Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex.
Whole-cell patch-clamp recordings and immunocytochemical experiments were performed to determine the short- and long-term effects of lateral fluid percussion head injury on the perisomatic inhibitory control of dentate granule cells in the adult rat, with special reference to the development of trauma-induced hyperexcitability. One week after the delivery of a single, moderate (2.0-2.2 atm) mechanical pressure wave to the neocortex, the feed-forward inhibitory control of dentate granule cell discharges was compromised, and the frequency of miniature IPSCs was decreased. Consistent with the electrophysiological data, the number of hilar parvalbumin (PV)- and cholecystokinin (CCK)-positive dentate interneurons supplying the inhibitory innervation of the perisomatic region of granule cells was decreased weeks and months after head injury. The initial injury to the hilar neurons took place instantaneously after the impact and did not require the recruitment of active physiological processes. Furthermore, the decrease in the number of PV- and CCK-positive hilar interneurons was similar to the decrease in the number of the AMPA-type glutamate receptor subunit 2/3-immunoreactive mossy cells, indicating that the pressure wave-transient causes injurious physical stretching and bending of most cells that are large and not tightly packed in a cell layer. These results reveal for the first time that moderate pressure wave-transients, triggered by traumatic head injury episodes, impact the dentate neuronal network in a unique temporal and spatial pattern, resulting in a net decrease in the perisomatic control of granule cell discharges.
Toth
Z
Z
Department of Anatomy and Neurobiology, University of California, Irvine, California 92697, USA.
Hollrigel
G S
GS
Gorcs
T
T
Soltesz
I
I
D000818:Animals; D001930:Brain Injuries / Q000150:complications / Q000503:physiopathology*; D002766:Cholecystokinin / Q000737:chemistry; D018891:Dentate Gyrus / Q000737:chemistry / Q000503:physiopathology*; D015536:Down-Regulation; D004827:Epilepsy / Q000209:etiology / Q000503:physiopathology; D007395:Interneurons / Q000502:physiology*; D008297:Male; D019599:Mossy Fibers, Hippocampal / Q000473:pathology; D019579:Neocortex / Q000293:injuries* / Q000503:physiopathology; D009419:Nerve Tissue Proteins / Q000737:chemistry; D009474:Neurons / Q000473:pathology / Q000502:physiology; D010320:Parvalbumins / Q000737:chemistry; D018408:Patch-Clamp Techniques; D011312:Pressure; D051381:Rats; D017208:Rats, Wistar; D018091:Receptors, AMPA / Q000032:analysis; D014949:Wounds, Nonpenetrating / Q000150:complications / Q000503:physiopathology*; D005680:gamma-Aminobutyric Acid / Q000502:physiology
D009419:Nerve Tissue Proteins; D010320:Parvalbumins; D018091:Receptors, AMPA; D005680:gamma-Aminobutyric Acid; D002766:Cholecystokinin