A cortico-hippocampal learning rule shapes inhibitory microcircuit activity to enhance hippocampal information flow.
How does coordinated activity between distinct brain regions implement a set of learning rules to sculpt information processing in a given neural circuit? Using interneuron cell-type-specific optical activation and pharmacogenetic silencing in vitro, we show that temporally precise pairing of direct entorhinal perforant path (PP) and hippocampal Schaffer collateral (SC) inputs to CA1 pyramidal cells selectively suppresses SC-associated perisomatic inhibition from cholecystokinin (CCK)-expressing interneurons. The CCK interneurons provide a surprisingly strong feedforward inhibitory drive to effectively control the coincident excitation of CA1 pyramidal neurons by convergent inputs. Thus, in-phase cortico-hippocampal activity provides a powerful heterosynaptic learning rule for long-term gating of information flow through the hippocampal excitatory macrocircuit by the silencing of the CCK inhibitory microcircuit.
Department of Neuroscience, Columbia University, 1051 Riverside Drive, New York, NY 10032, USA.
Jayeeta
J
Basu
Kalyan V
KV
Srinivas
Stephanie K
SK
Cheung
Hiroki
H
Taniguchi
Z Josh
ZJ
Huang
Steven A
SA
Siegelbaum
D000818:Animals; D001703:Biophysics; D002118:Calcium / Q000378:metabolism; D002540:Cerebral Cortex / Q000502:physiology*; D000075402:Channelrhodopsins; D002766:Cholecystokinin / Q000235:genetics; D003198:Computer Simulation; D004558:Electric Stimulation; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D006624:Hippocampus / Q000166:cytology*; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials / Q000187:drug effects; D008164:Luminescent Proteins / Q000235:genetics; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology*; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D062308:Optogenetics; D010320:Parvalbumins / Q000235:genetics; D018408:Patch-Clamp Techniques; D013569:Synapses / Q000187:drug effects / Q000502:physiology
D000075402:Channelrhodopsins; C501120:Dlx5 protein, mouse; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D018398:Homeodomain Proteins; D008164:Luminescent Proteins; D010320:Parvalbumins; D002766:Cholecystokinin; D002118:Calcium