Neuronal diversity in GABAergic long-range projections from the hippocampus.
The formation and recall of sensory, motor, and cognitive representations require coordinated fast communication among multiple cortical areas. Interareal projections are mainly mediated by glutamatergic pyramidal cell projections; only few long-range GABAergic connections have been reported. Using in vivo recording and labeling of single cells and retrograde axonal tracing, we demonstrate novel long-range GABAergic projection neurons in the rat hippocampus: (1) somatostatin- and predominantly mGluR1alpha-positive neurons in stratum oriens project to the subiculum, other cortical areas, and the medial septum; (2) neurons in stratum oriens, including somatostatin-negative ones; and (3) trilaminar cells project to the subiculum and/or other cortical areas but not the septum. These three populations strongly increase their firing during sharp wave-associated ripple oscillations, communicating this network state to the septotemporal system. Finally, a large population of somatostatin-negative GABAergic cells in stratum radiatum project to the molecular layers of the subiculum, presubiculum, retrosplenial cortex, and indusium griseum and fire rhythmically at high rates during theta oscillations but do not increase their firing during ripples. The GABAergic projection axons have a larger diameter and thicker myelin sheet than those of CA1 pyramidal cells. Therefore, rhythmic IPSCs are likely to precede the arrival of excitation in cortical areas (e.g., subiculum) that receive both glutamatergic and GABAergic projections from the CA1 area. Other areas, including the retrosplenial cortex, receive only rhythmic GABAergic CA1 input. We conclude that direct GABAergic projections from the hippocampus to other cortical areas and the septum contribute to coordinating oscillatory timing across structures.
Jinno
Shozo
S
Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford, United Kingdom. sjnno@med.kyushu-u.ac.jp
Klausberger
Thomas
T
Marton
Laszlo F
LF
Dalezios
Yannis
Y
Roberts
J David B
JD
Fuentealba
Pablo
P
Bushong
Eric A
EA
Henze
Darrell
D
Buzsáki
György
G
Somogyi
Peter
P
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D001710:Biotin / Q000031:analogs & derivatives / Q000493:pharmacokinetics; D001931:Brain Mapping; D003911:Dextrans / Q000493:pharmacokinetics; D006624:Hippocampus / Q000166:cytology* / Q000502:physiology; D053444:Inhibitory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D008297:Male; D046529:Microscopy, Electron, Transmission / Q000379:methods; D008959:Models, Neurological; D009419:Nerve Tissue Proteins / Q000378:metabolism; D009434:Neural Pathways / Q000033:anatomy & histology* / Q000378:metabolism; D009474:Neurons / Q000145:classification / Q000502:physiology* / Q000648:ultrastructure; D010835:Phytohemagglutinins / Q000493:pharmacokinetics; D051381:Rats; D017207:Rats, Sprague-Dawley; D018094:Receptors, Metabotropic Glutamate / Q000378:metabolism; D013004:Somatostatin / Q000378:metabolism; D013266:Stilbamidines / Q000493:pharmacokinetics; D005680:gamma-Aminobutyric Acid / Q000378:metabolism*
C049774:2-hydroxy-4,4'-diamidinostilbene, methanesulfonate salt; D003911:Dextrans; D009419:Nerve Tissue Proteins; D010835:Phytohemagglutinins; D018094:Receptors, Metabotropic Glutamate; D013266:Stilbamidines; C076397:biotinylated dextran amine; C100156:leukoagglutinins, plants; C104077:metabotropic glutamate receptor type 1; D013004:Somatostatin; D005680:gamma-Aminobutyric Acid; D001710:Biotin
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