The DeNardo Lab

Our brains integrate environmental cues with memories of past experiences to select appropriate behavioral responses. The medial prefrontal cortex (mPFC) plays a key role in analyzing the emotional significance of stimuli and promoting adaptive responses. We are particularly interested in how mPFC controls adaptive threat responding. mPFC is broadly interconnected with the limbic system, association cortices, and neuromodulatory systems, and individual mPFC connections have been linked to specific behaviors. However, little is known about the specific connectivity and function of mPFC neurons that contribute to distinct adaptive behaviors. Furthermore, mPFC undergoes a prolonged development that renders its circuitry vulnerable to genetic and environmental insults occurring early in life. As a result, mPFC dysfunction is linked to numerous psychiatric diseases including fear and anxiety disorders and depression. Yet remains it unclear how mPFC circuits develop and how their maturation can be perturbed by disease risk factors. We will address these questions using cutting-edge tools in systems- and cellular-level Neuroscience. We are seeking enthusiastic and motivated scientists to join the team!

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organization of mpfc circuits that give rise to adaptive behaviors

Using optogenetics, viral tracing, and the TRAP2 mouse for activity-dependent genetic labeling, we define the causal function and underlying connectivity of mPFC neurons that contribute to learned threat responses across the lifespan.

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mapping the activity patterns underlying ADAPTIVE AND MALADAPTIVE THREAT RESPONSES

Using the fiber photometry and UCLA Miniscopes, we explore mPFC activity patterns underlying learned threat responses including avoidance and conditioned fear in the mouse.

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how are mpfc circuits for adaptive behaviors wired during development?

Using RNAseq and viral tracing coupled to cell-type specific gene knockout, we will identify molecular cues that wire mPFC fear circuits during development, and ultimately explore the consequences of genetic mutations that increase risk for disease.

Publications

2023

Gongwer MW*, Klune CB*, Couto J, Jin B, Enos A, Chen R, Friedmann D, DeNardo LA. Brain-wide projections and differential encoding of prefrontal projection neurons underlying learned and innate threat avoidance (2023) The Journal of Neuroscience 43 (32) 5810-5830

Yang T, Bayless DW, Wei Y, Landayan D, Marcelo IM, Wang Y, DeNardo LA, Luo L, Druckmann S, Shah NM. Hypothalamic neurons that mirror aggression (2023) Cell 186, 1195-1121

2022

Qian K, Tol MJ, Wu J, Uchiyama LF, Xiao X, Cui L, Bedard AX, Weston TA, Rajendran PS, Vergnes L, Shimanaka Y, Yin Y, Jami-Alahmadi Y, Cohn W, Bajar BT, Lin CH, Jin B, DeNardo LA, Black DL, Whitelegge JP, Wohlschlegel JA, Reue K, Shivkumar K, Chen FJ, Young SG, Li P, Tontonoz P. CLSTN3B enforces adipocyte multilocularity to facilitate lipid utilization (2022) Nature 7942, 160-168

Chang YT, Kowalczyk M, Fogerson PM, Lee YJ, Haque M, Adams EL, Wang DC, DeNardo LA, Tessier-Lavigne M, Huguenard JR, Luo L, Huang WH. Loss of Rai1 enhances hippocampal excitability and epiloptogenesis in mouse models of Smith-Magenis syndrome (2022) PNAS 119 (43) e2210122119

Gabriel CJ, Zeidler Z, Jin B, Guo C, Goodpaster CG, Kashay AQ, Wu A, Delaney M, Cheung J, DiFazio LE, Sharpe MJ, Aharoni D, Wilke SA, DeNardo LA. BehaviorDEPOT: a simple, flexible tool for automated behavioral detection based on markerless pose tracking (2022) eLife https://elifesciences.org/articles/74314

Blagburn-Blanco SV, Chapelle MS, De Biase LM# and DeNardo LA#. Synapse-specific roles for microglia in development: New horizons in the prefrontal cortex (2022) Frontiers in Molecular Neuroscience https://doi.org/10.3389/fnmol.2022.965756

Osterhout JA, Kapoor V, Eichhorn SW, Vaughn E, Moore JD, Liu D, Lee D, DeNardo LA, Luo L, Zhang X, Dulac C. A preoptic neuron population controls fever and appetite during sickness (2022) Nature 6060, 937-944 https://doi.org/10.1038/s41586-022-04793-z

2021

Choe KY, Bethlehem RAI, Safrin M, Dong H, Salman E, Li Y, Grinevich V, Golshani P, DeNardo LA, Penagarikano O, Harris NG, Geschwind DH. Oxytocin normalizes altered circuit connectivity for social rescue of the Cntnap2 knockout mouse (2021) Neuron https://doi.org/10.1016/j.neuron.2021.11.031

Klune CB*, Jin B*, DeNardo LA. Linking mPFC circuit maturation to the developmental regulation of emotional memory and cognitive flexibility (2021) eLife 2019;8:e49041 DOI: 10.7554/eLife.49041

2020

Tasaka G, Feigin L, Maor I, Groysman M, DeNardo LA, Schiavo JK, Froemke RC, Luo L, Mizrahi A. The temporal association cortex plays a key role in auditory-driven maternal plasticity (2020) Neuron https://doi.org/10.1016/j.neuron.2020.05.004

Lee HS, Yamazaki R, Wang D, Arthaud S, Fort P, DeNardo LA, Luppi PH. Targeted recombination in active populations as a new mouse genetic model to study sleep-active neuronal populations: Demonstration that Lhx6+ neurons in the ventral zona incerta are activated during paradoxical sleep hypersomnia (2020) Journal of Sleep Research https://doi.org/10.1111/jsr.12976

2019

DeNardo LA, Liu CD, Allen WE, Adams EL, Friedmann D, Fu LX, Guenthner CJ, Tessier-Lavigne M, Luo L. Temporal Evolution in Cortical Ensembles Mediating Remote Memory Retrieval (2019) Nature Neuroscience https://doi.org/10.1038/s41593-018-0318-7

2018

Berns DS, DeNardo LA, Pederick D, Luo L Teneurin-3 controls topographic circuit assembly in the hippocampus (2018). Nature 15, 328-333.

2017

Savas JN, Wang YZ, DeNardo LA, Martinez-Bartolome S, McClatchy DB, Hark TJ, Shanks NF, Cozzolino KA, Lavallée-Adam M, Park SK, Kelly JW, Koo EH, Nakagawa T, Masliah E, Ghosh A, Yates 3rd JR (2017) Amyloid accumulation drives proteome-wide alterations in mouse models of Alzheimer's disease like pathology. Cell Reports 21, 2614-2627.

Allen WE*, DeNardo LA*, Chen MZ*, Liu CD, Loh KM, Fenno LE, Ramakrishnan C, Deisseroth K, Luo L (2017) Thirst-Associated Preoptic Neurons Encode an Aversive Motivational Drive. Science 357, 1149–1155.

DeNardo L, Luo L. (2017) Genetic Strategies to Access Activated Neurons. Current Opinion in Neurobiology 45, 121-129. 

2015

DeNardo LA*, Berns DS*, DeLoach KE, Luo L (2015) Connectivity of Mouse Somatosensory and Prefrontal Cortex Examined with Trans-synaptic Tracing. Nature Neuroscience 18, 1687-97.

Savas JN, Ribeiro LF, Wierda KD, Wright R, DeNardo-Wilke LA, Chamma I, Wang Yi-Zhi, Zemla R, Lavallee-Adam M, Vennekens KM, O’Sullivan ML, Antonios JK, Hall EA, Thoumine O, Attie AD, Yates JR, Ghosh A, De Wit J (2015) The Sorting Receptor SorCS1 Regulates Trafficking of Neurexin and AMPA receptors. Neuron 87, 764-80.

2012

DeNardo LA, de Wit J, Otto S, Ghosh A (2012) NGL-2 regulates input-specific synapse development in CA1 pyramidal neurons. Neuron 76, 762-75.

Wilke SA, Hall BJ, Antonios JK, DeNardo LA, Otto S, Yuan B, Chen F, Tiglio K, Williams ME, Qiu Z, Ghosh A (2012) NeuroD2 Regulates the Development of Hippocampal Mossy Fiber Synapses. Neural Development 7:9.