 |
 Previous Article | Next Article 
The Journal of Neuroscience, December 15, 2001, 21(24):9770-9781
Early Development of Neuronal Activity in the Primate Hippocampus
In Utero
Roustem
Khazipov1,
Monique
Esclapez1,
Olivier
Caillard1,
Christophe
Bernard1,
Ilgam
Khalilov1,
Roman
Tyzio1,
June
Hirsch1,
Volodymyr
Dzhala1,
Brigitte
Berger2, and
Yehezkel
Ben-Ari1
1 Institut de Neurobiologie de la
Méditerranée/Institut National de la Santé et de la
Recherche Médicale (INSERM) U29, Luminy, 13273 Marseille, France,
and 2 INSERM U106, Hopital de la Salpetriere, 75013 Paris,
France
Morphological studies suggest that the primate hippocampus develops
extensively before birth, but little is known about its functional
development. Patch-clamp recordings of hippocampal neurons and
reconstruction of biocytin-filled pyramidal cells were performed in
slices of macaque cynomolgus fetuses delivered by cesarean section. We
found that during the second half of gestation, axons and dendrites of
pyramidal cells grow intensively by hundreds of micrometers per day to
attain a high level of maturity near term. Synaptic currents appear
around midgestation and are correlated with the level of morphological
differentiation of pyramidal cells: the first synapses are GABAergic,
and their emergence correlates with the growth of apical dendrite into
stratum radiatum. A later occurrence of glutamatergic synaptic currents
correlates with a further differentiation of the axodendritic tree and
the appearance of spines. Relying on the number of dendritic spines, we
estimated that hundreds of new glutamatergic synapses are established
every day on a pyramidal neuron during the last third of gestation. Most of the synaptic activity is synchronized in spontaneous slow ( 0.1 Hz) network oscillations reminiscent of the giant depolarizing potentials in neonatal rodents. Epileptiform discharges can be evoked
by the GABA(A) receptor antagonist bicuculline by the last third of
gestation, and postsynaptic GABA(B) receptors contribute to the
termination of epileptiform discharges. Comparing the results obtained
in primates and rodents, we conclude that the template of early
hippocampal network development is conserved across the mammalian
evolution but that it is shifted toward fetal life in primate.
Key words:
hippocampus; primate; fetus; development; GABA; glutamate; epilepsy
Copyright © 2001 Society for Neuroscience 0270-6474/01/21249770-12$05.00/0
This article has been cited by other articles:
|
|
|
|
 
S. Rheims, M. Minlebaev, A. Ivanov, A. Represa, R. Khazipov, G. L. Holmes, Y. Ben-Ari, and Y. Zilberter
Excitatory GABA in Rodent Developing Neocortex In Vitro
J Neurophysiol,
August 1, 2008;
100(2):
609 - 619.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. D. Wang and A. R. Kriegstein
GABA Regulates Excitatory Synapse Formation in the Neocortex via NMDA Receptor Activation
J. Neurosci.,
May 21, 2008;
28(21):
5547 - 5558.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Petanjek, B. Berger, and M. Esclapez
Origins of Cortical GABAergic Neurons in the Cynomolgus Monkey
Cereb Cortex,
May 13, 2008;
(2008)
bhn078v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Petanjek, M. Judas, I. Kostovic, and H. B.M. Uylings
Lifespan Alterations of Basal Dendritic Trees of Pyramidal Neurons in the Human Prefrontal Cortex: A Layer-Specific Pattern
Cereb Cortex,
April 1, 2008;
18(4):
915 - 929.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Deng, J. Yao, C. Fang, N. Dong, B. Luscher, and G. Chen
Sequential Postsynaptic Maturation Governs the Temporal Order of GABAergic and Glutamatergic Synaptogenesis in Rat Embryonic Cultures
J. Neurosci.,
October 3, 2007;
27(40):
10860 - 10869.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Ben-Ari, J.-L. Gaiarsa, R. Tyzio, and R. Khazipov
GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations
Physiol Rev,
October 1, 2007;
87(4):
1215 - 1284.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Azimi-Zonooz, C. W. Shuttleworth, and J. A. Connor
GABAergic Protection of Hippocampal Pyramidal Neurons Against Glutamate Insult: Deficit in Young Animals Compared to Adults
J Neurophysiol,
July 1, 2006;
96(1):
299 - 308.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. L. Hanganu, Y. Ben-Ari, and R. Khazipov
Retinal waves trigger spindle bursts in the neonatal rat visual cortex.
J. Neurosci.,
June 21, 2006;
26(25):
6728 - 6736.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. S. Esposito, V. C. Piatti, D. A. Laplagne, N. A. Morgenstern, C. C. Ferrari, F. J. Pitossi, and A. F. Schinder
Neuronal Differentiation in the Adult Hippocampus Recapitulates Embryonic Development
J. Neurosci.,
November 2, 2005;
25(44):
10074 - 10086.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Kim, Z.-X. Yu, B. B. Fredholm, and S. A. Rivkees
Susceptibility of the developing brain to acute hypoglycemia involving A1 adenosine receptor activation
Am J Physiol Endocrinol Metab,
October 1, 2005;
289(4):
E562 - E569.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Bernard, M. Milh, Y. M. Morozov, Y. Ben-Ari, T. F. Freund, and H. Gozlan
Altering cannabinoid signaling during development disrupts neuronal activity
PNAS,
June 28, 2005;
102(26):
9388 - 9393.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. T. Sipila, K. Huttu, I. Soltesz, J. Voipio, and K. Kaila
Depolarizing GABA Acts on Intrinsically Bursting Pyramidal Neurons to Drive Giant Depolarizing Potentials in the Immature Hippocampus
J. Neurosci.,
June 1, 2005;
25(22):
5280 - 5289.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Wakisaka, A. Furuta, K. Masuda, W. Morikawa, M. Kuwano, and T. Iwaki
Cellular Distribution of NDRG1 Protein in the Rat Kidney and Brain During Normal Postnatal Development
J. Histochem. Cytochem.,
November 1, 2003;
51(11):
1515 - 1525.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Gozlan and Y. Ben-Ari
Interneurons are the Source and the Targets of the First Synapses Formed in the Rat Developing Hippocampal Circuit
Cereb Cortex,
June 1, 2003;
13(6):
684 - 692.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
