Afferent-specific properties of interneuron synapses underlie selective long-term regulation of feedback inhibitory circuits in CA1 hippocampus.
Hebbian long-term potentiation (LTP) develops at specific synapses onto hippocampal CA1 oriens/alveus interneurons (OA-INs), suggesting selective regulation of distinct input pathways. Afferent-specific properties at interneuron synapses have been characterized extensively in CA3 stratum lucidum cells, but given interneuron diversity these rules of transmission and plasticity may not hold in other interneuron types. Here, we used paired recordings and demonstrate that CA2/3 pyramidal cell (PC) feedforward and CA1 PC feedback synapses onto OA-INs show distinct AMPA receptor rectification and Ca(2+) permeability, short-term plasticity and mGluR2/3-mediated inhibition. Only feedback synapses undergo Hebbian LTP. OA-IN firing during repeated synaptic stimulation displays onset-transient or late-persistent responses consistent with activation of feedforward and feedback inputs, respectively. Input-output functions are preserved after theta-burst stimulation, but late-persistent responses selectively show mGluR1-dependent long-term increases. Thus, cell type- and afferent-specific rules of transmission and plasticity underlie distinct OA-IN input-output functions, providing selective long-term regulation in feedback inhibitory networks.
Croce
Ariane
A
Groupe de Recherche sur le Système Nerveux Central, Département de Physiologie, Université de Montréal, Succ. Centre-ville, Montréal, Québec, Canada.
Pelletier
Joe Guillaume
JG
Tartas
Maylis
M
Lacaille
Jean-Claude
JC
D000200:Action Potentials; D000818:Animals; D056547:CA1 Region, Hippocampal / Q000166:cytology / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D056651:CA2 Region, Hippocampal / Q000502:physiology; D056654:CA3 Region, Hippocampal / Q000502:physiology; D002118:Calcium / Q000378:metabolism; D025461:Feedback, Physiological; D066298:In Vitro Techniques; D007395:Interneurons / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D017774:Long-Term Potentiation; D009433:Neural Inhibition / Q000187:drug effects; D009434:Neural Pathways / Q000502:physiology; D009473:Neuronal Plasticity / Q000187:drug effects; D009475:Neurons, Afferent / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D018377:Neurotransmitter Agents / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D018091:Receptors, AMPA / Q000378:metabolism; D018094:Receptors, Metabotropic Glutamate / Q000378:metabolism; D009435:Synaptic Transmission / Q000187:drug effects; D013997:Time Factors
D018377:Neurotransmitter Agents; D018091:Receptors, AMPA; D018094:Receptors, Metabotropic Glutamate; C108822:metabotropic glutamate receptor 2; C102718:metabotropic glutamate receptor 3; D002118:Calcium
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