Septal cholinergic neurons gate hippocampal output to entorhinal cortex via oriens lacunosum moleculare interneurons

被引:46
作者
Haam, Juhee [1 ]
Zhou, Jingheng [1 ]
Cui, Guohong [1 ]
Yakel, Jerrel L. [1 ]
机构
[1] NIEHS, Neurobiol Lab, NIH, Dept Hlth & Human Serv, Res Triangle Pk, NC 27709 USA
关键词
acetylcholine; oriens lacunosum moleculare interneurons; hippocampus; memory; photometry; CENTRAL-NERVOUS-SYSTEM; DECLARATIVE MEMORY CONSOLIDATION; SYNAPTIC-TRANSMISSION; ALZHEIMERS-DISEASE; IN-VITRO; ACETYLCHOLINE-RELEASE; OLM INTERNEURONS; CA1; INTERNEURONS; BASAL FOREBRAIN; NEURAL ACTIVITY;
D O I
10.1073/pnas.1712538115
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Neuromodulation of neural networks, whereby a selected circuit is regulated by a particular modulator, plays a critical role in learning and memory. Among neuromodulators, acetylcholine (ACh) plays a critical role in hippocampus-dependent memory and has been shown to modulate neuronal circuits in the hippocampus. However, it has remained unknown how ACh modulates hippocampal output. Here, using in vitro and in vivo approaches, we show that ACh, by activating oriens lacunosum moleculare (OLM) interneurons and therefore augmenting the negative-feedback regulation to the CA1 pyramidal neurons, suppresses the circuit from the hippocampal area CA1 to the deep-layer entorhinal cortex (EC). We also demonstrate, using mouse behavior studies, that the ablation of OLM interneurons specifically impairs hippocampus-dependent but not hippocampus-independent learning. These data suggest that ACh plays an important role in regulating hippocampal output to the EC by activating OLM interneurons, which is critical for the formation of hippocampus-dependent memory.
引用
收藏
页码:E1886 / E1895
页数:10
相关论文
共 83 条
  • [41] Cholinergic Stimulation Enhances Neural Activity Associated with Encoding but Reduces Neural Activity Associated with Retrieval in Humans
    Kukolja, Juraj
    Thiel, Christiane M.
    Fink, Gereon R.
    [J]. JOURNAL OF NEUROSCIENCE, 2009, 29 (25) : 8119 - 8128
  • [42] Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones
    Lawrence, JJ
    Statland, JM
    Grinspan, ZM
    McBain, CJ
    [J]. JOURNAL OF PHYSIOLOGY-LONDON, 2006, 570 (03): : 595 - 610
  • [43] THE ROLE OF THE SEPTOHIPPOCAMPAL PATHWAY IN THE REGULATION OF HIPPOCAMPAL FIELD ACTIVITY AND BEHAVIOR - ANALYSIS BY THE INTRASEPTAL MICROINFUSION OF CARBACHOL, ATROPINE, AND PROCAINE
    LAWSON, VH
    BLAND, BH
    [J]. EXPERIMENTAL NEUROLOGY, 1993, 120 (01) : 132 - 144
  • [44] OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons
    Leao, Richardson N.
    Mikulovic, Sanja
    Leao, Katarina E.
    Munguba, Hermany
    Gezelius, Henrik
    Enjin, Anders
    Patra, Kalicharan
    Eriksson, Anders
    Loew, Leslie M.
    Tort, Adriano B. L.
    Kullander, Klas
    [J]. NATURE NEUROSCIENCE, 2012, 15 (11) : 1524 - 1530
  • [45] LI YW, 1995, J NEUROSCI, V15, P2888
  • [46] PASSIVE PROPAGATION OF LTD TO STRATUM ORIENS-ALVEUS INHIBITORY NEURONS MODULATES THE TEMPOROAMMONIC INPUT TO THE HIPPOCAMPAL CA1 REGION
    MACCAFERRI, G
    MCBAIN, CJ
    [J]. NEURON, 1995, 15 (01) : 137 - 145
  • [47] Novel modulatory mechanisms revealed by the sustained application of nicotine in the guinea-pig hippocampus in vitro
    Mann, EO
    Greenfield, SA
    [J]. JOURNAL OF PHYSIOLOGY-LONDON, 2003, 551 (02): : 539 - 550
  • [48] An acetylcholinesterase inhibitor, eserine, induces long-term depression at CA3-CA1 synapses in the hippocampus of adult rats
    Mans, Robert Alan
    Warmus, Brian A.
    Smith, Caroline C.
    McMahon, Lori L.
    [J]. JOURNAL OF NEUROPHYSIOLOGY, 2014, 112 (10) : 2388 - 2397
  • [49] MICRODIALYSIS MEASUREMENT OF CORTICAL AND HIPPOCAMPAL ACETYLCHOLINE-RELEASE DURING SLEEP-WAKE CYCLE IN FREELY MOVING CATS
    MARROSU, F
    PORTAS, C
    MASCIA, MS
    CASU, MA
    FA, M
    GIAGHEDDU, M
    IMPERATO, A
    GESSA, GL
    [J]. BRAIN RESEARCH, 1995, 671 (02) : 329 - 332
  • [50] Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons
    McQuiston, AR
    Madison, DV
    [J]. JOURNAL OF NEUROSCIENCE, 1999, 19 (14) : 5693 - 5702