BIOGRAPHICAL SKETCH

NAME POSITION TITLE Attila Losonczy Assistant Professor eRA COMMONS USER NAME (credential, e.g., agency login) ALOSONCZY EDUCATION/TRAINING (Begin with baccalaureate or other initial professional education, such as nursing, include postdoctoral training and residency training if applicable.) DEGREE INSTITUTION AND LOCATION MM/YY FIELD OF STUDY (if applicable) University Medical School of Pécs, Hungary M.D. 09/93-09/99 General Medicine Semmelweis University, Budapest, Hungary Ph.D. 10/99-10/04 Neurobiology LSU Medical Center, New Orleans, LA, USA Postdoc. 08/03-07/06 Neurophysiology Yale School of Medicine, New Haven, CT, USA Postdoc. 08/06-04/07 Neurophysiology HHMI Janelia Farm Research Campus, Ashburn, VA, Postdoc. 05/07-10/09 Neurophysiology USA

A. Personal Statement The goal of my research program is to promote our understanding of elementary molecular/cellular and circuit mechanisms of complex cognitive memory behaviors. My research focuses on the rodent , because here this degree of understanding appears to be within reach. Here, my ongoing work aims to dissect the role excitatory, inhibitory and neuromodulatory circuits in episodic memory formation and spatial navigation. I also aim to promote our understanding of how cell type-specific network dynamics is altered under pathological conditions in animal models of neurological and neuropsychiatric disorders, such as of epilepsy and schizophrenia. To address these questions, we combine large-scale subcellular-resolution functional imaging with electrophysiological, and cell-type specific manipulations in vivo and in vitro. I have established successful collaborations with molecular neurobiologists (R. Hen, J. Gogos, F. Polleux, B. Zemelman), physicists (A. Vaziri) theoretical and computational (L. Abbott, J. Lisman) and hippocampal cellular and systems neuroscientists (I. Soltesz, G. Buzsaki) to develop and implement experimental tools and theoretical frameworks for mechanistic investigations into hippocampal cognitive memory functions under normal and pathological conditions.

B. Positions and Honors

Positions and Employment 09/95-09/99 Undergraduate Research Assistant, Department of Anatomy, University Medical School of Pécs, Hungary, (Prof. G. Lazar) 10/99-03/00 Graduate student, Department of Pharmacology, Univ. Med. School of Pécs, Hungary, (Prof. L. Seress) 04/00-07/00 Visiting student, MRC Anatomical Neuropharmacology Unit, Oxford, UK, (Prof. P. Somogyi) 08/00- 07/03 Graduate student, Laboratory of Cellular Neurophysiology, Institute of Experimental Medicine of the Hungarian Academy of Sciences, Hungary (Prof. Z. Nusser) 08/03-07/06 Postdoctoral Fellow, Neuroscience Center, LSU Medical Center, New Orleans, LA, USA, (Prof. J.C. Magee) 08/06-04/07 Postdoctoral Fellow, Department of Cell Biology, Yale School of Medicine, New Haven, CT, USA, (Prof. G. Miesenbock) 05/07-10/09 Research Specialist, HHMI Janelia Farm Research Campus, Ashburn, VA, USA, (Prof. J.C. Magee)

1 11/09 - present Assistant Professor, Department of Neuroscience, Columbia University, New York, NY, USA 00-07/0004/00-07/ 04/00-07/00 Honors and Awards 2001 BIF Graduate Student Scholarship – Boehringer Ingelheim Foundation 2010 Member – Kavli Institute for Brain Science, Columbia University 2011 Searle Scholar – Searle Kinship Foundation 2012 HFSP Program Grant – Human Frontiers Science 2012 Harvey L. Karp Discovery Award 2013 Young Investigator Award – NARSAD 2013 Memory and Cognitive Disorders Award – McKnight Foundation 2014 Brain Initiative Award

Reviewer for Journals and Funds Science, Cell, Nature Neuroscience, Nature Reviews Neuroscience, Neuron, Nature Communications, The Journal of Neuroscience, Journal of Physiology, European Journal of Neuroscience, Hippocampus, Cerebral Cortex, IEEE Transactions on Neural Networks and Learning Systems, Journal of the Royal Society Interface

NIH Molecular and Cellular Substrates of Complex Brain Disorders Special Emphasis Panel ZRG1 MDCN- P(57), European Research Council (ERC), The Wellcome Trust (UK), Royal Society (UK), Human Brain Project (EU), Swiss Science Foundation, The Hungarian Scientific Research Fund, Hungarian Brain Project, Human Frontiers Science Program (HFSP)

Invited Speaker/Departmental Seminar 2015 Harvard Center for Brain Science 2015 Centre de Recherche Université Laval Robert-Giffard, Canada – invited by Lisa Topolnik 2014 GABAergic Signaling in Health and Disease, Washington DC 2014 Max Planck Florida Institute, Jupiter, Florida – invited by David Fitzpatrick 2014 Center for Biomedical Neuroscience, San Antonio, Texas – Neurology Ground Round 2014 Department of Neurobiology, Harvard Medical School – invited by Christopher Harvey 2014 Freiburg University, Germany – invited by Marlene Bartos 2014 Institute of Science and Technology, Vienna, Austria – invited by Peter Jonas 2014 Gordon Research Conferences – Synaptic transmission, Waterville Valley, New Hampshire 2014 FENS – In vivo functional recording of neuronal population activity, Milan, Italy 2014 Conference Jacques Monod – Optical imaging of brain structure and function on multiple spacial scales, Roscoff, France – invited by Angus Silver 2014 Department of Neuroscience, Yale University, New Haven – invited by Michael Higley 2014 NIH/NIGMS, Bethesda – invited by Chris McBain 2014 Epilepsy Research Center Symposium, Irvine – invited by Ivan Soltesz 2014 IBRO Workshop, Debrecen, Hungary 2013 Institute of Experimental Medicine, Budapest, Hungary – invited by Tamas Freund 2013 Friedrich Miescher Institute, Basel, Switzerland – invited by Pico Caroni 2013 Gordon Research Conferences – Inhibition in the CNS, Les Diablerets, Switzerland 2013 Gordon Research Conferences – Dendrites, Les Diablerets, Switzerland 2013 Picower Institute, MIT, Boston – invited by Susumu Tonegawa 2012 HHMI Janelia Farm Conference – Neuron types in the hippocampal formation 2012 Department of Neurobiology, New York University, New York – invited by Gord Fishell 2012 Albert Einstein College of Medicine, Department of Neuroscience – invited by Pablo Castillo 2012 HHMI Janelia Farm Conference – Dendrites, substrates for information processing 2011 IBRO/FENS Conference, Ljubljana 2011 Department of Physiology, Columbia University, New York – invited by Wes Gruber 2008 Department of Neuroscience, Yale, New Haven 2008 Picower Institute, MIT, Boston 2006 Department of Anatomy, UC Irvine 2005 Southern Photonics Conference, Atlanta

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C. Peer-reviewed Publications

1) Turi, G.F., Wittmann, G., Lechan, M.R., and Losonczy A. Ambient GABA modulates septo-hippocampal inhibitory terminals via presynaptic GABAb receptors. Neuropharmacology, 2015 (online) 2) Kaifosh, P. and Losonczy, A (2014) The inside track: privileged neural communication through axon- carrying dendrites. Neuron, 83:1231-1234 3) Piant S, Specht A, Zemelman B, Losonczy A, and Bolze, F. (2014) Two-photon sensitive photolabile protecting groups: From molecular engineering to nanostructuration. Biomedical Optics, doi.org/10.1364/BIOMED.2014.BT3A. 4) Kaifosh, P., Zaremba, J., Danielson, N., and Losonczy, A. (2014) SIMA: Python software for analysis of dynamic fluorescence imaging data. Frontiers in Neuroinformatics, 8:80. doi:10.3389/fninf.2014.00080. 5) Denny, C.A., Kheirbek, M.A., Alba, E.L., Tanaka, K.F., Brachman, R.A., Laughman, K.B., Tomm, N.K., Turi, G.F., Losonczy, A., and Hen, R. (2014). Hippocampal memory traces are differentially modulated by experience, time, and adult . Neuron, 83:189-201., PMID: 24991962 6) Lee, S-H., Marchionni, I., Bezaire, M., Varga, C., Danielson, N., Lovett-Barron, M., Losonczy, A., and Soltesz, I. (2014). Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells. Neuron, 82:1129-1144, PMID: 24836505 8) Lovett-Barron, M., Kaifosh, P., Kheirbek, M.A., Danielson, N., Zaremba, J.D., Reardon, T.R., Turi, F.G., Hen, R., Zemelman, B.V., and Losonczy, A. (2014). Dendritic inhibition in the hippocampus supports fear learning. Science, 21, 857-63., PMID: 24558155 9) Lovett-Barron, M., Losonczy, A. (2014). Behavioral consequences of GABAergic neuronal diversity. Current Opinion in Neurobiology, 26, 27-33., PMID: 24650501 10) Kaifosh, P., Lovett-Barron, M., Turi, G., Reardon., T.T., and Losonczy, A. (2013). Septo-hippocampal GABAergic signaling across multiple modalities in awake mouse. Nature Neuroscience, 16, 1182- 1184., PMID: 23912949 11) Lovett-Barron, M., and Losonczy, A. (2013). Circuits supporting the grid. Nature Neuroscience, 16, 255-257., PMCID: PMC23434976 12) Royer, S., Zemelman, B.V., Losonczy, A., Kim, J., Chance, F., Magee, J.C., and Buzsáki, G., (2012). Control of timing, rate and firing patterns of hippocampal place cells by dendritic and perisomatic inhibition. Nature Neuroscience, 15, 769-775., PMCID: PMC22446878 13) Lovett-Barron, M., Turi, G.F., Kaifosh, P., Lee, P.H., Bolze, F., Sun X-H., Nicoud J-F., Zemelman, B.V., Sternson, S.M., and Losonczy, A. (2012) Regulation of neuronal input output transformation by tunable dendritic inhibition. Nature Neuroscience, 15, 423-430., PMCID: PMC22246433 Oren, I., and Kullmann, D. (2012) New and Views, Nature Neuroscience, 15, 344-345. Cover illustration 14) Bolze, F., Nicoud J.F., Bourgogne, C., Gug, S., Sun, X.H., Goeldner, M., Specht, A., Donato, L.. Warther, D., Turi, G.F., and Losonczy, A. (2012). Two-photon uncaging: the chemist point of view. Optical Materials, 34, 1664-1669. 15) Losonczy, A., Zemelman, B.V., Vaziri, A. and Magee, J.C. (2010) Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons. Nature Neuroscience, 13, 967- 972., PCMID: PMC2921679 16) Royer, S., Zemelman. B.V., Losonczy, A., Buzsáki, G. and Magee, J.C. (2010) Optoelectronic neural interface (ONI): light-assisted perturbation of silicon probe-monitored local circuits in the behaving animal. European Journal of Neuroscience, 31, 2279-2291., PMCID: PMC2954764 17) Makara, J.K., Losonczy, A., Wen, Q., and Magee, J.C. (2009) Experience-dependent compartmentalized dendritic plasticity in rat hippocampal CA1 pyramidal neurons. Nature Neuroscience, 12, 1485-1487., PCMID: PMC2921679 18) Varga, V., Losonczy, A., Zemelman, B.V., Borhegyi, Z., Nyiri, G., Domonkos, G., Hangya, B., Holderith, B., Magee, J.C., and Freund, T.F. (2009) Fast synaptic subcortical control of hippocampal circuits. Science, 326, 449–453., PCMID: PMC2921679

3 19) Losonczy, A., Makara, J.K., and Magee, J.C. (2008) Compartmentalized dendritic plasticity and input feature storage in neurons. Nature, 452, 436-441., PCMID: PMC2921679 Spruston, N. (2008) News and Views. Nature, 452, 420-421. 20) Gasparini, S., Losonczy, A., Chen, X., Johnston, D., and Magee, J.C. (2007) Associative pairing enhances action potential back-propagation in radial oblique branches of CA1 pyramidal neurons Journal of Physiology, 580, 787-800., PCMID: PMC2075451 21) Losonczy, A., and Magee, J.C. (2006) Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron, 50, 291-307., PMID: 16630839 Judkewitz, B., Roth, A., Häusser, M., (2006) News and Views. 50, 180-183. Cover illustration 22) Losonczy, A., Biro, A.A., and Nusser, Z. (2004) Persistently active cannabinoid receptors mute subpopulation of hippocampal interneurons. Proceedings of the National Academy of Sciences USA, 101, 1362-1367., PMCID: PMC337058 23) Losonczy, A., Somogyi, P., and Nusser, Z. (2003) Reduction of excitatory postsynaptic responses by persistently active metabotropic glutamate receptors in the hippocampus.. Journal of Neurophysiology, 89: 1910-1919., PMID: 12686572 24) Losonczy, A., Zhang, L., Shigemoto, R., Somogyi, P., and Nusser, Z. (2002) Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones. Journal of Physiology, 542: 193-210., PMCID: PMC2290398

D. Research Support ACTIVE 1R01MH100631-01A1 (Losonczy) 3/1/2014 – 2/28/2019 NIH/NIMH Hippocampal inhibitory control of contextual fear learning

The major goals of the project are to dissect the role hippocampal GABAergic inhibitory circuits in contextual fear learning.

1U01NS090583-01 (Soltesz) 9/30/2014 – 7/31/2017 NIH/NINDS Towards a complete description of the circuitry underlying memory replay

The major goal of the project is to understand how the hippocampus generates sharp-wave- ripples.

Human Frontiers Science Program Grant (Losonczy) 9/1/2012 – 9/01/2015 Human Frontiers Science Program In vivo functional imaging and high-resolution manipulations of hippocampal memory circuits

The major goal of the project is to develop novel imaging, photoactivation and opto-chemical methods to study activity in the hippocampus

Memory and Cognitive Disorders Award (Losonczy) 2/1/2013 – 2/1/2016 McKnight Foundation Dissecting hippocampal microcircuit dysfunctions underlying cognitive memory deficits in schizophrenia

The major goal of the project is to dissect hippocampal microcircuit mechanisms of cognitive memory deficits in mouse models of schizophrenia using in vivo recordings

PENDING

GRANT11828896 (Soltesz, Losonczy) 9/1/2015 – 8/31/2020 NIH 4 Closed-loop intervention in epilepsy

This study aims to study the effect of optogenetic intervention in epilepsy.

GRANT11830695 (Vaziri, Losonczy) 9/1/2015 – 8/31/2020 NIH High-speed volumetric imaging of neuronal network activity at depth using Multiplexed Scanned Temporal Focusing (MuST)

The major goal of this study is to develop and implement novel functional imaging techniques to study cortical circuit function.

INACTIVE

Searle Scholarship (Losonczy) 6/20/2011 – 6/20/2014 Searle Kinship Foundation Inhibitory control of hippocampal memory functions

This study aims to study the role of in inhibition during hippocampal spatial navigation using in vivo intracellular recordings.

Young Investigator Award (Losonczy) 2/1/2013 – 2/1/2015 The Brain and Behavior Research Foundation

This major goal of this project is to dissect hippocampal GABAergic inhibitory circuit deficits in schizophrenia

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