Dr. Marie-Ève Tremblay

Dr. Marie-Ève Tremblay
Position
Professor, Canada Research Chair (Tier II) of Neurobiology of Aging and CognitionDivision of Medical Sciences
Contact
Office: Medical Sciences Building, room 322evetremblay@uvic.ca250-721-8739website
Area of expertise

Aging, cognition, microglia-synapse interactions, non-invasive brain imaging

Dr. Tremblay’s research focuses on aging and cognition, using both animal and human brain models to explore the significance of microglial remodelling of neuronal circuits and elimination of synapses in the pathogenesis of brain disorders. She has developed state-of-the-art expertise in non-invasive imaging of the brain—combining chronic longitudinal two-photon in vivo imaging and correlative immunocytochemical electron microscopy with 3D reconstruction—to study the physiological roles of immune cells across the lifespan.

Dr. Tremblay came to the University of Victoria from the Université Laval in Quebec, where she was an Associate Professor in the Molecular Medicine Department. While at the Université Laval, Dr. Tremblay received a CIHR Foundation Scheme grant and a Canada Research Chair, Tier II in Neuroimmune Plasticity in Health and Therapy, among other impressive grants and awards. She has developed national and international prominence for her work, and has collaborated with many scientists. She also supports diversity and inclusivity, whether she is recruiting trainees or organizing events that include speaker panels.

Dr. Tremblay received her PhD in Sciences neurologiques at Université de Montréal in 2009. She was a Postdoctoral Fellow in the Department of Neurobiology and Anatomy and Center for Visual Science at the University of Rochester from 2009 – 2011 and in the Department of Psychiatry at the University of Wisconsin-Madison from 2011 – 2012.

 

A series of discoveries spanning the last decade has challenged our view of microglia, the resident immune cells of the brain, by showing their essential contribution to the experience-dependent remodelling of neuronal circuits. In this emerging field of investigation, Dr. Tremblay’s research program aims to determine –using a combination of non-invasive imaging techniques (electron microscopy with immunostaining and 3D-reconstruction, two-photon in vivo microscopy)– how this newly-defined basic mechanism could be implicated in the loss of synapses that best correlates with the impairment of learning and memory across chronic stress, depression, schizophrenia, aging, and neurodegenerative diseases.

At the University of Victoria, Dr. Tremblay plans to explore therapeutic interventions promoting resilience of the brain immune cells to stress that will, in turn, promote healthy cognitive aging and theoretically prevent related brain conditions through the maintenance of its complex circuitry and plasticity. Her research will have translational and biomarker development aspects that will serve well in creating potential collaborations with many researchers within the Division of Medical Sciences, as well as with researchers from other departments and institutions affiliated with the university.

 

View all of Dr. Tremblay's publication 

Research Articles

 

Cisbani G, Poggini S, Laflamme N, Pons V, Tremblay ME, Branchi I, and Rivest S (2020) The Intellicage system provides a reproducible and standardized method to assess behavioral changes in cuprizone-induced demyelination mouse model. Behavioral Brain Research (impact factor 2.98) 400: 113039.

Madore C, Leyrolle Q, Morel L, Delpech JC, Greenhalgh AD, Lacabanne C, Bosch-Bouju C, Bourel J, Thomazeau A, Hopperton KE, Beccari S, Sere A, Aubert A, De Smedt-Peyrusse V, Lecours C, Bisht K, Fourgeaud L, Gregoire S, Bretillon L, Grant NJ, Badaut J, Gressens P, Sierra A, Butovsky O, Tremblay ME, Bazinet RP, Joffre C, Nadjar A, and Layé S (2020) Essential omega-3 fatty acids tune microglial phagocytosis of synaptic elements in the developing brain. Nature Communications (impact factor 12.12) 11: 6133.

Hui CW, Vecchiarelli HA, Gervais E, Luo X, Michaud F, Scheefhals L, Bisht K, Sharma K, Topolnik L*, and Tremblay ME* (2020) Sex differences of microglia and synapses in the hippocampal dentate gyrus of adult mouse offspring exposed to maternal immune activation. Frontiers in Cellular Neuroscience – Non-neuronal cells (impact factor 3.93) 14: 558181. *Co-corresponding authors.

Francavilla R, Guet-McCreight A, Amalyan S, Hui CW, Topolnik D, Michaud F, Marino B, Tremblay ME, Skinner FK, and Topolnik K (2020) Alterations in intrinsic and synaptic properties of hippocampal CA1 VIP interneurons during aging. Frontiers in Cellular Neuroscience – Cellular Neurophysiology (impact factor 3.92) 14: 554405.

Lecours C St-Pierre MK, Picard K, Bordeleau M, Bourque M, Awogbindin IO, Benadjal A, Gonzalez Ibanez F, Gagnon D, Cantin L, Parent M, Di Paolo T, and Tremblay ME (2020) Levodopa partially rescues microglial numerical, morphological, and phagolysosomal alterations in a monkey model of Parkinson’s disease. Brain, Behavior and Immunity (impact factor 6.63) 90: 81.

Bordeleau M, Lacabanne C, Fernández de Cossío L, Vernoux N, Savage JC, González-Ibáñez F, and Tremblay ME (2020) Microglial and peripheral immune priming is partially sexually dimorphic in adolescent mouse offspring exposed to maternal high fat diet. Journal of Neuroinflammation (impact factor 5.70) 17: 264.

Gratuze M, Leyns CEG, Sauerbeck AD, St-Pierre MK, Xiong M, Kim N, Remolina Serrano J, Tremblay ME, Kummer TT, Colonna M, Ulrich JD, and Holtzman DM (2020) Impact of TREM2R47H variant on tau pathology-induced gliosis and neurodegeneration. Journal of Clinical Investigation (impact factor 12.28) 130: 4954.

Melki I, Allaeys I, Tessandier N, Lévesque T, Cloutier N, Laroche A, Vernoux N, Becker Y, Hadrien Benk-Fortin, Julien AS, Zufferey A, Labelle ER, Poirier G, Patey N, Soulet D, Tremblay ME, McKenzie S, Lood C, Fortin PR, and Boilard E (2020) Platelets release mitochondrial antigens in systemic lupus erythematosus. Science Translational Medicine (impact factor 16.30). In press.

Matovic S, Ichiyama A, Igarashi H, Salter E, Sunstrum J, Wang XF, Henry M, Kuebler E, Vernoux N, Martinez-Trujillo J, Tremblay ME, and Wataru I (2020) Neuronal hyperactivity dampens neuronal intrinsic excitability and stress responsiveness during chronic stress. The Journal of Physiology (impact factor 4.55) 598: 2757.

Ouellette J, Toussay X, Comin CH, da F. Costa L, Ho M, Lacalle-Aurioles M, Freitas-Andrade M, Liu QY, Leclerc S, Pan Y, Liu Z, Thibodeau JF, Yin M, Carrier M, Morse CJ, Van Dyken P, Bergin CJ, Baillet S, Kennedy CR, Tremblay ME, Benoit YD, Stanford WL, Burger D, Stewart DJ, and Lacoste B (2020) Vascular contributions to 16p11.2 deletion autism syndrome modeled in mice. Nature Neuroscience (impact factor 21.12) 23: 1090.

Awarded University of Ottawa’s Faculty of Medicine paper of the year 2020.

Savage JC, St-Pierre MK, Carrier M, El Hajj H, Weiser Novak S, Sanchez MG, Cicchetti F, and Tremblay ME (2020) Microglial physiological properties and interactions with synapses are altered at presymptomatic stages in a mouse model of Huntington's disease pathology. Journal of Neuroinflammation (impact factor 5.70) 17: 98.

Tian W, Alsaadi R, Guo Z, Kalinina A, Carrier M, Tremblay ME, Lacoste B, Lagace D, and Russell RC (2020) An antibody for analysis of autophagy induction. Nature Methods (impact factor 28.47) 17: 232.

Savage JC, St-Pierre MK, Hui CW, and Tremblay ME (2019) Microglial ultrastructure in the hippocampus of a lipopolysaccharide-induced sickness mouse model. Frontiers in Neuroscience – Neurodegeneration (impact factor 3.71) 13: 1340.

Lounas A, Vernoux N, Tremblay ME, Germain M, and Richard FJ (2019) Mitochondrial sub-cellular localization of cAMP-specific phosphodiesterase 8A in ovarian follicular cells. Scientific Reports (impact factor 4.01) 9: 12493.

Gonzalez Ibanez F, Picard K, Bordeleau M, Sharma K, Bisht K, and Tremblay ME (2019) Immunofluorescence staining using IBA1 and TMEM119 for microglial density, morphology and peripheral myeloid cell infiltration analysis in mouse brain. Journal of Visualized Experiments (impact factor 1.05) 152: e60510. doi: 10.3791/60510.

El Hajj H, Savage JC, Bisht K, Parent M, Vallières L, Rivest S, and Tremblay ME (2019) Ultrastructural evidence of microglial heterogeneity in Alzheimer’s disease amyloid pathology. Journal of Neuroinflammation (impact factor 5.70) 16: 87.

Becker Y, Loignon RC, Julien AS, Marcoux G, Allaeys I, Lévesque T, Rollet-Labelle E, Benk-Fortin H, Cloutier N, Melki I, Eder L, Wagner E, Pelletier M, El Hajj H, Tremblay ME, Belleannée C, Hébert MJ, Dieudé M, Rauch J, Fortin PR, and Boilard E (2019) Anti-mitochondrial autoantibodies in systemic lupus erythematosus and their association with disease manifestations. Scientific Reports (impact factor 4.01) 9: 4530.

Jean LeBlanc N, Menet R, Picard K, Parent G, Tremblay ME, and ElAli A (2019) Canonical Wnt Pathway Maintains Blood-Brain Barrier Integrity Upon Ischemic Stroke and Its Activation Ameliorates Tissue Plasminogen Activator Therapy. Molecular Neurobiology (impact factor 4.26) 56: 6521.

Bellver-Landete V, Bretheau F, Mailhot B, Vallières N, Lessard M, Janelle ME, Vernoux VTremblay ME, Fuehrmann T, Shoichet M, and Lacroix S (2019) Microglia are an essential component of the neuroprotective scar that forms after spinal cord injury. Nature Communications (impact factor 12.35) 10: 518.

Hui CW, Bhardwaj SK, Sharma K, Joseph AT, Bisht KPicard KTremblay ME*, and Srivastava L* (2019) Microglia in the developing prefrontal cortex of rats show dynamic changes following neonatal disconnection of the ventral hippocampus. Neuropharmacology (impact factor 4.37) 146: 264. *Co-corresponding authors.

Denis HL, Lamontagne-Proulx J, St-Amour I, Mason SL, Rowley JW, Cloutier N, Tremblay MEEl Hajj H, Vincent AT, Gould PV, Chouinard S, Weyrich AS, Rondina MT, Barker RA, Boilard E, and Cicchetti F (2018) Platelet abnormalities in Huntington's disease. Journal of Neurology, Neurosurgery, and Psychiatry (impact factor 7.14) 90: 272.

Maxan A, Mason S, Saint-Pierre M, Smith E, Ho A, Harrower T, Watts C, Tai Y, Pavese N, Savage JCTremblay ME, Gould P, Rosser A, Dunnett S, Piccini P, Barker R, and Cicchetti F (2018) Outcome of cell suspension allografts in a patient with Huntington’s disease. Annals of Neurology (impact factor 10.24) 84: 950.

Acharjee S, Verbeek M, Gomez C, Bisht K, Lee B, Benoit L, Sharkey K, Benediktsson A, Tremblay ME, and Pittman Q (2018) Reduced microglial activity and enhanced glutamate transmission in the basolateral amygdala in early CNS autoimmunity. Journal of Neuroscience (impact factor 5.97) 38: 9019.

Bernet A, Bastien A, Soulet D, Jerczynski O, Roy C, Rodrigues Alves MB, Lecours CTremblay ME, Bailey J, Robert C, and Belleannée C (2018) Cell-lineage specificity of primary cilia during postnatal epididymal development. Human Reproduction (impact factor 5.51) 33: 1829.

Baldy C, Fournier S, Boisjoly-Villeneuve STremblay ME, and Kinkead R (2018) The influence of sex and neonatal stress on medullary microglia in rat pups. Experimental Physiology (impact factor 2.87) 103: 1192.

Hui CWSt-Pierre MK, Detuncq J, Aumailley L, Dubois MJ, Couture V, Skuk D, Marette A, Tremblay JP, Lebel M*, and Tremblay ME* (2018) Nonfunctional mutant Wrn protein leads to neurological deficits, neuronal stress, microglial alteration, and immune imbalance in a mouse model of Werner syndrome. Brain, Behavior, and Immunity (impact factor 6.31) 73: 450. * Co-corresponding authors.

Laflamme N, Cisbani G, Préfontaine P, Srour Y, Bernier J, St-Pierre MKTremblay ME, and Rivest S (2018) mCSF-induced microglial activation prevents myelin loss and promotes its repair in a mouse model of multiple sclerosis. Frontiers in Cellular Neuroscience (impact factor 3.90) 12: 178.

Iulita MF, Vallerand D, Beauvillier M, Haupert N, Ulysse CA, Gagné AVernoux N, Duchemin S, Boily M, Tremblay ME, and Girouard H (2018) Differential effect of angiotensin II and blood pressure on hippocampal inflammation in mice. Journal of Neuroinfammation (impact factor 5.19) 15: 62.

Henry MSBisht KVernoux N, Gendron L, Torres-Berrio A, Drolet G*, and Tremblay ME* (2018) Delta opioid receptor signaling promotes resilience to stress under the repeated social defeat paradigm in mice. Frontiers in Molecular Neuroscience (impact factor 3.72) 11: 100. *Equal contribution.

Garofalo S, Porzia A, Mainiero F, Di Angelantonio S, Cortese B, Basilico B, Pagani F, Cignitti G, Chece G, Maggio R, Tremblay MESavage JBisht K, Esposito V, Bernardini G, Seyfried T, Mieczkowski J, Stepniak K, Kaminska B, Santoni A, and Limatola C (2018) Environmental stimuli shape microglial plasticity in glioma. eLife (impact factor 7.62). pii: e33415.

Hui CWSt-Pierre AEl Hajj HRemy Y, Hebert SS, Luheshi GN, Srivastava L, and Tremblay ME (2018) Prenatal immune challenge leads to sex-dependent behavioral, microglial, and molecular abnormalities associated with schizophrenia later in life. Frontiers in Molecular Neuroscience (impact factor 3.72) 11: 13.

Paris I, Savage JC, Escobar L, Gagnon SHui CWTremblay ME, Sierra A, and Valero J (2017) ProMoIJ: a new tool for automatic three-dimensional analysis of microglial processes motility. GLIA (impact factor 5.85) 66: 828.

Tenorio-Lopes L, Henry MS, Marques D, Tremblay ME, Drolet G, Bretzner F, and Kinkead R (2017) Neonatal maternal separation opposes the facilitatory effect of castration on the respiratory response to hypercapnia of the adult male rat: evidence for the involvement of the medial amygdala. Journal of Neuroendocrinology (impact factor 3.39) 29: 1.

Lowery RL, Tremblay ME, Hopkins BE, and Majewska AK (2017) The microglial fractalkine receptor is not required for activity-dependent plasticity in the mouse visual system. GLIA (impact factor 5.85) 65: 1744.

Stamatiades E, Tremblay ME, Bohm M, Bisht K, Kao D, Coelho C, Crozet L, Diebold S, Davidson A, Heeger PS, Nimmerjahn F, and Geissmann F (2016) Immune monitoring of trans-endothelial transport by resident kidney macrophages. Cell (impact factor 36.22) 166: 991. Featured in Nature Reviews Nephrology (2016) 12: 579 and recommended by Faculty of 1000 (“exceptional” mention).

Goupil S, Maréchal L, El Hajj HTremblay ME, Richard FJ, and Leclerc P (2016) Identification and localization of the cyclic nucleotide phosphodiesterase 10A in bovine testis and mature spermatozoa. PLoS ONE (impact factor 2.77) 11: e0161035.

Alboni S, Poggini S, Garofalo S, Milior G, El Hajj HLecours CGirard IGagnon SBoisjoly-Villeneuve S, Brunello N, Wolfer DP, Limatola C, Tremblay ME*, Maggi L*, and Branchi I* (2016) Fluoxetine treatment affects the inflammatory response and microglial function according to the quality of the living environment. Brain, Behavior, and Immunity (impact factor 6.31) 58: 261. *Equal contribution.

Bisht KSharma KLecours CSánchez MGEl Hajj H, Milior G, Olmos-Alonso A, Gómez-Nicola D, Luheshi G, Vallières L, Branchi I, Maggi L, Limatola C, Butovsky O, and Tremblay ME (2016) Dark microglia: a new phenotype predominantly associated with pathological states. GLIA (impact factor 5.85) 64: 826.
Featured in New Scientist, The Jackson Laboratory, AlzForum, among others.

Sipe GO*, Lowery RL*, Tremblay ME, Kelly EA, Lamantia CL, and Majewska AK (2016) Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex. Nature Communications (impact factor 12.35) 7: 10905. *Equal contribution. Recommended by Faculty of 1000.

Abiega O, Beccari S, Diaz-Aparicio I, Nadjar A, Layé S, Leyrolle Q, Gómez-Nicola D, Domercq M, Pérez A, Sánchez-Zafra V, Paris I, Valero J, Savage JCHui CWTremblay ME, Deudero JJP, Brewster AL, Anderson AE, Zaldumbide L, Galbarriatu L, Marinas A, Vivanco MdM, Matute C, Maletic-Savatic M, Encinas JM, and Sierra A (2016) Neuronal hyperactivity disturbs ATP microgradients and triggers apoptosis/microglial phagocytosis uncoupling. PLoS Biology (impact factor 9.16) 14: e1002466.

Tremblay ME, Zhang I, Bisht KSavage JCLecours C, Parent M, Titorenko V, and Maysinger D (2016) Remodeling of lipid bodies by docosahexaenoic acid in activated microglial cells. Journal of Neuroinflammation (impact factor 5.19) 13: 116.

Groulx N, Lecours C, Turgeon N, Volckens J, Tremblay ME, and Duchaine C (2016) Nano-scale aerovirology: an efficient yet simple method to analyse the viral content of single bioaerosols. Aerosol Science & Technology (impact factor 2.00) 50: 732.

Bisht K*, El Hajj H*, Savage JCSánchez MG, and Tremblay ME (2016) Correlative light and electron microscopy to study microglial interactions with β-amyloid plaques. Journal of Visualized Experiments (impact factor 1.18) 112: e54060. doi:10.3791/54060 *Equal contribution.

Smith PY, Hernandez-Rapp J, Jolivette F, Lecours CBisht K, Goupil C, Parsi S, Morin F, Planel E, Bennett DA, Fernandez-Gomez FJ, Sergeant N, Buée L, Tremblay ME, Calon F, and Hébert SS (2015) miR-132/212 deficiency impairs Tau metabolism and promotes aggregation in mice. Human Molecular Genetics (impact factor 4.90) 4: 6721.

Milior G*, Lecours C*, Samson LBisht K, Poggini S, Pagani F, Deflorio C, Lauro C, Alboni S, Limatola C, Branchi I#Tremblay ME#, and Maggi L# (2015) Fractalkine receptor deficiency impairs microglial and neuronal responsiveness to chronic stress. Brain, Behavior, and Immunity (impact factor 6.31) 55: 114-25. *,#Equal contribution.
Selected for cover page of July 2016 edition.

Audoy-Rémus J, Bozoyan L, Dumas A, Filali M, Lecours C, Lacroix S, Rivest S, Tremblay ME, and Vallières L (2015) GPR84 deficiency reduces microgliosis, but accelerates dendritic degeneration and cognitive decline in a mouse model of Alzheimer’s disease. Brain, Behavior, and Immunity (impact factor 6.31) 46: 112.

Bastien D, Bellver Landete V, Lessard M, Vallières N, Champagne M, Takashima A, Tremblay ME, Doyon Y, and Lacroix S (2015) Il-1α gene deletion protects oligodendrocytes after spinal cord injury through upregulation of the survival factor Tox3. Journal of Neuroscience (impact factor 5.97) 35: 10715.

Lampron A, Larochelle A, Plante MM, Sánchez MG, Yong VW, Stys P, Tremblay ME, and Rivest S (2015) Inefficient clearance of myelin debris by microglia impairs remyelinating processes. Journal of Experimental Medicine (impact factor 10.79) 212: 481.

Lamantia CL, Tremblay ME, and Majewska AK (2014) Characterization of the BAC Id3-EGFP transgenic mouse line for in vivo imaging of astrocytes. Neurophotonics (impact factor 4.13) 1: 011014.

Kelly EA, Tremblay ME, Gahmberg CG, Tian L, and Majewska AK (2014) The subcellular localization of Intracellular adhesion molecule-5 (Telencephalin) in the visual cortex is not developmentally regulated in the absence of Matrix metalloproteinase-9. The Journal of Comparative Neurology (impact factor 3.40) 522: 676.

Marker DF*, Tremblay ME*, Puccini JM, Barbieri J, Gantz Marker MA, Loweth CJ, Muly EC, Lu SM, Goodfellow VS, Dewhurst S, and Gelbard HA (2013) The new small molecule mixed lineage kinase 3 inhibitor URMC-099 is neuroprotective and anti-inflammatory in models of HIV associated neurocognitive disorders. Journal of Neuroscience (impact factor 5.97) 33: 9998. *Equal contribution. Recommended by Faculty of 1000.

Horn KE, Glasgow SD, Gobert D, Bull SJ, Luk T, Girgis J, Tremblay ME, McEachern D, Bouchard JF, Haber M, Hamel E, Krimpenfort P, Murai KK, Berns A, Doucet G, Chapman CA, Ruthazer ES, and Kennedy TE (2013) DCC expression by neurons regulates synaptic plasticity in the adult brain. Cell Reports (impact factor 7.82) 3: 173.

Tremblay ME*, Zettel ML*, Ison JR, Allen PD, and Majewska AK (2012) Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices. GLIA (impact factor 5.85) 60: 541. *Equal contribution.

Lu SM, Tremblay ME, King I, Qi J, Reynolds H, Marker DF, Varrone J, Majewska AK, Dewhurst S, and Gelbard HA (2011) HIV-1 Tat-induced microgliosis and synaptic damage via interactions between peripheral and central myeloid cells. PLoS ONE (impact factor 2.77) 6: e23915. Recommended by Faculty of 1000.

Tremblay ME, Lowery RL, and Majewska AK (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biology (impact factor 9.16) 8: e1000527. Featured in New Scientist, News Feature of Nature (2012) 485: 570, Research Highlights of Nature (2010) 468: 136, Simons Foundation Autism Research Initiative, AlzForum, among others. Recommended by Faculty of 1000.

Marker DF*, Tremblay ME*, Lu SM, Majewska AK, and Gelbard HA (2010) A thin-skull window technique for chronic two-photon in vivo imaging of murine microglia in models of neuroinflammation. Journal of Visualized Experiments (impact factor 1.18) 43. doi:10.3791/2059. *Equal contribution.

Tremblay ME, Riad M, and Majewska AK (2010) Preparation of mouse brain tissue for immunoelectron microscopy. Journal of Visualized Experiments (impact factor 1.18) 41. doi:10.3791/2021.

Kelly EA, Tremblay ME, McCasland JS, and Majewska AK (2010) Postsynaptic deregulation in GAP-43 heterozygous mouse barrel cortex. Cerebral Cortex (impact factor 6.31) 20: 1696.

Bouvier D, Tremblay ME, Riad M, Corera AT, Gingras D, Horn KE, Fotouhi M, Girard M, Murai KK, Kennedy TE, McPherson P, Pasquale EB, Fon EA, and Doucet G (2010) EphA4 is localized in clathrin-coated and synaptic vesicles in adult mouse brain. Journal of Neurochemistry (impact factor 4.87) 113: 153.

Tremblay ME, Riad M, Chierzi S, Murai KK, Pasquale EB, and Doucet G (2009) Developmental course of EphA4 cellular and subcellular localization in the postnatal rat hippocampus. The Journal of Comparative Neurology (impact factor 3.40) 512: 798.

Bouvier D, Corera AT, Tremblay ME, Riad M, Chagnon M, Murai KK, Pasquale EB, Fon EA, and Doucet G (2008) Pre-synaptic and post-synaptic localization of EphA4 and EphB2 in adult mouse forebrain. Journal of Neurochemistry (impact factor 4.87) 106: 682.

Tremblay ME, Riad M, Bouvier D, Murai KK, Paquale EB, Descarries L, and Doucet G (2007) Localization of EphA4 in axon terminals and dendritic spines of adult rat hippocampus. The Journal of Comparative Neurology (impact factor 3.40) 501: 691.

Tremblay ME, Henry J, and Anctil M (2004) Spawning and gamete follicle rupture in the cnidarian Renilla koellikeri: effects of putative neurohormones. General and Comparative Endocrinology (impact factor 2.45) 137: 9.

 

 

Editorials and commentary

 

Tremblay ME (2020) A diversity of cell types, subtypes and phenotypes in the central nervous system: the importance of studying their complex relationships. Frontiers in Cellular Neuroscience – Non-neuronal cells (impact factor 3.90) 14: 628347.

Sharma K and Tremblay ME (2020) Microglia: multiple states and multiple roles in the normal and diseased brain and spinal cord. Neuroscience Letters (impact factor 2.27) 729: 135019.

Savage JC and Tremblay ME (2019) Studying laboratory mice -into the wild. Trends in Neurosciences (impact factor 12.89) 42: 566.

 

Addenda

 

Bisht K, Sharma K, Lacoste B, and Tremblay ME (2016) Dark microglia: Why are they dark? Communicative & Integrative Biology (no impact factor). 9: 5 e1230575.

Kelly EA, Tremblay ME, Gahmberg CG, Tian L, and Majewska AK (2013) Interactions between Adhesion Molecule-5 positive elements and their surroundings in the rodent visual cortex. Communicative & Integrative Biology (no impact factor) 6: 6 e27315.

Tremblay ME, Marker DF, Puccini JM, Muly EC, Lu SM, and Gelbard HA (2013) Ultrastructure of microglia-synapse interactions in the HIV-1 Tat-injected murine central nervous system. Communicative & Integrative Biology (no impact factor) 6: 6 e27670.

Tremblay ME and Majewska AK (2011) A role for microglia in synaptic plasticity? Communicative & Integrative Biology (no impact factor) 4: 2 220.

 

Invited Reviews

 

Bordeleau MFernandez De Cossio L, Chakravarty MM, and Tremblay ME (2020) From maternal diet to neurodevelopmental disorders: a story of neuroinflammation. Frontiers in Cellular Neuroscience – Non-neuronal cells (impact factor 3.90). In press.

Vecchiarelli H, Šimončičová E, and Tremblay ME (2020) Microglial involvement with psychiatric diseases. Psychiatric Times. In press.

Carrier M, Guilbert J, Lévesque JP, Tremblay ME, and Desjardins M (2020) Structural and functional features of the developing brain capillaries, and their alteration in schizophrenia. Frontiers in Cellular Neuroscience – Non-neuronal cells (impact factor 3.90). In press.

Subramanian J, Savage JC, and Tremblay ME (2020) Synaptic loss in Alzheimer’s disease: mechanistic insights provided by two-photon in vivo imaging of transgenic mouse models. Frontiers in Cellular Neuroscience (impact factor 3.90) 14: 592-607.

Tremblay ME, Madore C, Bordeleau M, Tian L, and Verkhratsky A (2020) Neuropathobiology of COVID-19: The role for glia. Frontiers in Cellular Neuroscience (impact factor 3.90) 14: 592214.

Carrier M, Robert ME, Gonzalez Ibanez F, Desjardins M, and Tremblay ME (2020) Imaging the neuroimmune dynamics across space and time. Frontiers in Cellular Neuroscience (impact factor 3.90) 14: 903.

Comer AL, Carrier M, Tremblay ME, and Cruz-Martin A (2020) The inflamed brain in schizophrenia: the convergence of genetic and environmental risk factors that lead to uncontrolled neuroinflammation. Frontiers in Cellular Neuroscience (impact factor 3.90) 14: 274.

Iovino L, Tremblay ME, and Civiero L (2020) Glutamate-induced excitotoxicity in Parkinson’s disease: the role of glial cells. Journal of Pharmacological Sciences (impact factor 2.84) 144: 151.

Awogbindin IO, Ishola IO, St-Pierre MK, Carrier M, Savage JC, Di Paolo T, and Tremblay ME (2020) Remodeling microglia to a protective phenotype in Parkinson’s disease? Neuroscience Letters (impact factor 2.27) 735: 135164.

St-Pierre KM, Šimončičová E, Bögi E, and Tremblay ME (2020) Shedding light on the dark side of the microglia. ASN Neuro (impact factor 4.17) 12: 1759091420925335. Highlighted in the Editor’s Choice Collection.

Inta D, Wölnerhanssen BK, Meyer-Gerspach AC, Lang E, Schweinfurth N, Mallien AS, Vasilescu AN, Schmidt A, Rea K, Westendorf AM, Tremblay ME, Sartorius A, Gass P, Cryan JF, Borgwardt S, and Lang UE (2020) Common pathways in depression and obesity: the role of the gut microbiome and diets. Current Behavioral Neuroscience Reports (no impact factor) 7: 15.

Garofalo S, Picard K, Limatola C, Nadjar A, Pascual O, and Tremblay ME (2020) Role of glia in the regulation of sleep in health and disease. Comprehensive Physiology (impact factor 6.25) 10: 687.

Bordeleau M, Carrier M, Luheshi GN*, and Tremblay ME* (2019) Microglia along sex lines: from brain colonization, maturation and function, to implication in neurodevelopmental disorders. Seminars in Cell and Developmental Biology (impact factor 6.69) 94: 152. *Equal contribution.

Stratoulias V, Venero JL, Tremblay ME, and Joseph B (2019) Microglia subtypes: diversity within the microglial community. The EMBO Journal (impact factor 10.56) 38: e101997.

Tremblay ME, Cookson MR, and Civiero L (2019) Glial phagocytic clearance in Parkinson’s disease. Molecular Neurodegeneration (impact factor 6.43) 14: 16.

Nichols MR, St-Pierre MK, Wendeln AC, Makoni NJ, Gouwens LK, Garrad EC, Sohrabi M, Neher JN, Tremblay ME, and Combs CK (2019) Inflammatory Mechanisms in Neurodegeneration. Journal of Neurochemistry (impact factor 4.87) 149: 562.

Lecours CBordeleau M, Cantin L, Parent M, Di Paolo T, and Tremblay ME (2018) Microglial implication in Parkinson’s disease: loss of beneficial physiological roles or gain of inflammatory functions. Frontiers in Cellular Neuroscience (impact factor 3.90) 12: 282.

Savage JCPicard KGonzalez Ibanez F, and Tremblay ME (2018) A brief history of microglial ultrastructure: distinctive features, phenotypes, and functions discovered over the past 60 years by electron microscopy. Frontiers in Immunology (impact factor 4.72) 9: 803.

Bisht KSharma K, and Tremblay ME (2018) Chronic stress as a risk factor for Alzheimer’s disease: roles of microglia-mediated synaptic remodeling, inflammation, and oxidative stress. Neurobiology of Stress (no impact factor yet) 9: 9.

Mallard C, Tremblay ME, and Vexler Z (2017) Microglia and neonatal brain injury. Neuroscience (impact factor 3.38). pii: S0306-4522.

Tay TL, Bechade C, D’Andrea I, St-Pierre MKHenry M, Roumier A, and Tremblay ME (2017) Microglia gone rogue: impacts on psychiatric disorders across the lifespan. Frontiers in Molecular Neuroscience (impact factor 3.72) 10: 421.

Nadjar A, Wigren HK, and Tremblay ME (2017) Roles of microglial phagocytosis and inflammatory mediators in the pathophysiology of sleep disorders. Frontiers in Cellular Neuroscience (impact factor 3.90) 11: 250.

Henry MS, Gendron L, Tremblay ME*, and Drolet G* (2017) Enkephalins: endogenous analgesics with an emerging role in stress resilience. Neural Plasticity (impact factor 3.16) 2017: 1546125. *Equal contribution.

Tian L, Hui CWBisht K, Tan Y, Sharma K, Chen S, Zhang X, and Tremblay ME (2017) Microglia under psychosocial stressors along the aging trajectory: Consequences on neuronal circuits, behavior, and brain diseases. Progress in Neuro-Psychopharmacology & Biological Psychiatry (impact factor 4.19) 79: 27.

Tay TL, Savage JCHui CWBisht K, and Tremblay ME (2017) Microglia across the lifespan: from origin to function in brain development, plasticity and cognition. The Journal of Physiology (impact factor 4.95) 595: 1929.

Tremblay MELecours CSamson L, Sánchez-Zafra V, and Sierra A (2015) From the Cajal alumni Achúcarro and Río-Hortega to the rediscovery of never-resting microglia. Frontiers in Neuroanatomy (impact factor 2.92) 9: 45.

Paolicelli RC, Bisht K, and Tremblay ME (2014) Fractalkine regulation of microglial physiology and consequences on the brain and behavior. Frontiers in Cellular Neuroscience (impact factor 3.90) 8: 129.

Sierra A, Beccari S, Diaz-Aparicio I, Encinas JM, Comeau S, and Tremblay ME (2014) Surveillance, phagocytosis, and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plasticity (impact factor 3.16) 2014: 610343.

Siskova Z and Tremblay ME (2013) Microglia and synapses: interactions in health and neurodegeneration. Neural Plasticity (impact factor 3.16) 2013: 425845.

Tremblay ME (2012) The role of microglia at synapses in the healthy CNS: novel insights from recent imaging studies. Neuron Glia Biology (impact factor 6.64) 7: 67.

Tremblay ME, Stevens B, Sierra A, Wake H, Bessis A, and Nimmerjahn A (2011) The role of microglia in the healthy brain. Journal of Neuroscience (impact factor 5.97) 31: 16064. Featured in UW-Madison School of Medicine and Public Health news and events. Recommended by Faculty of 1000.

Frigon A, Yakovenko S, Gritsenko V, Tremblay ME, and Barrière G (2008) Strengthening corticospinal connections with chronic electrical stimulation after injury. Journal of Neuroscience (impact factor 5.97) 28: 3262.

 

Book Chapters

 

Delage C, Rendina DN, Melacon KE, Tremblay ME, and Bilbo SD (2021) Sex differences in microglia as a risk factor for Alzheimer’s disease, in Sex and Gender Differences in Alzheimer’s Disease (Elsevier).

Delage C, Rendina DN, Melacon KE, Tremblay ME, and Bilbo SD (2021) Sex differences in microglia as a risk factor for Alzheimer’s disease, in Sex and Gender Differences in Alzheimer’s Disease (Elsevier).

Tay TL, Carrier M, and Tremblay ME (2019) Physiology of microglia, in Neuroglia in Neurodegenerative Diseases (Springer).

Savage JC, Carrier M, and Tremblay ME (2019) Morphology of microglia across contexts of health and disease, in Methods in Molecular Biology (Springer).

Tremblay ME and Majewska AK (2019) Ultrastructural analyses of microglial interactions with synapses, in Methods in Molecular Biology (Springer).

St-Pierre MK, Bordeleau M, and Tremblay ME (2019) Identifying dark microglia, in Methods in Molecular Biology (Springer).

Sierra A and Tremblay ME (2014) Chapter 1: Introduction, in Microglia in Health and Disease (Springer).

Tremblay ME, Paolicelli RC, Stevens B, Wake H, and Bessis A (2014) Chapter 9: Developing and mature synapses, in Microglia in Health and Disease (Springer).

Sierra A and Tremblay ME (2014) Chapter 10: Adult neurogenesis, learning and memory, in Microglia in Health and Disease (Springer).

Postdoctoral Fellows     2020 –

Haley Vecchiarelli
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CIHR Postdoctoral Fellowship

Michael Smith Foundation Research Trainee Award

My research interest is broadly how the immune system affects the brain to influence behaviour. My current work in Dr. Marie-Ève Tremblay's laboratory looks at how chronic stress influences microglia to produce cognitive deficits, using two-photon in vivo imaging, electron microscopy and behavioural analysis.

 

2021 –

Ifeoluwa O. Awogbindin
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CIHR Postdoctoral Fellowship

My project aims to determine the contribution of oligodendrocytes to the progression of Parkinson’s disease, and the implication of dark microglia in normal postnatal development and following maternal immune activation using confocal, STED and FIB-SEM imaging.

2021 – 2022

Benneth Ben-Azu
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Visiting

The hallmark of my PhD work was to elucidate the protective role of morin, a neuroactive flavonoid, in rodent models of schizophrenia. My postdoctoral fellowship in Dr. Marie-Ève Tremblay’s laboratory focuses on the neurodevelopmental molecular adjustments in double-hit mouse models of schizophrenia, and the consequences on microglial phenotypic remodeling.

2023 - 

Marianela Traetta

Postdoctoral Fellowship

Focus on different microglial states and functions during normal development and their involvement in neurodevelopmental disorders.

2023 - 

Adriano Chaves

UVic-Aspiration Postdoctoral Fellowship

 

Main goal is to investigate microglia-stimulating strategies to reinstate brain plasticity by the remodelling of the extracellular matrix. Interested in approaches that boost brain gamma waves, which are associated with the impressive antidepressant effect of ketamine.

PhD Students     2017 –

Fernando González Ibáñez
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Visiting student

My PhD project supervised by Dr. Marie-Ève Tremblay focuses on the impact of two environmental risk factors for disease (cigarette smoking, chronic psychological stress) on the brain and behaviour. My work focuses on microglia and their involvement in the remodeling of neuronal circuits as an underlying mechanism driving cognitive alteration. 2019 –

Micaël Carrier
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Visiting student

My project focuses on the origin of dark microglia (from the embryonic yolk sac or bone marrow) and characterizes, using a transgenic mouse model, the interactions of bone marrow-derived myeloid cells at synapses, with interest in applying this model to study schizophrenia. I am currently the trainee in charge of our laboratory's two-photon experiments. 2022 -  Jared VanderZwaag My project aims to understand the role of microglial reactivity in neurodevelopment and neuroplasticity and investigate the effects of pharmacological agents on microglia. 2023 Colin Murray   2020 – Eva Šimončičová My thesis project will focus on characterizing microglial changes along the aging trajectory. Older age-associated microglial variability will be further investigated in the context of susceptibility to infectious diseases and related consequences on cognitive functioning. MSc Students     2022 - Bianca Bobotis   2021 – Victor Lau My project will investigate further characterization of dark microglia with different staining and SEM microscopy methods. I also intend to look at senescent glia in Alzheimer’s patients brains, versus age-matched controls. 2022 -  Sophia Loewen My project is looking at the effects of helminth infection, Salmonella infection, and bile acid diet on the hippocampal region of mice. I will analyze microglial density, distribution and morphology to understand their physiological functions that are necessary for homeostasis and neuroprotection. Additionally, I will be looking at microglia’s ultrastructural features to understand their interactions with synapses. Undergrad Research Students     2020 –

Mohammadparsa Khakpour
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Undergrad student (Tremblay lab, Sep 2020 – Sep 2021)

Laboratory technician (Sep 2021 – )

My main duties are consist of conducting field research and other related activities to collect data and samples of animal populations, analyzing related data, assisting and performing other related Biological and biomedical experiments by applying different procedures and techniques, manuscript writing and training other lab members. 2021 -

Torin Halvorson
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NSERC Student (Tremblay lab, May –Aug 2021)
MD Student (Tremblay lab part-time, Aug 2021 –)

My research is investigating the characteristics of dark microglia, a class of highly active microglia associated with aging and neurodegenerative disease. My project seeks to isolate dark microglia and use cutting-edge proteomics and metabolomics analyses to better understand these cells and their roles in neurodegeneration. We ultimately aim to develop therapeutic strategies that target dark microglia to mitigate or reverse the effects of aging and disease. 2021 –

Chloe McKee
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Directed Studies Student (Tremblay lab, Jan – April 2021)

SURA Student (Tremblay lab, May –Aug 2021)

Honours Student and DMS JCURA Recipient (Tremblay lab, Sep 2021 – Apr 2022)

My research is investigating the effects of fractalkine receptor deficiency, a key receptor involved in microglia-neuron communication, on microglial diversity and ultrastructure in aged mice of the two sexes. My project uses transmission electron microscopy to image microglia in the hippocampal brain region, with a specific focuses on identifying dark microglia and quantifying ultrastructural features associated with cellular stress and ageing.   Makenna Gargus     Colby Sandberg     Cameo Volk     Michael Walkin     Mariem Mahmood     Keysa Mundel     Sean Foster     Maryam Zafarullah     Linnea Poyhia     Crisel Vital     Isabelle Coral   Former Students     2016 – 2021

Maude Bordeleau
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PhD

  2017 – 2021

Fanny Decoeur
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PhD, co-supervision

  2018 – 2020

Constantin Delmas
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PhD, co-supervision

  2019 – 2020 Marie-Ève Robert

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MSc

  2024-2029

Project Grant, CIHR

The impact of gestational cannabis exposure on brain and behavioural development: a study spanning fetal development to adulthood. Co-Investigator with PI Megha Mallar Chakravarty, and Co-Investigators Jibran Khokhar, José Ignacio Nazif-Munoz, and Brian Nieman. $983,025.

2024-26               

Universal Call Nº 06/2023, Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP)

Modulation of Dectin-1 receptors as a new neuroimmune strategy for the treatment of depression: animal model studies, International Co-Applicant with Principal Investigator (PI) Silvania Mendes Vasconcelos, and collaborators Adriano Chaves-Filho and Tatiana de Queiroz. R$200,000, approx. $54,000.     

2023-26               

Operating Grant, CIHR

Uncovering the role of chronic inflammation and serious respiratory infections in brain aging and cognitive impairment, Co-Investigator with PI Dawn Bowdish, and Co-Investigators Chris Verschoor, Katrina Choe, Michael Chong, Andrew Costa, Aaron Jones, Jeff Kwong and Candice Quin. $750,000.

2023-25               

Research Grant, European Leukodystrophy Association (ELA)

International, Alexander disease at the nanoscale in patient-derived brain organoids, Co-PI with Elly Hol. 100,000€.

2023-28               

Project Grant, CIHR

Role of adolescent ventral hippocampus in the development of corticolimbic system and behaviours related to neurodevelopmental disorders.  Co-Investigator with PI Lalit Srivastava, and Co-Investigators Mark Brendon and Tak Pan Wong. $925,625.

2023-28               

Project Grant, CIHR, The mitochondrial delta opioid receptor

Role, targeting and molecular mechanisms. Co-Investigator with PI Jean-Luc Parent and Co-PI Louis Gendron, as well as Co-Investigator Étienne Hébert Châtelain. $952,426.

2023-25               

Research Agreement with the Vagus Nerve Society

Non-invasive Vagus Nerve Stimulation and the Prevention of Maternal Immune Activation-Induced Autism and Schizophrenia Phenotypes in the Offspring, PI. $55,000.

2023-24               

Project Grant, CIHR

Role of adolescent ventral hippocampus in the development of corticolimbic system and behaviors related to neurodevelopmental disorders. Co-Investigator with PI Lalit Srivastava, and Co-Investigators Mark Brandon and Tak Pan Wong. Bridge Funding, $100,000.

2023-24               

Project Grant, CIHR

Reelin, sex, depression, and development of novel pharmacotherapy and biomarkers. Co-Investigator with PI Hector Caruncho and Co-Investigators Lisa Kalynchuk and Olav Krigolson. Bridge Funding, $100,000.

2023-24               

Project Grant, CIHR, The impact of gestational cannabis exposure on brain and behavioural development

A study spanning fetal development to adulthood. Co-Investigator with PI Mallar Chakravarty and Co-Investigators Rosemary Bagot, Jibran Kokhar, and Brian Nieman. Bridge Funding, $100,000.

2023 

National Research Council of Canada’s Industrial Research Assistance Program in partnership with Cyclenium Pharma Inc.

Lead discovery to PTSD in-vivo Proof-of-Concept, Subcontractor with Helmut Thomas (PI). $180,000.

2022-26               

Joint Canada-Israel Research Program, Canadian Institutes of Health Research (CIHR), the International Development Research Center (IDRC), the Israel Science Foundation (ISF), and the Azrieli Foundation

Investigating the outcomes of senescence on microglial physiological and immune functions: implications for viral infection and Alzheimer’s disease pathology along the aging trajectory, PI with Dan Frenkel (Co-PI) and Benneth Ben-Azu (Co-PI). $1,500,000.

2022

Pilot Grant, Parkinson Canada

COVID-19 and Parkinson’s disease in a mouse model, Co-investigator with Thérèse Di Paolo (PI) and Guy Boivin (Co-investigator). $75,000.

2021-26               

Project Grant, CIHR, Investigating dark microglia during normal postnatal development and following maternal immune activation

PI with Maciej Lalowski, Luca Peruzzotti-Jametti and Leigh Anne Swayne (Co-investigators). $1,051,876.

2021

Operating Grant, CIHR, Emerging COVID-19 Research Gaps and Priorities Funding Opportunity

Understanding and treating the adverse effects of COVID-19 on the brain. Co- PI with Leigh Anne Swayne (PI) and Darwyn Kobasa (Co-investigator), $293,000.

2021-22

FRAXA Fellowship Grant, FRAXA Research Foundation

Contribution of microglia to the therapeutic effects of metformin and adiponectin in Fragile-X syndrome. Co-principal investigator with Brian Christie (PI), US$90,000.

2021 

Research Contract with Med-Life Discoveries LP.

PI, $20,000.

2021-26

Project Grant, CIHR, Bringing focus to the invisible injury

Defining a role for microbleeds and microglia in mild traumatic brain injury. Co-investigator with Brian Christie (PI) and Patrick Nahirney (Co-investigator), $967,725.

2021

University of Victoria Research Accelerator Fund Grant

Understanding the adverse effects of SARS-CoV-2 infection on the brain, Co-investigator with PI Leigh Anne Swayne, $30,000.

2020-23               

Swiss National Science Foundation “Sinergia” Grant

Understanding gut-brain interactions and the effect of dietary measures in obesity and depression: a translational study. Project Partner with Dragos Inta (PI), Bettina Wölnerhanssen (Co-investigator), Stefan Borgwardt (Co-investigator), and John F. Cryan (Co-investigator), CHF 2,602,315.

2020-25

John R. Evans Leaders Fund and Infrastructure Operating Fund, Canada Foundation for Innovation

Laboratory of ultrastructural insights into the neurobiology of aging and cognition, Principal Investigator (PI), $1,237,500

2019-23

Swiss National Science Foundation “Sinergia” Grant

Understanding gut-brain interactions and the effect of dietary measures in obesity and depression: a translational study. Project Partner with Dragos Inta (PI), Bettina Wölnerhanssen (Co-investigator), Stefan Borgwardt (Co-investigator), and John F. Cryan (Co-investigator), CHF 2,602,315

2019-20

ThéCell (Québec Cell, Tissue and Gene Therapy Network)-CMDO (Cardiometabolic Health, Diabetes and Obesity Research Network) Inter-Network Initiative

Caractérisation de la variabilité fonctionnelle des cellules souches mésenchymateuses humaines dérivées des tissus adipeux de patients sains ou dysmétaboliques, Co-Investigator with Mohammad-Ali Jenabian, André Tchernof (PI) and Julie Fradette (PI), $20,000

2018-21

Fonds de recherche du Québec en nature et technologies (FRQNT) Team Grant

La régulation de la fonction mitochondriale par l’AMPc, une nouvelle stratégie pour améliorer la qualité de vie des ovocytes lors de la maturation in vitro, Co-Investigator with François Richard (PI) and Marc Germain, $205,740

2018-21

ERANET-Neuron Synaptic Dysfunction in Disorders of the Central Nervous System

Microglial control of synaptic function in stress response and vulnerability to depression, Coordinator and PI with Igor Branchi, Martin Fuhrmann, Maciej Lalowski, Bozena Kaminska, and Valeria Mondelli, €1,213,000

2017-20

Heart and Stroke Foundation of Canada, Grant-in-Aid

Rho-kinase2 inhibition as an early intervention after ischemic stroke to modulate cerebrovascular plasticity and promote functional recovery, Co-Investigator with Baptiste Lacoste (PI) and Jean-Claude Béïque (Co-Investigator), $259,000

2016-21

CIHR Foundation Scheme Grant

Targeting microglia-synapse interactions to rescue from brain circuits elimination and cognitive dysfunction, PI with Program Expert Lisa Topolnik, $953,000

2015-20

Operating grant, CIHR

Role of developing hippocampus in organizing prefrontal cortical functions, Co-Investigator with Lalit Srivastava (PI) and Tak Wong (Co-Investigator), $667,165

2014-22

Natural Sciences and Engineering Research Council of Canada (NSERC)

Microglia-synapse interactions: their roles in the brain’s adaptation to environmental challenges, PI, $312,000


Neuroscience Graduate Program