Biography
Synaptic and molecular mechanisms in learning and memory formation My lab is currently investigating the synaptic and molecular mechanisms involved in learning and memory formation in the mammalian central nervous system. Electrophysiological techniques are used to study synaptic transmission in a variety of in vitro preparations but most work concerns the mechanisms responsible for long-lasting changes in synaptic transmission that occur in the hippocampus, a region of the brain known to have an important role in learning and memory. In our experiments we use electrophysiological, pharmacological, and molecular genetic (transgenic mice) approaches to decipher the molecular components of the biochemical pathways responsible for memory formation in the mammalian brain and eventually hope to understand how alterations in these pathways may contribute to the memory impairment that occurs in pathological conditions such as Alzheimer’s disease or even as a result of normal aging.
Publications
A selected list of publications:
Ryan Tomás J, Kopanitsa Maksym V, Indersmitten Tim, Nithianantharajah Jess, Afinowi Nurudeen O, Pettit Charles, Stanford Lianne E, Sprengel Rolf, Saksida Lisa M, Bussey Timothy J, O’Dell Thomas J, Grant Seth G N, Komiyama Noboru H Evolution of GluN2A/B cytoplasmic domains diversified vertebrate synaptic plasticity and behavior Nature neuroscience, 2013; 16(1): 25-32.
Shigetomi Eiji, Jackson-Weaver Olan, Huckstepp Robert T, O’Dell Thomas J, Khakh Baljit S TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release The Journal of neuroscience : the official journal of the Society for Neuroscience, 2013; 33(24): 10143-53.
Ch’ng Toh Hean, Uzgil Besim, Lin Peter, Avliyakulov Nuraly K, O’Dell Thomas J, Martin Kelsey C Activity-dependent transport of the transcriptional coactivator CRTC1 from synapse to nucleus Cell, 2012; 150(1): 207-21.
Ziehn Marina O, Avedisian Andrea A, Dervin Shannon M, O’Dell Thomas J, Voskuhl Rhonda R Estriol preserves synaptic transmission in the hippocampus during autoimmune demyelinating disease Laboratory investigation; a journal of technical methods and pathology, 2012; 92(8): 1234-45.
Zheng Sika, Gray Erin E, Chawla Geetanjali, Porse Bo Torben, O’Dell Thomas J, Black Douglas L PSD-95 is post-transcriptionally repressed during early neural development by PTBP1 and PTBP2 Nature neuroscience, 2012; 15(3): 381-8, S1.
Coba Marcelo P, Komiyama Noboru H, Nithianantharajah Jess, Kopanitsa Maksym V, Indersmitten Tim, Skene Nathan G, Tuck Ellie J, Fricker David G, Elsegood Kathryn A, Stanford Lianne E, Afinowi Nurudeen O, Saksida Lisa M, Bussey Timothy J, O’Dell Thomas J, Grant Seth G N TNiK is required for postsynaptic and nuclear signaling pathways and cognitive function The Journal of neuroscience : the official journal of the Society for Neuroscience, 2012; 32(40): 13987-99.
Ziehn Marina O, Avedisian Andrea A, Dervin Shannon M, Umeda Elizabeth A, O’Dell Thomas J, Voskuhl Rhonda R Therapeutic testosterone administration preserves excitatory synaptic transmission in the hippocampus during autoimmune demyelinating disease The Journal of neuroscience : the official journal of the Society for Neuroscience, 2012; 32(36): 12312-24.
Moody Teena D, Watabe Ayako M, Indersmitten Tim, Komiyama Noboru H, Grant Seth G N, O’Dell Thomas J Beta-adrenergic receptor activation rescues theta frequency stimulation-induced LTP deficits in mice expressing C-terminally truncated NMDA receptor GluN2A subunits Learning & memory (Cold Spring Harbor, N.Y.), 2011; 18(2): 118-27.
Carlisle Holly J, Luong Tinh N, Medina-Marino Andrew, Schenker Leslie, Khorosheva Eugenia, Indersmitten Tim, Gunapala Keith M, Steele Andrew D, O’Dell Thomas J, Patterson Paul H, Kennedy Mary B Deletion of densin-180 results in abnormal behaviors associated with mental illness and reduces mGluR5 and DISC1 in the postsynaptic density fraction The Journal of neuroscience : the official journal of the Society for Neuroscience, 2011; 31(45): 16194-207.
Tenorio Gustavo, Connor Steven A, Guévremont Diane, Abraham Wickliffe C, Williams Joanna, O’Dell Thomas J, Nguyen Peter V ‘Silent’ priming of translation-dependent LTP by Ã-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors Learning & memory (Cold Spring Harbor, N.Y.), 2010; 17(12): 627-38.
Wiltgen Brian J, Royle Gordon A, Gray Erin E, Abdipranoto Andrea, Thangthaeng Nopporn, Jacobs Nate, Saab Faysal, Tonegawa Susumu, Heinemann Stephen F, O’Dell Thomas J, Fanselow Michael S, Vissel Bryce A role for calcium-permeable AMPA receptors in synaptic plasticity and learning PloS one, 2010; 5(9): .
Bliss Joanne M, Gray Erin E, Dhaka Ajay, O’Dell Thomas J, Colicelli John Fear learning and extinction are linked to neuronal plasticity through Rin1 signaling Journal of neuroscience research, 2010; 88(4): 917-26.
Arbuckle Margaret I, Komiyama Noboru H, Delaney Ada, Coba Marcelo, Garry Emer M, Rosie Roberta, Allchorne Andrew J, Forsyth Lynsey H, Bence Matthew, Carlisle Holly J, O’Dell Thomas J, Mitchell Rory, Fleetwood-Walker Susan M, Grant Seth G N The SH3 domain of postsynaptic density 95 mediates inflammatory pain through phosphatidylinositol-3-kinase recruitment EMBO reports, 2010; 11(6): 473-8.
O’Dell Thomas J, Connor Steven A, Gelinas Jennifer N, Nguyen Peter V Viagra for your synapses: Enhancement of hippocampal long-term potentiation by activation of beta-adrenergic receptors Cellular signalling, 2010; 22(5): 728-36.
Jeffrey Rachel A, Ch’ng Toh Hean, O’Dell Thomas J, Martin Kelsey C Activity-dependent anchoring of importin alpha at the synapse involves regulated binding to the cytoplasmic tail of the NR1-1a subunit of the NMDA receptor The Journal of neuroscience : the official journal of the Society for Neuroscience, 2009; 29(50): 15613-20.
Wang Louisa M-C, Dragich Joanna M, Kudo Takashi, Odom Irene H, Welsh David K, O’Dell Thomas J, Colwell Christopher S Expression of the circadian clock gene Period2 in the hippocampus: possible implications for synaptic plasticity and learned behaviour ASN neuro, 2009; 1(3): .
Fink Ann E, O’Dell Thomas J Short trains of theta frequency stimulation enhance CA1 pyramidal neuron excitability in the absence of synaptic potentiation The Journal of neuroscience : the official journal of the Society for Neuroscience, 2009; 29(36): 11203-14.
Chaudhary V Bala, Bowker Matthew A, O’Dell Thomas E, Grace James B, Redman Andrea E, Rillig Matthias C, Johnson Nancy C Untangling the biological contributions to soil stability in semiarid shrublands Ecological applications : a publication of the Ecological Society of America, 2009; 19(1): 110-22.
Carlisle Holly J, Fink Ann E, Grant Seth G N, O’Dell Thomas J Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity The Journal of physiology, 2008; 586(Pt 24): 5885-900.
Fink Ann E, Sariñana Joshua, Gray Erin E, O’dell Thomas J Activity-dependent depression of local excitatory connections in the CA1 region of mouse hippocampus Journal of neurophysiology, 2007; 97(6): 3926-36.
Gray Erin E, Fink Ann E, Sariñana Joshua, Vissel Bryce, O’Dell Thomas J Long-term potentiation in the hippocampal CA1 region does not require insertion and activation of GluR2-lacking AMPA receptors Journal of neurophysiology, 2007; 98(4): 2488-92.
Delgado Jary Y, Coba Marcelo, Anderson Christopher N G, Thompson Kimberly R, Gray Erin E, Heusner Carrie L, Martin Kelsey C, Grant Seth G N, O’Dell Thomas J NMDA receptor activation dephosphorylates AMPA receptor glutamate receptor 1 subunits at threonine 840 The Journal of neuroscience : the official journal of the Society for Neuroscience, 2007; 27(48): 13210-21.
Cuthbert Peter C, Stanford Lianne E, Coba Marcelo P, Ainge James A, Fink Ann E, Opazo Patricio, Delgado Jary Y, Komiyama Noboru H, O’Dell Thomas J, Grant Seth G N Synapse-associated protein 102/dlgh3 couples the NMDA receptor to specific plasticity pathways and learning strategies The Journal of neuroscience : the official journal of the Society for Neuroscience, 2007; 27(10): 2673-82.
Dunham Susie M, O’Dell Thomas E, Molina Randy Forest stand age and the occurrence of chanterelle (Cantharellus) species in Oregon’s central Cascade Mountains Mycological research, 2006; 110(Pt 12): 1433-40.
Dunham Susie M, O’Dell Thomas E, Molina Randy Spatial analysis of within-population microsatellite variability reveals restricted gene flow in the Pacific golden chanterelle (Cantharellus formosus) Mycologia, 2006; 98(2): 250-9.
Delgado Jary Y, O’dell Thomas J Long-term potentiation persists in an occult state following mGluR-dependent depotentiation Neuropharmacology, 2005; 48(7): 936-48.
Ho Oanh H, Delgado Jary Y, O’Dell Thomas J Phosphorylation of proteins involved in activity-dependent forms of synaptic plasticity is altered in hippocampal slices maintained in vitro Journal of neurochemistry, 2004; 91(6): 1344-57.
Thompson Kimberly R, Otis Klara Olofsdotter, Chen Dillon Y, Zhao Yali, O’Dell Thomas J, Martin Kelsey C Synapse to nucleus signaling during long-term synaptic plasticity; a role for the classical active nuclear import pathway Neuron, 2004; 44(6): 997-1009.
Watabe Ayako M, O’Dell Thomas J Age-related changes in theta frequency stimulation-induced long-term potentiation Neurobiology of aging, 2003; 24(2): 267-72.
Dunham Susie M, O’Dell Thomas E, Molina Randy Analysis of nrDNA sequences and microsatellite allele frequencies reveals a cryptic chanterelle species Cantharellus cascadensis sp. nov. from the American Pacific Northwest Mycological research, 2003; 107(Pt 10): 1163-77.
Opazo Patricio, Watabe Ayako M, Grant Seth G N, O’Dell Thomas J Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms The Journal of neuroscience : the official journal of the Society for Neuroscience, 2003; 23(9): 3679-88.
Dhaka Ajay, Costa Rui M, Hu Hailiang, Irvin Dwain K, Patel Apoor, Kornblum Harley I, Silva Alcino J, O’Dell Thomas J, Colicelli John The RAS effector RIN1 modulates the formation of aversive memories The Journal of neuroscience : the official journal of the Society for Neuroscience, 2003; 23(3): 748-57.
Watabe Ayako M, Carlisle Holly J, O’Dell Thomas J Postsynaptic induction and presynaptic expression of group 1 mGluR-dependent LTD in the hippocampal CA1 region Journal of neurophysiology, 2002; 87(3): 1395-403.
Komiyama Noboru H, Watabe Ayako M, Carlisle Holly J, Porter Karen, Charlesworth Paul, Monti Jennifer, Strathdee Douglas J C, O’Carroll Colin M, Martin Stephen J, Morris Richard G M, O’Dell Thomas J, Grant Seth G N SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor The Journal of neuroscience : the official journal of the Society for Neuroscience, 2002; 22(22): 9721-32.
Grant, SG O’Dell, TJ Multiprotein complex signaling and the plasticity problem Current opinion in neurobiology. , 2001; 11(3): 363-8.
Watabe, AM Zaki, PA O’Dell, TJ Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region The Journal of neuroscience : the official journal of the Society for Neuroscience. , 2000; 20(16): 5924-31.
Makhinson, M Chotiner, JK Watson, JB O’Dell, TJ Adenylyl cyclase activation modulates activity-dependent changes in synaptic strength and Ca2+/calmodulin-dependent kinase II autophosphorylation The Journal of neuroscience : the official journal of the Society for Neuroscience. , 1999; 19(7): 2500-10.
Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RGM, O’Dell TJ, and Grant, SGN Enhanced long term potentiation and impaired learning in mice with mutant postsynatpic density-95 protein, Nature, 1998; 396: 433-439.
Thomas MJ, Watabe AM, Moody TD, Makhinson M, and O’Dell TJ Postsynaptic complex spike bursting enables the inductio of LTP by theta frequency synaptic stimulation, J. Neuroscience, 1998; 18: 7118-7126.
Thomas, MJ Moody, TD Makhinson, M O’Dell, TJ Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region Neuron. , 1996; 17(3): 475-82.
Biography
Gina Poe has been working since 1995 on the mechanisms through which sleep serves memory consolidation and restructuring. Dr. Poe is a southern California native who graduated from Stanford University then worked for two post-baccalaureate years at the VA researching Air Force Test Pilots’ brainwave signatures under high-G maneuvers. She then earned her PhD in Basic Sleep in the Neuroscience Interdepartmental Program at UCLA under the guidance of Ronald Harper then moved to the University of Arizona for her postdoctoral studies with Carol Barnes and Bruce McNaughtons looking at graceful degradation of hippocampal function in aged rats as well as hippocampal coding in a 3-D maze navigated in the 1998 space shuttle mission. She brought these multiunit teachings to answer a burning question of whether REM sleep were for remembering or forgetting and found that activity of neurons during REM sleep is consistent both with the consolidation of novel memories and the elimination of already consolidated memories from the hippocampus, readying the associative memory network for new learning the next day. Moving first to Washington State University then to the University of Michigan before joining UCLA in 2016, Poe has over 80 undergraduates, 9 graduate students, and 8 postdoctoral scholars, and has served in university faculty governance as well as led 5 different programs designed to diversify the neuroscience workforce and increase representation of people of the global majority in the STEM fields. At UCLA she continues research and teaching and Directs the COMPASS-Life Sciences and BRI-SURE programs and co-Directs the MARC-U*STAR program. Nationally she has served as course director of the Marine Biological Lab’s SPINES course and co-Directs the Society for Neuroscience’s NSP program which earned the nation’s highest mentoring honor in 2018. These programs have over 1000 PhD level alumni.
Research Interests
The Poe lab investigates the mechanisms by which sleep traits serve learning and memory consolidation. Memories are encoded by the pattern of synaptic connections between neurons. We employ tetrode recording and optogenetic techniques in learning animals to see how neural patterns underlying learning are reactivated during sleep, and how activity during sleep influences the neural memory code. Both strengthening and weakening of synapses is important to the process of sculpting a network when we make new memories and integrate them into old schema. Results from our studies suggest that while synaptic strengthening can be efficiently accomplished during the waking learning process, the synaptic weakening part of memory integration requires conditions unique to sleep. The absence of noradrenaline during sleep spindles and REM sleep as well as the low levels of serotonin during REM sleep allow the brain to integrate new memories and to refresh and renew old synapses so that we are ready to build new associations the next waking period. Memory difficulties involved in post-traumatic stress disorder, Schizophrenia, Alzheimer’s disease and even autism involve abnormalities in the sleep-dependent memory consolidation process that my lab studies. Keywords: Sleep, learning and memory, PTSD, memory consolidation, reconsolidation, REM sleep, sleep spindles, Norepinephrine, LTP, depotentiation, reversal learning, optogenetics, electrophysiology, tetrode recordings, hippocampus, prefrontal cortex.
Education
B.A., Human Biology, Stanford University 1987
Ph.D., Neuroscience, University of California, Los Angeles 1995
Selected Publications
Cao J, Herman AB, West GB, Poe G, Savage VM. Unraveling why we sleep: Quantitative analysis reveals abrupt transition from neural reorganization to repair in early development. Sci Adv 6(38):eaba0398 (11 pages), 2020. doi: 10.1126/sciadv.aba0398.
Guthrie R, Ciliberti D, Mankin E, Poe GR. Recurrent hippocampo-neocortical sleep-state divergence in humans. PNAS 119(44): e2123427119, PM36279474, 2022.
Frazer M, Cabrera Y, Guthrie R, Poe GR. Shining a light on the mechanisms of sleep for memory consolidation. Current Sleep Medicine Rep, 7:221-231, 2021. https://doi.org/10.1007/s40675-021-00204-3.
Cabrera Y, Holloway J, Poe GR (2020) ‘Sleep Changes Across the Female Hormonal Cycle Affecting Memory: Implications for Resilient Adaptation to Traumatic Experiences.’ J Womens Health (Larchmt), 29 (3): 446-451. PMID: 32186966
Swift KM, Keus K, Echeverria CG, Cabrera Y, Jimenez J, Holloway J, Clawson BC, Poe GR () ‘Sex differences within sleep in gonadally-intact rats.’ Sleep, 2019.PMID: 31784755
Swift KM, Gross BA, Frazer MA, Bauer DS, Clark KJD, Vazey EM, Aston-Jones G, Li Y, Pickering AE, Sara SJ, Poe GR (2018) ‘Abnormal Locus Coeruleus Sleep Activity Alters Sleep Signatures of Memory Consolidation and Impairs Place Cell Stability and Spatial Memory.’ Curr Biol, 28 (22): 3599-3609.e4. PMID: 30393040
Zaborszky L, Gombkoto P, Varsanyi P, Poe GR, Role L, Ananth M, Rajebhosale P, Talmage D, Hasselmo M, Dannenberg H, Minces V, Chiba A, “Specific basal forebrain-cortical cholinergic circuits coordinate cognitive operations”, J Neurosci, 38 (44): 9446-9458 (2018).
Lewis P, Knoblich G, Poe GR, “Recasting reality: how memory replay in sleep boosts creative problem solving”, Trends Cogni Sci, 22 (6): 491-503 (2018).
Bjorness TE, Booth V, Poe GR (2018) ‘Hippocampal theta power pressure builds over non-REM sleep and dissipates within REM sleep episodes.’ Arch Ital Biol, 156 (3): 112-126. PMID: 30324607
Poe GR (2017) ‘Sleep Is for Forgetting.’ J Neurosci, 37 (3): 464-473. PMID: 28100731
Javanbakht, A and Poe, GR, “Behavioral neuroscience of circuits involved in arousal regulation”, The Neurobiology of PTSD, Ressler, K and Liberzon, I(Eds.), 130-147 (2016).
Emrick JJ, Gross BA, Riley BT, Poe GR (2016) ‘Different Simultaneous Sleep States in the Hippocampus and Neocortex.’ Sleep, 39 (12): 2201-2209. PMID: 27748240
Vanderheyden WM, George SA, Urpa L, Kehoe M, Liberzon I, Poe GR (2015) ‘Sleep alterations following exposure to stress predict fear-associated memory impairments in a rodent model of PTSD.’ Exp Brain Res, 233 (8): 2335-46. PMID: 26019008.
Watts A, Gritton HJ, Sweigart J, Poe GR (2012) ‘Antidepressant suppression of non-REM sleep spindles and REM sleep impairs hippocampus-dependent learning while augmenting striatum-dependent learning.’ J Neurosci, 32 (39): 13411-20. PMID: 23015432
Booth V, Poe GR (2006) ‘Input source and strength influences overall firing phase of model hippocampal CA1 pyramidal cells during theta: relevance to REM sleep reactivation and memory consolidation.’ Hippocampus, 16 (2): 161-73. PMID: 16411243