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TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus

Author

Listed:
  • Joaquin I. Hurtado-Zavala

    (Trans-synaptic Signaling Group, European Neuroscience Institute)

  • Binu Ramachandran

    (Trans-synaptic Signaling Group, European Neuroscience Institute)

  • Saheeb Ahmed

    (Trans-synaptic Signaling Group, European Neuroscience Institute
    University Medical Center Göttingen)

  • Rashi Halder

    (German Center for Neurodegenerative Disease, University Medical Center Goettingen)

  • Christiane Bolleyer

    (Trans-synaptic Signaling Group, European Neuroscience Institute)

  • Ankit Awasthi

    (Trans-synaptic Signaling Group, European Neuroscience Institute)

  • Markus A. Stahlberg

    (Trans-synaptic Signaling Group, European Neuroscience Institute)

  • Robin J. Wagener

    (Institute for Neuroanatomy, University Medical Center Goettingen
    Faculty of Medicine, University of Geneva)

  • Kristin Anderson

    (Lehigh University)

  • Ryan M. Drenan

    (Purdue University)

  • Henry A. Lester

    (California Institute of Technology)

  • Julie M. Miwa

    (Lehigh University)

  • Jochen F. Staiger

    (Institute for Neuroanatomy, University Medical Center Goettingen)

  • Andre Fischer

    (German Center for Neurodegenerative Disease, University Medical Center Goettingen)

  • Camin Dean

    (Trans-synaptic Signaling Group, European Neuroscience Institute)

Abstract

TRPV1 is an ion channel activated by heat and pungent agents including capsaicin, and has been extensively studied in nociception of sensory neurons. However, the location and function of TRPV1 in the hippocampus is debated. We found that TRPV1 is expressed in oriens-lacunosum-moleculare (OLM) interneurons in the hippocampus, and promotes excitatory innervation. TRPV1 knockout mice have reduced glutamatergic innervation of OLM neurons. When activated by capsaicin, TRPV1 recruits more glutamatergic, but not GABAergic, terminals to OLM neurons in vitro. When TRPV1 is blocked, glutamatergic input to OLM neurons is dramatically reduced. Heterologous expression of TRPV1 also increases excitatory innervation. Moreover, TRPV1 knockouts have reduced Schaffer collateral LTP, which is rescued by activating OLM neurons with nicotine—via α2β2-containing nicotinic receptors—to bypass innervation defects. Our results reveal a synaptogenic function of TRPV1 in a specific interneuron population in the hippocampus, where it is important for gating hippocampal plasticity.

Suggested Citation

  • Joaquin I. Hurtado-Zavala & Binu Ramachandran & Saheeb Ahmed & Rashi Halder & Christiane Bolleyer & Ankit Awasthi & Markus A. Stahlberg & Robin J. Wagener & Kristin Anderson & Ryan M. Drenan & Henry A, 2017. "TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus," Nature Communications, Nature, vol. 8(1), pages 1-20, August.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms15878
    DOI: 10.1038/ncomms15878
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