Maturation of glutamatergic neurotransmission in dentate gyrus granule cells.
We studied the development of glutamatergic neurotransmission in dentate gyrus granule cells (GCs) in hippocampal slices from 5 to 12-day-old rats. The active postnatal neuronogenesis in dentate permits GCs with staggered birthdates to be studied in situ in a single preparation. We recorded evoked responses to medial perforant path stimulation using visually-guided whole-cell patch clamping to select immature GCs, and biocytin filling to correlate electrophysiologic responses with maturational stage. Even within this immature cell population we found four distinct electrophysiologic patterns. Type 1 cells had no glutamatergic current; Type 2 cells had only N-methyl-D-aspartate receptor (NMDA) current; Type 3 cells had both NMDA and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) current although the NMDA component could be isolated at low stimulus intensity (NMDA threshold<AMPA threshold); Type 4 cells had both AMPA and NMDA currents with NMDA threshold>/=AMPA threshold. Type 1 cells were least mature, and Type 4 cells most mature as assessed by cell properties, dendritic arborization, and penetration of dendrites into the molecular layer. Thus NMDA-mediated currents predominate early in GC development as is consistent with their role in processes that determine dentate architecture - neuronal migration, dendritic outgrowth and regression, and synapse stabilization. By analogy with 'silent synapses' (i.e. synapses that contain only NMDA receptors), Type 2 cells are candidate 'silent cells' that may undergo activity-dependent acquisition of functional fast-conducting AMPA receptors with maturation.
Ye
G L
GL
The Division of Pediatric Neurology, Evanston Hospital, 2650 Ridge Avenue, Evanston, IL 60201, USA.
Song Liu
X
X
Pasternak
J F
JF
Trommer
B L
BL
D000818:Animals; D000831:Animals, Newborn / Q000254:growth & development / Q000502:physiology; D016922:Cellular Senescence / Q000502:physiology; D018891:Dentate Gyrus / Q000166:cytology / Q000254:growth & development / Q000502:physiology* / Q000648:ultrastructure; D005071:Evoked Potentials / Q000502:physiology; D005260:Female; D018698:Glutamic Acid / Q000502:physiology*; D066298:In Vitro Techniques; D008297:Male; D009474:Neurons / Q000502:physiology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D018091:Receptors, AMPA / Q000502:physiology; D016194:Receptors, N-Methyl-D-Aspartate / Q000502:physiology; D009435:Synaptic Transmission / Q000502:physiology*
D018091:Receptors, AMPA; D016194:Receptors, N-Methyl-D-Aspartate; D018698:Glutamic Acid