural segregation and integration of visual information. Vision in honeybees has been extensively studied at the behavioral level and, to a lesser degree, at the physiological level using intracellular electrophysiological recordings of single neurons. However, our knowledge of visual processing in honeybees is still limited by the lack of functional studies of visual processing at the circuit level. Here we contribute to filling this gap by providing a neuroanatomical and neurophysiological characterization at the circuit level of a practically unstudied visual area of the bee brain, the anterior optic tubercle (AOTu). First, we analyzed the internal organization and neuronal connections of the AOTu. Second, we established a novel protocol for performing optophysiological recordings of visual circuit activity in the honeybee brain and studied the responses of AOTu interneurons during stimulation of distinct eye regions. Our neuroanatomical data show an intricate compartmentalization and connectivity of the AOTu, revealing a dorsoventral segregation of the visual input to the AOTu. Light stimuli presented in different parts of the visual field (dorsal, lateral, or ventral) induce distinct patterns of activation in AOTu output interneurons, retaining to some extent the dorsoventral input segregation revealed by our neuroanatomical data. In particular, activity patterns evoked by dorsal and ventral eye stimulation are clearly segregated into distinct AOTu subunits. Our results therefore suggest an involvement of the AOTu in the processing of dorsoventrally segregated visual information in the honeybee brain.
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Schmuker, Michael Yamagata, Nobuhiro Nawrot, Martin Paul Menzel, Randolf
Front Neuroeng ( Frontiers in Neuroengineering ) 4 ( DECEMBER ) 17 - 17 2011年 [査読有り]
研究論文（学術雑誌）
The honeybee Apis mellifera has a remarkable ability to detect and locate food sources during foraging, and to associate odor cues with food rewards. In the honeybee's olfactory system, sensory input is first processed in the antennal lobe (AL) network. Uniglomerular projection neurons (PNs) convey the sensory code from the AL to higher brain regions via two parallel but anatomically distinct pathways, the lateral and the medial antenno-cerebral tract (l- and m-ACT). Neurons innervating either tract show characteristic differences in odor selectivity, concentration dependence, and representation of mixtures. It is still unknown how this differential stimulus representation is achieved within the AL network. In this contribution, we use a computational network model to demonstrate that the experimentally observed features of odor coding in PNs can be reproduced by varying lateral inhibition and gain control in an otherwise unchanged AL network. We show that odor coding in the l-ACT supports detection and accurate identification of weak odor traces at the expense of concentration sensitivity, while odor coding in the m-ACT provides the basis for the computation and following of concentration gradients but provides weaker discrimination power. Both coding strategies are mutually exclusive, which creates a tradeoff between detection accuracy and sensitivity. The development of two parallel systems may thus reflect an evolutionary solution to this problem that enables honeybees to achieve both tasks during bee foraging in their natural environment, and which could inspire the development of artificial chemosensory devices for odor-guided navigation in robots.
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Yamagata, Nobuhiro Mizunami, Makoto
Proc Biol Sci ( Proceedings of the Royal Society B: Biological Sciences ) 277 ( 1693 ) 2465 - 74 2010年08月 [査読有り]
研究論文（学術雑誌）
Pheromones play major roles in intraspecific communication in many animals. Elaborated communication systems in eusocial insects provide excellent materials to study neural mechanisms for social pheromone processing. We previously reported that alarm pheromone information is processed in a specific cluster of glomeruli in the antennal lobe of the ant Camponotus obscuripes. However, representation of alarm pheromone information in a secondary olfactory centre is unknown in any animal. Olfactory information in the antennal lobe is transmitted to secondary olfactory centres, including the lateral horn, by projection neurons (PNs). In this study, we compared distributions of terminal boutons of alarm pheromone-sensitive and -insensitive PNs in the lateral horn of ants. Distributions of their dendrites largely overlapped, but there was a region where boutons of pheromone-sensitive PNs, but not those of pheromone-insensitive PNs, were significantly denser than in the rest of the lateral horn. Moreover, most of a major type of pheromone-sensitive efferent neurons from the lateral horn extended dendritic branches in this region, suggesting specialization of this region for alarm pheromone processing. This study is the first study to demonstrate the presence of specialized areas for the processing of a non-sexual, social pheromone in the secondary olfactory centre in any animal.
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Alarm pheromone processing in the ant brain: an evolutionary perspective.
Mizunami, Makoto Yamagata, Nobuhiro Nishino, Hiroshi
Front Behav Neurosci ( Frontiers in Behavioral Neuroscience ) 4 ( JUN ) 28 - 28 2010年 [査読有り]
研究論文（学術雑誌）
Social insects exhibit sophisticated communication by means of pheromones, one example of which is the use of alarm pheromones to alert nestmates for colony defense. We review recent advances in the understanding of the processing of alarm pheromone information in the ant brain. We found that information about formic acid and n-undecane, alarm pheromone components, is processed in a set of specific glomeruli in the antennal lobe of the ant Camponotus obscuripes. Alarm pheromone information is then transmitted, via projection neurons (PNs), to the lateral horn and the calyces of the mushroom body of the protocerebrum. In the lateral horn, we found a specific area where terminal boutons of alarm pheromone-sensitive PNs are more densely distributed than in the rest of the lateral horn. Some neurons in the protocerebrum responded specifically to formic acid or n-undecane and they may participate in the control of behavioral responses to each pheromone component. Other neurons, especially those originating from the mushroom body lobe, responded also to non-pheromonal odors and may play roles in integration of pheromonal and non-pheromonal signals. We found that a class of neurons receive inputs in the lateral horn and the mushroom body lobe and terminate in a variety of premotor areas. These neurons may participate in the control of aggressive behavior, which is sensitized by alarm pheromones and is triggered by non-pheromonal sensory stimuli associated with a potential enemy. We propose that the alarm pheromone processing system has evolved by differentiation of a part of general odor processing system.
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Differential odor processing in two olfactory pathways in the honeybee.
Yamagata, Nobuhiro Schmuker, Michael Szyszka, Paul Mizunami, Makoto Menzel, Randolf
Front Syst Neurosci ( Frontiers in Systems Neuroscience ) 3 ( DEC ) 16 - 16 2009年 [査読有り]
研究論文（学術雑誌）
An important component in understanding central olfactory processing and coding in the insect brain relates to the characterization of the functional divisions between morphologically distinct types of projection neurons (PN). Using calcium imaging, we investigated how the identity, concentration and mixtures of odors are represented in axon terminals (boutons) of two types of PNs - lPN and mPN. In lPN boutons we found less concentration dependence, narrow tuning profiles at a high concentration, which may be optimized for fine, concentration-invariant odor discrimination. In mPN boutons, however, we found clear rising concentration dependence, broader tuning profiles at a high concentration, which may be optimized for concentration coding. In addition, we found more mixture suppression in lPNs than in mPNs, indicating lPNs better adaptation for synthetic mixture processing. These results suggest a functional division of odor processing in both PN types.
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Neural pathways for the processing of alarm pheromone in the ant brain.
Yamagata, Nobuhiro Nishino, Hiroshi Mizunami, Makoto
J Comp Neurol ( Journal of Comparative Neurology ) 505 ( 4 ) 424 - 42 2007年12月 [査読有り]
研究論文（学術雑誌）
Social insects like ants exhibit sophisticated communication by means of pheromones, one example of which is the use of alarm pheromones to alert nestmates for colony defense. In the ant Camponotus obscuripes, we have reported that information about formic acid and n-undecane, alarm pheromone components, is processed in a set of specific glomeruli in the antennal lobe (primary olfactory center). Alarm pheromone signals are then transmitted, mainly via uniglomerular projection neurons (uni-PNs), to the protocerebrum (PR), where sensory signals are integrated to form motor commands for behavioral responses. In this study, we physiologically and morphologically characterized 63 alarm pheromone-sensitive PR neurons in ants by using intracellular recording and staining techniques. Most of the pheromone-sensitive PR neurons had dendrites in the mushroom body (MB), the lateral horn, or the medial PR. Some neurons with dendrites in these areas responded specifically to formic acid or n-undecane and may participate in the control of specific behavioral responses to each pheromone component. Other neurons responded also to non-pheromonal odors, in contrast to uni-PNs, most of which responded specifically to alarm pheromones. Responses to non-pheromonal odors were most prominent in efferent neurons of the MB lobe, suggesting that they may participate in integration of pheromonal and non-pheromonal information. We found a class of PR neurons that receives input in all of these pheromone-processing areas and terminates in a variety of premotor areas. These neurons may participate in the control of pheromone-sensitized aggressive behavior, which is triggered by non-pheromonal sensory stimuli associated with a potential enemy.
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Pheromone-sensitive glomeruli in the primary olfactory centre of ants.
Yamagata, Nobuhiro Nishino, Hiroshi Mizunami, Makoto
Proc Biol Sci ( Proceedings of the Royal Society B: Biological Sciences ) 273 ( 1598 ) 2219 - 25 2006年09月 [査読有り]
研究論文（学術雑誌）
Tremendous evolutional success and the ecological dominance of social insects, including ants, termites and social bees, are due to their efficient social organizations and their underlying communication systems. Functional division into reproductive and sterile castes, cooperation in defending the nest, rearing the young and gathering food are all regulated by communication by means of various kinds of pheromones. No brain structures specifically involved in the processing of non-sexual pheromone have been physiologically identified in any social insects. By use of intracellular recording and staining techniques, we studied responses of projection neurons of the antennal lobe (primary olfactory centre) of ants to alarm pheromone, which plays predominant roles in colony defence. Among 23 alarm pheromone-sensitive projection neurons recorded and stained in this study, eight were uniglomerular projection neurons with dendrites in one glomerulus, a structural unit of the antennal lobe, and the remaining 15 were multiglomerular projection neurons with dendrites in multiple glomeruli. Notably, all alarm pheromone-sensitive uniglomerular projection neurons had dendrites in one of five 'alarm pheromone-sensitive (AS)' glomeruli that form a cluster in the dorsalmost part of the antennal lobe. All alarm pheromone-sensitive multiglomerular projection neurons had dendrites in some of the AS glomeruli as well as in glomeruli in the anterodorsal area of the antennal lobe. The results suggest that components of alarm pheromone are processed in a specific cluster of glomeruli in the antennal lobe of ants.
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Fujiwara-Tsujii, Nao Yamagata, Nobuhiro Takeda, Takeshi Mizunami, Makoto Yamaoka, Ryohei
Zoolog Sci ( Zoological Science ) 23 ( 4 ) 353 - 8 2006年04月 [査読有り]
研究論文（学術雑誌）
The alarm pheromone of the ant Camponotus obscuripes (Formicinae) was identified and quantified by gas chromatography (GC) and gas chromatography-mass spectrometry (GC-MS). Comparisons between alarm pheromone components and extracts from the major exocrine gland of this ant species revealed that the sources of its alarm pheromone are Dufour's gland and the poison gland. Most components of Dufour's gland were saturated hydrocarbons. n-Undecane comprised more than 90% of all components and in a single Dufour's gland amounted to 19 microg. n-Decane and n-pentadecane were also included in the Dufour's gland secretion. Only formic acid was detected in the poison gland, in amounts ranging from 0.049 to 0.91 microl. This ant species releases a mixture of these substances, each of which has a different volatility and function. When the ants sensed formic acid, they eluded the source of the odor; however, they aggressively approached odors of n-undecane and n-decane, which are highly volatile. In contrast, n-pentadecane, which has the lowest volatility among the identified compounds, was shown to calm the ants. The volatilities of the alarm pheromone components were closely related to their roles in alarm communication. Highly volatile components vaporized rapidly and spread widely, and induced drastic reactions among the ants. As these components became diluted, the less volatile components calmed the excited ants. How the worker ants utilize this alarm communication system for efficient deployment of their nestmates in colony defense is also discussed herein.
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Yamagata, Nobuhiro Fujiwara-Tsujii, Nao Yamaoka, Ryohei Mizunami, Makoto
Naturwissenschaften ( Naturwissenschaften ) 92 ( 11 ) 532 - 6 2005年11月 [査読有り]
研究論文（学術雑誌）
Communication by means of pheromones plays predominant roles in colony integration by social insects. However, almost nothing is known about pheromone processing in the brains of social insects. In this study, we successfully applied intracellular recording and staining techniques to anatomically and physiologically characterize brain neurons of the ant Camponotus obscuripes. We identified 42 protocerebral neurons that responded to undecane and/or formic acid, components of alarm pheromones that evoke attraction or evasive behavior, respectively. Notably, 30 (71%) of these neurons were efferent (output) or feedback neurons of the mushroom body, and many of these exhibited different responses to formic acid and undecane. Eight of the remaining 12 neurons had arborizations in the lateral and/or medial protocerebrum, which receive terminations of efferent neurons of the mushroom body and from which premotor descending neurons originate. The remaining four neurons were bilateral neurons that connect lateral accessory lobes or dorsal protocerebrums of both hemispheres. We suggest that the mushroom body of the ant participates in the processing of alarm pheromones. Seventeen (40%) of 42 neurons exhibited responses to nonpheromonal odors, indicating that the pheromonal and nonpheromonal signals are not fully segregated when they are processed in the protocerebrum. This may be related to modulatory functions of alarm pheromones, i.e., they change alertness of the ant and change responses to a variety of sensory stimuli.