Minghong Ma Lab

Publications

(^†equal contribution; *corresponding author)

2025

Sniffen SE, Ryu SE, Kokoska MM, Bhattarai J, Wang Y, Thomas ER, Skates GM, Johnson NL, Chavez AA, Iaconis SR, Janke E, Zhang Y-F, Ma M, Wesson DW* (2025). Directing negative emotional states through parallel genetically-distinct basolateral amygdala pathways to ventral striatum subregions. Mol Psychiatry, in press.

Sun Y, Wang X, Zhang DY, Zhang Z, Bhattarai JP, Wang Y, Dong W, Zhang F, Park KH, Galanaugh J, Sambangi A, Yang Q, Kim SH, Wheeler G, Goncalves T, Wang Q, Geschwind D, Kawaguchi R, Wang H, Xu F, Binder ZA, Chen IH, Pai EL, Stone S, Nasrallah M, Christian KM, Fuccillo M, O'Rourke DM, Ma M, Ming GL*, Song H* (2025). Brain-wide neuronal circuit connectome of human glioblastoma. Nature, 641:222-231.

Johnson NL, Cotelo-Larrea A, Stetzik LA, Akkaya UM, Zhang Z, Gadziola MA, Varga AG, Ma M, Wesson DW* (2025) Dopaminergic signaling to ventral striatum neurons initiates sniffing behavior. Nature Commun, 16:336.

2024

Choi A, Smith J, Wang Y, Shin H, Kim B, Wiest A, Jin X, An I, Hong J, Antila H, Thomas S, Bhattarai JP, Beier K, Ma M, Weber F, Chung S* (2024). Circuit mechanism underlying fragmented sleep and memory deficits in 16p11.2 deletion mouse model of autism. iScience. 27:111285.

Yu H, Nagi SS, Usoskin D, Hu Y, Kupari J, Bouchatta O, Yan H, Cranfill SL, Gautam M, Su Y, Lu Y, Wymer J, Glanz M, Albrecht P, Song H, Ming GL, Prouty S, Seykora J, Wu H, Ma M, Marshall A, Rice FL, Li M, Olausson H*, Ernfors P*, Luo W*. (2024) Leveraging deep single-soma RNA sequencing to explore the neural basis of human somatosensation. Nat Neurosci, 27:2326-2340.

Gautam M, Yamada A, Yamada AI, Wu Q, Kridsada K, Ling J, Yu H, Dong P, Ma M, Gu J*, Luo W* (2024) Distinct local and global functions of mouse Aβ low-threshold mechanoreceptors in mechanical nociception. Nature Commun, 15:2911.

Yang K^†, Hasegawa Y^†, Bhattarai JP, Hua J, Dower M, Etyemez S, Prasad N, Duvall L, Paez A, Smith A, Wang Y, Zhang YF, Lane AP, Ishizuka K, Kamath V, Ma M, Kamiya A, Sawa A* (2024) Inflammation-related pathology in the olfactory epithelium: its impact on the olfactory system in psychotic disorders. Mol Psychiatry, 29:1453-1464.

2023

Yang K*, Ayala-Grosso C, Bhattarai JP, Sheriff A, Takahashi T, Cristino AS, Zelano C, Ma M* (2023). Unraveling the Link between Olfactory Deficits and Neuropsychiatric Disorders. J Neurosci, 43:7501-7510. (Review)

Zhang Y-F*, Wu J^†, Wang Y^†, Johnson NL^†, Bhattarai JP^†, Li G, Wang W, Guevara Espitia C, Shoenhard H, Fuccillo MV, Wesson DW, Ma M* (2023) Ventral striatal islands of Calleja neurons bidirectionally mediate depressive behaviors in mice. Nature Commun, 14: 6887.

Cansler HL*, in’t Zandt EE, Carlson KS, Khan WT, Ma M, Wesson DW (2023) Organization and engagement of a prefrontal-olfactory network during olfactory selective attentions. Cerebral Cortex, 33:1504-1526.

Janke E, Bhattarai JP, Ma M* (2023). Intranasal Pressure Recording for Monitoring Mouse Respiration. Methods Mol Biol. 2710:49-60. (Book chapter)

2022

Janke E*, Zhang M, Ryu SE, Bhattarai JP, Schreck MR, Moberly AH, Luo W, Ding L, Wesson DW, Ma M* (2022) Machine learning-based clustering and classification of mouse behaviors via respiratory patterns. iScience, 25:105625.

Yu H*, Xiong J, Ye AY, Cranfill SL, Cannonier T, Gautam M, Zhang M, Bilal R, Park JE, Xue Y, Polam V, Vujovic Z, Dai D, Ong W, Ip J, Hsieh A, Mimouni N, Lozada A, Sosale M, Ahn A, Ma M, Ding L, Arsuaga J, Luo W* (2022) Scratch-AID, a deep learning-based system for automatic detection of mouse scratching behavior with high accuracy. eLife, 11:e84042.

Johnson NL, Patten T, Ma M, De Biasi M*, Wesson DW* (2022). Chemosensory contributions of e-cigarette additives on nicotine use. Front Neurosci,16:893587. (Review)

Hasegawa Y, Ma M, Sawa A, Lane AP*, Kamiya A* (2022). Olfactory impairment in psychiatric disorders: Does nasal inflammation impact disease psychophysiology? Transl Psychiatry,12(1):314. (Review)

Xu R^†, Cong X^†, Zheng Q, Xu L, Ni MJ, de March CA, Matsunami H, Golebiowski G, Ma M*, Yu Y* (2022) Interactions among key residues regulate mammalian odorant receptor trafficking. FASEB J, 36:e22384.

Zhang YF*, Janke E, Bhattarai JP, Wesson DW, Ma M* (2022) Self-directed orofacial grooming promotes social attraction in mice via chemosensory communication. iScience, 25:104284.

Schreck MR*, Zhuang L, Janke E, Moberly AH, Bhattarai JP, Gottfried JA, Wesson DW, Ma M* (2022) State-dependent olfactory processing in freely behaving mice. Cell Reports, 38:110450.

Cui L, Guo J, Cranfill SL, Gautam M, Bhattarai J, Olson W, Beattie K, Challis RC, Wu Q, Song X, Raabe T, Gradinaru V, Ma M, Liu Q*, Luo W* (2022). Glutamate in primary afferents is required for itch transmission. Neuron,110:809-823.

Beattie K, Jiang H, Gautam M, MacVittie MK, Miller B, Ma M, Liu Q, Luo W* (2022). TRPC3 Antagonizes Pruritus in a Mouse Contact Dermatitis Model. J Invest Dermatol, 142:1136-1144.

Kulason S, Ratnanather JT, Miller MI, Kamath V, Hua J, Yang K, Ma M, Ishizuka K, Sawa A* (2022). A comparative neuroimaging perspective of olfaction and higher-order olfactory processing: on health and disease. Sem Cell Dev Biol, 129:22-30. (Review)

Bhattarai JP, Etyemez S, Jaaro-Peled H, Janke E, Leon Tolosa UD, Kamiya A, Gottfried JA, Sawa A*, Ma M* (2022). Olfactory modulation of the medial prefrontal cortex circuitry: Implications for social cognition. Sem Cell Dev Biol, 129:31-39. (Review)

2021

Zhang YF, Vargas Cifuentes L^†, Wright KN^†, Bhattarai JP^†, Mohrhardt J^†, Fleck D^†, Janke E, Jiang C, Cranfill SL, Goldstein N, Schreck M, Moberly AH, Yu Y, Arenkiel BR, Betley JN, Luo W, Stegmaier J, Wesson DW*, Spehr M*, Fuccillo MV*, Ma M* (2021) Ventral striatal islands of Calleja neurons control grooming in mice. Nature Neurosci, 24:1699-1710.

Wang L^†, Ren W^†, Li X, Zhang X, Tian H, Bhattarai JP, Challis RC, Lee AC, Zhao S, Yu H, Ma M*, Yu Y* (2021) Chitinase-Like Protein Ym2 (Chil4) Regulates Regeneration of the Olfactory Epithelium via Interaction with Inflammation. J Neurosci, 41:5620-5637. [Cover story].

Schreck M, Ma M* (2021) Sensory neuroscience: Early value-based odor categorization. Current Biology, 31: R396-R398. (Comment on Kudryavitskaya et al., Flexible categorization in the mouse olfactory bulb. Curr. Biol. 2021; 31:1616-1631)

2018-2020

Bhattarai JP*, Schreck M, Moberly AH, Luo W, Ma M* (2020). Aversive learning increases release probability of olfactory sensory neurons. Current Biology, 30:31-41.

White KA^†, Zhang YF^†, Zhang Z^†, Bhattarai JP, Moberly AH, In 't Zandt E, Peña-Bravo JI, Mi H, Jia X, Fuccillo MV, Xu F, Ma M, Wesson DW* (2019). Glutamatergic neurons in the piriform cortex influence the activity of D1 and D2-type receptor expressing olfactory tubercle neurons. J Neurosci, 39:9546-9559.

Abdus-Saboor I^†, Fried NT^†, Lay M, Dong P, Burdge J, Lu M, Ma M, Dong X, Long D, Luo W* (2019). Development of a Mouse Pain Scale Using Sub-second Behavioral Mapping and Statistical Modeling. Cell Reports, 28:1623-1634.e4.

Moberly AH^*, Schreck M, Bhattarai JP, Zweifel LS, Luo W, Ma M^* (2018) Olfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior. Nature Commun, 9:1528.

Grosmaitre X*, Ma M* (2018). Odor-induced electrical and calcium signals from olfactory sensory neurons in situ.  In Olfactory Receptors: Methods and Protocols. Springer. (Method)

2016-2017

Dong P, Guo C, Huang S, Ma M, Liu Q*, Luo W* (2017) TRPC3 is dispensable for β-Alanine triggered acute itch. Scientific Reports, 7:13869.

Olson W, Abdus-Saboor I, Cui L, Burdge J, Raabe T, Ma M, Luo W* (2017) Sparse genetic tracing reveals regionally specific functional organization of mammalian nociceptors. eLife, 29507. doi: 10.7554/eLife.29507.   

Yu Y^†*, Moberly AH^†, Bhattarai JP, Duan C, Zheng Q, Li F, Huang H, Olson W, Luo W, Wen T, Yu H, Ma M* (2017). The stem cell marker Lgr5 defines a subset of post‐mitotic neurons in the olfactory bulb. J Neurosci, 37: 9403-9414.

Efimova N, Korobova F, Stankewich MC, Moberly AH, Stolz DB, Wang J, Kashina A, Ma M, Svitkina T* (2017) βIII spectrin is necessary for formation of the constricted neck of dendritic spines and regulation of synaptic activity in neurons. J Neurosci, 37: 6442-6459.

Ma M, Leinders-Zufall T* (2017). Olfactory sensory neurons of the peripheral olfactory system. Reference Module in Neuroscience and Biobehavioral Psychology. Elsevier, pp.1-7. ISBN 9780128093245. http://dx.doi.org/10.1016/B978-0-12-809324-5.02899-6

Cui L, Miao X, Liang L, Abdus-Saboor I, Olson W, Fleming MS, Ma M, Tao YX*, Luo W* (2016) Identification of early RET+ deep dorsal spinal cord interneurons in gating pain. Neuron, 91: 1137-53.  

Challis RC*, Tian H, Yin W, Ma M* (2016) Genetic ablation of Type III adenylyl cyclase exerts region-specific effects on cilia architecture in the mouse nose. Plos One, 11: e0150638.

Challis RC, Ma M* (2016). Sour taste finds closure in a potassium channel. Proc Natl Acad Sci U S A., 113:246-247. (Comment on Ye et al. (2016) The K⁺ channel Kir2.1 functions in tandem with proton influx to mediate sour taste transduction. PNAS, 113:E229-238).

2014-2015

Yu Y^†, de March CA^†, Ni MJ, Adipietro KA, Golebiowski J*, Matsunami H*, Ma M* (2015). Responsiveness of G-protein coupled odorant receptors is partially attributed to the activation mechanism. Proc Natl Acad Sci U S A, 112: 14966-14971.

Challis RC, Wang J, Tian H, He J, Jiang J, Chen X, Connelly T, Ma L, Yin W, Yu CR, Pluznick JL, Storm DR, Huang L, Zhao K, Ma M* (2015). An olfactory cilia pattern in the mammalian nose ensures high sensitivity to odors. Current Biology, 25: 2503-2512.  [Commented by Wall CM and Zhao H (2015) Sensory Biology: Novel Peripheral Organization for Better Smell. Current Biology. 25: R833-6]

de March CA^†, Yu Y^†, Ni MJ, Adipietro KA, Matsunami H*, Ma M*, Golebiowski J* (2015). Conserved residues control activation of mammalian G protein-coupled odorant receptors. J Am Chem Soc, 137: 8611-8616.

Jiang Y^†, Li Y^†, Tian H, Ma M*, Matsunami H* (2015). Muscarinic acetylcholine receptor M3 modulates odorant receptor activity via inhibition of β-Arrestin-2 recruitment. Nature Commun, 6: 6448.

Connelly T^†, Yiqun Yu^†, Grosmaitre X, Wang J, Santarelli LC, Savigner A, Qiao X, Wang Z, Storm DR, Ma M* (2015). G Protein-coupled odorant receptors underlie mechanosensitivity in mammalian olfactory sensory neurons. Proc Natl Acad Sci U S A, 112:590-595.

Ma M*, Fleischer J, Breer H, Eisthen H (2015). The septal organ, Grueneberg ganglion, and terminal nerve. Chapter 52. In: Handbook of Olfaction and Gustation. Ed. Richard Doty. Published by John Wiley & Sons, Inc. (Book chapter)

Omura M, Grosmaitre X, Ma M, Mombaerts P* (2014). The b2-adrenergic receptor as a surrogate odorant receptor in mouse olfactory sensory neurons. Mol Cell Neurosci, 58:1-10.

2010-2013

Zhao S, Tian H, Ma L, Yuan Y, Yu RC, Ma M* (2013) Activity-dependent modulation of odorant receptor gene expression in the mouse olfactory epithelium. Plos One, 8:e69862.

Connelly T, Savigner A, Ma M* (2013) Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors. J Neurophysiol, 110:55-62.

He J, Tian H, Lee AC, Ma M* (2012) Postnatal experience modulates functional properties of mouse olfactory sensory neurons. Eur J Neurosci, 36:2452-60. [Cover Figure]

Duan X, Block E, Li Z, Connelly T, Zhang J, Huang Z, Su X, Pan Y, Wu L, Chi Q, Thomas S, Zhang S, Ma M, Matsunami H*, Chen GQ, Zhuang H*. (2012) Crucial role of copper in detection of metal-coordinating odorants. Proc Natl Acad Sci U S A, 109:3492-7.

Ma M* (2012). Odor and pheromone sensing via chemoreceptors. Adv Exp Med Biol. 739:93-106. (Review)

Lee AC, He J, Ma M* (2011) Olfactory marker protein is critical for functional maturation of olfactory sensory neurons and development of mother preference. J Neurosci, 31:2974-2982.

Tan J, Savigner A, Ma M, Luo M* (2010) Odor information processing by the olfactory bulb analyzed in gene-targeted mice. Neuron, 65: 912-926.

Ma M* (2010). Multiple olfactory subsystems convey various sensory signals. In The Neurobiology of Olfaction, ed. by A Menini. Published by CRC Press, pp225-240. (Book chapter)

2003-2009

Grosmaitre X, Fuss SH, Lee AC, Adipietro KA, Matsunami H, Mombaerts P, Ma M* (2009) SR1, a mouse odorant receptor with an unusually broad response profile. J Neurosci, 29: 14545-14552.

Lee AC, Tian H, Grosmaitre X, Ma M* (2009) Expression patterns of odorant receptors and response properties of olfactory sensory neurons in aged mice. Chem Senses, 34: 695-703.

Savigner A*, Duchamp-Viret P, Grosmaitre X, Chaput M, Garcia S, Ma M, Palouzier-Paulignan B (2009): Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin. J Neurophysiol, 101: 2898-2906.

Zhao L, Ding T, Cyrus T, Cheng Y, Tian H, Ma M, Falotico R, Praticò D* (2009) Low-dose oral sirolimus reduces atherogenesis and vascular inflammation and induces plaque stabilization in mice lacking the low-density lipoprotein receptor. Brit J Pharmacol, 156: 774-785.

Leinders-Zufall T*, Ma M (2009). Olfactory epithelium. In: Encyclopedia of Neuroscience, 4th edition.  Squire L, Albright T, Bloom F, Gage F, Spitzer N (eds), pp. 113-118, Elsevier Science, Amsterdam.

Tian H, Ma M* (2008b) Activity plays a role in eliminating olfactory sensory neurons expressing multiple odorant receptors in the mouse septal organ. Mol Cell Neurosci, 38: 484-488.

Tian H, Ma M* (2008a). Differential development of odorant receptor expression patterns in the olfactory epithelium: a quantitative analysis in the mouse septal organ. Dev Neurobiol, 68: 476-486.

Liu N*, Crasto CJ, Ma M (2007) Integrated olfactory receptor and microarray gene expression databases. BMC Bioinformatics, 8:231.

Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M* (2007) Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nature Neurosci, 10: 348-354. [Featured in RESEARCH HIGHLIGHTS in Nature (March 1, 2007), 446:5]

Ma M* (2007). Encoding olfactory signals via multiple chemosensory systems. Critical Reviews in Biochemistry and Molecular Biology, 42: 463-480. (Review)

Grosmaitre X, Vassalli A, Mombaerts P, Shepherd GM, Ma M* (2006). Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc Natl Acad Sci, USA, 103: 1970-1975. [Featured in “In This Issue” by PNAS]

Ma M* (2005). Olfactory system coding.  In: Yearbook of Science and Technology. Published by McGraw-Hill, pp240-244.

Tian H, Ma M* (2004) Molecular organization of the olfactory septal organ. J Neurosci, 24: 8383-8390.

Zhang X, Rogers M, Tian H, Zhang X, Zou D, Liu J, Ma M, Shepherd GM, Firestein SJ* (2004) High-throughput microarray detection of odorant receptor gene expression in the mouse. Proc Natl Acad Sci, USA, 101, 14168-14173.

Ma M*, Grosmaitre X, Iwema C, Baker H, Greer CA, Shepherd GM (2003) Olfactory signal transduction in the mouse septal organ. J Neurosci, 23: 317-324.

Before 2003

Ma M*, Shepherd GM (2001). Recording from vertebrate olfactory receptor neurons: from isolated cells to intact epithelial preparations. In Methods and Frontiers in Chemosensory Research, ed. by Sidney A Simon and Miguel AL Nicolelis. Published by CRC Press, pp65-77. (Method)

Ma M*, Shepherd GM (2000) Functional mosaic organization of mouse olfactory receptor neurons. Proc Natl Acad Sci, USA, 97, 12869-12874.

Ma M*, Chen WR, Shepherd GM (1999) Electrophysiological characterization of rat and mouse olfactory receptor neurons from an intact epithelial preparation. J Neurosci Methods, 92: 31-40.

Leinders-Zufall T^†, Ma M^†, Zufall F* (1999) Impaired odor adaptation in olfactory receptor neurons after inhibition of Ca²⁺/calmodulin kinase II. J Neurosci, RC19: 1-6.

Ma M, Koester J* (1996) The role of K+ currents in frequency-dependent spike broadening in Aplysia R20 neurons: A dynamic clamp analysis. J Neurosci, 16: 4089-4101.

Ma M, Koester J* (1995) Consequences and mechanisms of spike broadening of R20 cells in Aplysia californica. J Neurosci, 15: 6720-6734.

Sun JS*, Li B, Ma MH, Diao YC* (1994) Transcallosal circuitry revealed by blocking and disinhibiting callosal input in the cat. Vis Neurosci, 11: 189-197.

Li B, Sun JS, Ma MH, Diao YC* (1993) The influence of callosal afference onto the directional and orientational selectivities of single neurons in the 17/18 border region of the cat. Acta Biophysica Sinica, 9: 407-414.

Ma MH, Li B, Sun JS, Diao YC* (1991) Effects of GABA and bicuculline on the properties of visual superior colliculus neurons in golden hamsters. Acta Physiologica Sinica, 43: 573-579.

Sun JS, Li B, Ma MH, Diao YC* (1991) The influence of callosal afference on the responsiveness of single neurons at the 17/18 border region in the cat. Acta Biophysica Sinica. 7: 495-500.