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Volume 17, Number 12,
Issue of June 15, 1997
pp. 4764-4784
Copyright ©1997 Society for Neuroscience
Glutamatergic Enteric Neurons
Received Feb. 3, 1997; revised March 26, 1997; accepted March 31, 1997.
Min-Tsai Liu1,
Jeffrey
D. Rothstein2,
Michael D. Gershon1, and
Annette L. Kirchgessner1
1 Department of Anatomy and Cell Biology, Columbia
University College of Physicians and Surgeons, New York, New York
10032, and 2 Department of Neurology, The Johns Hopkins
University, Baltimore, Maryland 21224-6522
We tested the hypothesis that glutamate, the major excitatory
neurotransmitter of the CNS, is also an excitatory neurotransmitter in
the enteric nervous system (ENS). Glutamate immunoreactivity was found
in cholinergic enteric neurons, many of which were identified as
sensory by their co-storage of substance P and/or calbindin. Glutamate
immunoreactivity was concentrated in terminal varicosities with a
majority of small clear synaptic vesicles. The immunoreactivities of
both AMPA and NMDA receptor subunits were also detected on neurons in
both submucosal and myenteric plexuses. The immunoreactivity of the
EAAC1 neuronal glutamate transporter was widespread in both plexuses.
Glutamate evoked depolarizing responses in myenteric neurons that had
fast and slow components. The fast component was mimicked by AMPA, and
the slow component was mimicked by NMDA. The fast component and the
response to AMPA mimicked fast EPSPs evoked in 2/AH neurons; moreover,
fast EPSPs as well as fast glutamate and AMPA responses were blocked by
selective AMPA antagonists and potentiated by the glutamate uptake
inhibitor L-( )-threo-3-hydroxyaspartic acid. These observations demonstrate, for the first time, the presence
of glutamatergic neurons and glutamate-mediated neurotransmission in
the ENS.
Key words:
enteric nervous system;
electrophysiology;
excitatory
amino acids;
glutamate transporters;
sensory neurons;
depolarization
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