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  4. Takaki Komiyama

Takaki Komiyama

Research

Animals constantly modify their behavior through experience. Flexible behavior is key to our ability to adapt to the ever-changing environment. My laboratory is interested in studying the activity of neuronal ensembles in behaving animals, and how it changes with learning.

We have recently set up a paradigm where mice learn to associate sensory information (two different odors) to motor outputs (lick vs no-lick) under head-fixation. We combined this with two-photon calcium imaging, which can monitor the activity of a microcircuit of many tens of neurons simultaneously from a small area of the brain. Imaging the motor cortex during the learning of this task revealed neurons with diverse task-related response types. Intriguingly, different response types were spatially intermingled; even immediately adjacent neurons often had very different response types. As the mouse learned the task under the microscope, the activity coupling of neurons with similar response types specifically increased, even though they are intermingled with neurons with dissimilar response types. This suggests that intermingled subnetworks of functionally-related neurons form in a learning-related way, an observation that became possible with our cutting-edge technique combining imaging and behavior.

We are working to extend this study. How plastic are neuronal microcircuits during other forms of learning? How plastic are they in other parts of the brain? What are the cellular and molecular mechanisms of the microcircuit plasticity? Are the observed activity and plasticity required for learning? How does the activity of identified individual neurons change over days to weeks? We are asking these questions, combining a variety of techniques including in vivo two-photon imaging, optogenetics, electrophysiology, genetics and behavior.

Figure 1: Activity of cortical axons visualized by two-photon calcium imaging in a task-performing mouse

Figure 2: Activity of a cortical neuronal population visualized by two-photon calcium imaging in a task-performing mouse

Select Publications

  • Hattori, R. and Komiyama, T. “PatchWarp: Corrections of non-uniform image distortions in two-photon calcium imaging data by patchwork affine transformations” Preprint at https://www.biorxiv.org/content/10.1101/2021.11.10.468164v1
  • Hattori, R. and Komiyama, T. (2022) “Context-dependent persistency as a coding mechanism for robust and widely distributed value coding.” Neuron, in press.
  • Ren, C. and Komiyama, T. (2021) “Wide-field calcium imaging of cortex-wide activity in awake, head-fixed mice.” STAR Protocols, 2 (4), 100973.
  • Meamardoost, S., Bhattacharya, M., Hwang, E.J., Komiyama, T., Mewes, C., Wang, L., Zhang, Y., Gunawan, R. (2021) “FARCI: Fast and Robust Connectome Inference.” Brain Sciences, 11(12), 1556. Preprint at https://www.biorxiv.org/content/10.1101/2020.10.07.330175v1
  • Liu, X.*, Ren, C.*, Huang, Z., Wilson, M., Kim, J-H., Lu, Y., Ramezani, M., Komiyama, T., and Kuzum, D. (2021) “Decoding of cortex-wide brain activity from local recordings of neural potentials.” Journal of Neural Engineering, 18(6), 066009. Preprint at https://www.biorxiv.org/content/10.1101/2021.10.14.464468v1
  • Hwang, E.J.*, Dahlen, J.E.*, Mukundan, M., and Komiyama, T. (2021) “Disengagement of motor cortex during long-term learning tracks the performance level of learned movements.” Journal of Neuroscience, 41(33), 7029-7047.
  • Ren, C. and Komiyama, T. (2021) “Characterizing cortex-wide dynamics with wide-field calcium imaging.” (Review) Journal of Neuroscience, 41(19), 4160-4168.
  • Liu, X.*, Ren, C.*, Lu, Y.*, Liu, Y., Leutgeb, S., Komiyama, T.#, and Kuzum, D.# (#: co-correspondence) (2021) “Multimodal neural recordings with Neuro-FITM uncover diverse patterns of cortical-hippocampal interactions.” Nature Neuroscience (cover article), 24, 886–896
  • Bathe, M.*, Hernandez, R.*, Komiyama, T.*, Machiraju, R.*, and Neogi S.* (*: co-first authors) (2021) “Autonomous Computing Materials.” (Perspective) ACS Nano, 15, 3, 3586–3592.
  • Wu, A.*, Yu, B.*, Chen, Q., Matthews, G.A., Lu, C., Campbell, E., Tye, K.M., and Komiyama, T. (2020) “Context-dependent plasticity of adult-born neurons instructed by cortical feedback.” Science Advances, 6(42), eabc8319.
  • Ma, Z., Liu, H., Komiyama, T., and Wessel, R. (2020) “Stability of layer-specific motor cortex network states during learning-associated neural reorganizations.” Journal of Neurophysiology, 124(5), 1327-42.
  • Ding, D., Lu, Y., Zhao, R., Liu, X., De-Eknamkul, C., Ren, C., Mehrsa, A., Komiyama, T., and Kuzum, D. (2020) “Evaluation of Durability of Transparent Graphene Electrodes Fabricated on Different Flexible Substrates for Chronic in vivo Experiments.” IEEE Transactions on Biomedical Engineering, 67(11): 3203-10.
  • Wu, A.*, Yu, B.*, and Komiyama, T. (2020) “Plasticity in olfactory bulb circuits.” (Review) Current Opinion in Neurobiology, 64:17-23.
  • Hwang, E.J., Link, T., Hu, Y.Y., Lu, S., Wang, E.H., Lilascharoen, V., Aronson, S., O’Neil, K., Lim, B.K., and Komiyama, T. (2019) “Corticostriatal flow of action selection bias.” Neuron, 104(6): 1126-1140.
  • Hwang, E.J.*, Dahlen, J.E.*, Hu, Y.Y., Aguilar, K., Yu, B., Mukundan, M., Mitani, A. and Komiyama, T. (2019) “Disengagement of motor cortex from movement control during long-term learning.” Science Advances, 5(10): eaay0001.
  • Hattori, R., Danskin, B., Babic, Z., Mlynaryk, N., and Komiyama, T. (2019) “Area-specificity and plasticity of value coding during learning.” Cell, 177(7):1858-1872.
  • Liu, X., Ren, C., Lu, Y., Hattori, R., Shi, Y., Zhao, R., Ding, D., Komiyama, T., and Kuzum, D. (2019) “Decoding ECoG high gamma power from cellular calcium response using transparent graphene microelectrodes.” IEEE International EMBS Conference On Neural Engineering (NER’19).
  • Zhao, R., Liu, X., Lu, Y., Ren, C., Mehrsa, A., Komiyama, T. and Kuzum, D. (2018) “3D expandable microwire electrode arrays made of programmable shape memory materials.” IEEE International Electron Devices Meeting (IEDM).
  • Mitani, A.# and Komiyama, T. (2018) “Real-time processing of two-photon calcium imaging data including lateral motion artifact correction.” Frontiers in Neuroinformatics, 12:98. doi: 10.3389/fninf.2018.00098.
  • Desjardins, M.*, Kılıç, K.*, Thunemann, M., Mateo, C., Holland, D., Ferri, C.G.L., Cremonesi, J.A., Li, B., Cheng, Q., Weldy, K.L., Saisan, P.A., Kleinfeld, D., Komiyama, T., Liu, T.T., Bussell, R., Wong, E.C., Scadeng, M., Dunn, A.K., Boas, D.A., Sakadžić, S., Mandeville, J.B., Buxton, R.B., Dale, A.M., and Devor, A. (2018) “Longitudinal awake mouse imaging: from two-photon microscopy to functional magnetic resonance imaging.” Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4 (6), 533-542.
  • Lu, Y., Liu, X., Hattori, R., Ren, C., Komiyama, T., and Kuzum, D. (2018) "Ultra-low Impedance Graphene Microelectrodes with High Optical Transparency for Simultaneous Deep 2-photon Imaging in Transgenic Mice." Advanced Functional Materials, 1800002. DOI: 10.1002/adfm.201800002.
  • Li, W.L., Chu, M., Wu, A., Suzuki, Y., Imayoshi, I., Komiyama, T. (2018) "Adult-born neurons facilitate olfactory bulb pattern separation during task engagement." eLife, 2018;7:e33006
  • Mitani, A., Dong, M. and Komiyama, T. (2018) "Brain-computer interface with inhibitory neurons reveals subtype-specific strategies." Current Biology, 28(1), 77-83.
  • Chu, M.W., Li, W.L. and Komiyama, T. (2017) “Lack of pattern separation in sensory inputs to the olfactory bulb during perceptual learning.” eNeuro*, *0287-17.201.
  • Hwang, E.J.*, Dahlen, J.E.*, Mukundan, M. and Komiyama, T. (2017) “History-dependent action selection bias in the posterior parietal cortex.” Nature Communications*,* 8, 1242.
  • Hattori, R.*, Kuchibhotla, K.*, Froemke, R.#, and Komiyama, T.#(2017) Functions and dysfunctions of neocortical inhibitory neuron subtypes. (Review) Nature Neuroscience , 20, 1199-1208.
  • Peters, A.J., Lee, J., Hedrick, N.G., O'Neil, K., and *Komiyama, T*. (2017) Reorganization of corticospinal output during motor learning. *Nature Neuroscience*, *20, 1133-41 - *Rated by Faculty of 1000**
  • Makino, H.*#, Ren, C.*, Liu, H.*, Kim, A.N., Kondapaneni, N., Liu, X., Kuzum, D. and *Komiyama, T.#*(2017) Transformation of cortex-wide emergent properties during motor learning. *Neuron*, 94(4), 880-90. - *Preview* by Banerjee and Long, *Neuron* 94(4), 698-700.
  • Peters, A.J., Liu, H. and *Komiyama, T.* (2017) Learning in the rodent motor cortex. (Review) *Annual Review of Neuroscience*, *40, 77-97.*
  • McIntyre, J.C., Thiebaud, N., McGann, J.P., *Komiyama, T.* and Rothermel, M. (2017) Neuromodulation in chemosensory systems. (Review) *Chemical Senses*, 42(5), 375-9.
  • Makino, H.*, Hwang, E.J.*, Hedrick, N.G.* and Komiyama, T. (2016) “Circuit mechanisms of sensorimotor learning.” (Review) Neuron, 92(4), 705-21.
  • Chu, M.W., Li, W.L. and Komiyama, T. (2016) “Balancing the robustness and efficiency of odor representations during learning.” Neuron, 92(1), 174-86.
  • Makino, H. and Komiyama, T. (2015) “Learning enhances the relative impact of top-down processing in the visual cortex.” Nature Neuroscience, 18(8), 1116-22.
  • Chen, S.X., Kim, A.N., Peters, A.J. and Komiyama, T. (2015) “Subtype-specific plasticity of inhibitory circuits during motor learning.” Nature Neuroscience, 18(8), 1109-15.
  • Boyd, A., Kato, H.K., Komiyama, T. and Isaacson, J.S. (2015) "Broadcasting of cortical activity to the olfactory bulb." Cell Reports, 10(7), 1032-9.
  • Peters, A.J., Chen, S.X. and Komiyama, T. (2014) Emergence of Reproducible Spatiotemporal Activity During Motor Learning. Nature, online.
  • Guo ZV, Hires SA, Li N, O'Connor DH, Komiyama T, Ophir E, Huber D, Bonardi C, Morandell K, Gutnisky D, Peron S, Xu NL, Cox J, Svoboda K. (2014) Procedures for behavioral experiments in head-fixed mice. PLoS One, 9(2):e88678.
  • Kato, H.K., Gillet, S.N, Peters, A.J., Isaacson, J.S. and Komiyama, T. (2013) Parvalbumin-Expressing Interneurons Linearly Control Olfactory Bulb Output. Neuron, 80(5), 1218-31.
  • Kato, H.K.*, Chu, M.W.*, Isaacson, J.S. and Komiyama, T. (2012) Dynamic Sensory Representations in the Olfactory Bulb: Modulation by Wakefulness and Experience. Neuron, 76(5), 962-975.
  • Sweeney LB, Chou YH, Wu Z, Joo W, Komiyama T, Potter CJ, Kolodkin AL, Garcia KC, Luo L. (2011) Secreted semaphorins from degenerating larval ORN axons direct adult projection neuron dendrite targeting. Neuron, 72(5), 734-47.
  • Komiyama, T.*, Sato, T.R., O'Connor, D.H., Zhang, Y.X., Huber, D., Hooks, B.M., Gabbito, M. and Svoboda, K. (2010) Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature, 464(7292), 1182-1186. (*: correspondence) Faculty of 1000 Article Factor: 15
  • O'Connor, D.H., Clack, N.G., Huber, D., Komiyama, T., Myers, E.W. and Svoboda, K. (2010) Vibrissa-based object localization in head-fixed mice. J. Neuroscience, 30, 1947-1967.
  • Komiyama, T. and Luo, L. (2007) Intrinsic control of precise dendritic targeting by an ensemble of transcription factors. Current Biology 17, 278-285.
  • Komiyama, T., Sweeney, L.B., Schuldiner, O., Garcia, K.C. and Luo, L. (2007) Graded expression of Semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128, 399-410.
  • Sweeney, L.B.*, Couto, A., Chou, Y-H., Berdnik, D., Dickson, B.J., Luo, L. and Komiyama, T.* (2007) Temporal target restriction of olfactory receptor neurons through Semaphorin-1a/PlexinA mediated axon-axon interactions. Neuron 53, 185-200. (*: equal contribution)
  • Komiyama, T. and Liqun Luo (2006) Development of wiring specificity of the olfactory system. Current Opinion in Neurobiology 16(1), 67-73.
  • Komiyama, T., Carlson, J.R. and Luo, L. (2004) Olfactory receptor neuron axon targeting: Intrinsic transcriptional control and hierarchical interactions. Nature Neuroscience 7, 819-825.
  • Komiyama, T.*, Johnson, W.A., Luo, L. and Jefferis, G.S.X.E.* (2003) From lineage to wiring specificity: POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell 112, 157-167. (*: equal contribution)

Biography

Dr. Komiyama was a Postdoc at Janelia Farm, Howard Hughes Medical Institute, received his Phd in Neurosciences at Stanford University (2006) and his BA in Biochemistry at University of Tokyo (2001). His Honors include: Helen Hay Whitney Foundation Postdoctoral Fellowship, Harold M. Weintraub Graduate Student Award, Japan-Stanford Association Graduate Fellowship, Stanford Graduate Fellowship, Pew Scholars Program, Packard Fellowship and Sloan Research Fellowship. Dr. Komiyama is a NYSCF-Robertson Investigator.

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