Journal of Neuroscience, Vol 13, 650-659, Copyright © 1993 by Society for Neuroscience
Evidence for presynaptic inhibition of the olfactory commissural pathway by cholinergic agonists and stimulation of the nucleus of the diagonal band
WT Nickell and MT Shipley
Department of Anatomy and Cell Biology, University of Cincinnati College of Medicine, Ohio 45267-0521.
We have investigated the role of the projection from the magnocellular
basal forebrain to the olfactory bulb in regulating synaptic transmission
in the commissural connection between the two olfactory bulbs. Commissural
fibers arise in the contralateral anterior olfactory nucleus, travel in the
anterior wing of the anterior commissure (AC), and terminate in the granule
cell layer of the olfactory bulb. Electrical stimulation of the commissure
causes synaptic activation of granule cells in the granule cell layer of
the bulb; the resulting field potential is a reliable indicator of this
synaptic current. Microinjections of cholinergic agonists, but not of
identical, or larger, quantities of vehicle, reduced the amplitude of this
AC field potential. Systemic injection of scopolamine reversed this
depression and returned the AC response amplitude to control levels.
Irreversible AChE inhibition also reduced the amplitude of the AC response,
and muscarinic blockade reversed this effect. Cholinergic terminals in the
olfactory bulb arise entirely from the axons of magnocellular basal
forebrain neurons in the nucleus of the diagonal band (NDB). Electrical
stimulation of NDB, which should release ACh, as well as other
transmitters, depressed the AC response. Brief trains of NDB shocks caused
a moderate decrease in the AC response that lasted 1-2 sec. Longer shock
trains, which caused marked potentiation of the NDB field potential, caused
a profound, prolonged (> 20 sec) inhibition of the AC response.
Antidromic tests demonstrated that NDB stimulation significantly decreased
the excitability of AC terminals. This and other characteristics of the
inhibition strongly suggest that the decrease in amplitude of the field
potential response to AC stimulation caused by cholinergic agonists and
stimulation of NDB is due to presynaptic inhibition leading to reduced
release of transmitter from AC terminals. These results suggest that one
function of the basal forebrain projection to the olfactory bulb is
inhibition of the commissural connection between the two olfactory bulbs.
As NDB has been implicated in theta pacemaker input to the olfactory bulb,
phasic NDB inhibition of centrifugal afferents to the bulb could function
to coordinate signal processing temporally in the olfactory system.
Temporal coordination may be particularly important to olfactory circuit
function, as this system lacks the point-to-point topographical
organization characteristic of other sensory systems.
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