DEVELOPMENTAL CHANGES IN MEMBRANE PROPERTIES AND POSTSYNAPTIC CURRENTS OF
GRANULE CELLS IN RAT DENTATE GYRUS.
Liu, Ying-Bing, Peter A. Lio, Joseph F. Pasternak, and Barbara L. Trommer.
Division of Pediatric Neurology, Evanston Hospital, Evanston, Illinois,
60201 and the Departments of Pediatrics and Neurology, Northwestern University
Medical School, Chicago, Illinois, 60611.
APStracts 3:0056N, 1996.
SUMMARY AND CONCLUSIONS
1. Whole cell patch-clamp recordings were used to study dentate gyrus granule
cells in hippocampal slices from juvenile rats (postnatal days 8-32). Membrane
properties were measured using current clamp recordings and were correlated
with morphology of a subgroup of neurons filled with biocytin. The components
of the postsynaptic currents (PSCs) induced by medial perforant path
stimulation were characterized using specific receptor antagonists in voltage
clamp recordings. 2. Granule cells located in the middle third of the superior
blade of stratum granulosum from the rostral third of hippocampus were divided
into three groups according to their input resistance (IR). Neurons with low
IR (206 +/- 182 M[omega]) had hyperpolarized resting membrane potentials (-82
+/- 7 mV) and high amplitude action potentials (108 +/- 23 mV). Neurons with
high IR (1259 +/- 204 M[omega]) had more depolarized resting membrane
potentials (-54 +/- 6 mV) and lower amplitude action potentials (71 +/- 10
mV). Neurons with intermediate IR (619+/-166 M[omega]) also had intermediate
resting membrane potentials (-63+/-7 mV) and action potential amplitudes
(86+/-14 mV). Low input resistance neurons became increasingly prevalent with
advancing postnatal age, but neurons from each group could be found throughout
the entire period under study. 3. Morphologic studies of low IR neurons
revealed an extensive dendritic arborization that traversed the entire
molecular layer and was characteristic of mature granule cells. High IR cells
had smaller somata and short, simple dendritic arborization that incompletely
penetrated the molecular layer and were classified as immature. Intermediate
IR cells had morphologic features of intermediate maturity. 4. The initial
phase of the PSC evoked at -80 mV was a fast inward current that was
comparable with respect to latency to peak, latency to onset, and 10-90% rise
time in neurons of all maturities held at -80 mV. This current was CNQX
sensitive. 5. The decay phase of PSCs at -80 mV varied with neuronal maturity.
Mature neurons had monoexponential decays (_ = 8.9+/-3.6). Intermediate and
immature neurons had prominent later inward currents that resulted in slower
decays . In the case of the immature neurons the inward current during the
decay phase could be separated from the initial fast inward peak. The later
inward currents in intermediate and immature neurons were bicuculline
sensitive. 6. Using uniform ionic conditions of the extracellular and patch
solutions, I-V relations and reversal potentials for pharmacologically
isolated AMPA, NMDA, and GABA A currents were comparable across all cell
maturities. Calculated ratios for peak GABA A /NMDA/AMPA currents decreased
significantly with maturation as follows: 9.4+/-2.9/1.4+/-0.5/1.0 for immature
cells, 7.2+/-2.5/1.5+/-0.7/1.0 for intermediate cells, and 2.0+/-1.2/0.9+/-
0.4/1.0 for mature cells. 7. GABA current was mediated both by polysynaptic
activation of interneurons and by direct activation of interneurons with
monosynaptic input onto granule cells. The proportional contributions of mono-
and polysynaptic GABA to total GABA were comparable across all cell
maturities; latency to peak GABA current decreased with increasing cell
maturity for both mono and polysynaptic components. 8. We conclude that PSCs
evoked in granule cells by medial perforant path activation in neurons of all
maturities consist of both glutamatergic and GABAergic components. PSCs are
dominatedb y GABA-ergic neurotransmission in immature granule cells, and the
contribution of glutamatergic neurotransmission increases with neuronal
maturation. The greater ratio of peak GABA A to glutamate currents and the
longer time interval between their respective peaks combine to produce a
distinctive PSC shape in the immature compared with mature granule cells.
Received 1 December 1995; accepted in final form 8 March 1996.
APS Manuscript Number J812-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 27 March 96