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Journal of Neuroscience, Vol 13, 808-819, Copyright © 1993 by Society for Neuroscience
Synaptic potentials in the central terminals of locust proprioceptive afferents generated by other afferents from the same sense organ
M Burrows and G Laurent
Division of Biology, California Institute of Technology, Pasadena 91125.
Afferent neurons from a proprioceptor [the femoral chordotonal organ (FCO)]
at the femoro-tibial joint of a locust hindleg carry patterns of spikes to
the CNS in which information is coded about the positions and movements of
the tibia. Intracellular recordings from the afferents of this organ as
they enter the CNS reveal spikes and depolarizing post- synaptic potentials
(PSPs) during voluntary or imposed movements of the joint. Some of these
PSPs are generated as a result of spikes in other FCO afferents, and can be
evoked experimentally by electrical stimulation of the nerve from the
organ. One afferent does not appear to synapse directly on another, but
instead activates reliable pathways involving other central neurons.
Current clamping of individual afferents in isolated ganglia shows that the
PSPs are increased in amplitude by hyperpolarizing currents injected into
an afferent, and decreased by depolarizing ones. They reverse at about -68
mV (n = 5). At the normal resting potential of the afferents, -72 mV (+/-
0.42 SE, n = 57), the PSPs are therefore depolarizing, and are associated
with an increased conductance of the membrane. The changes in membrane
potential and conductances associated with the PSPs can be mimicked by
pressure injection of GABA into the regions of neuropil that contain the
terminals of the afferents. The potential evoked by GABA is associated with
an increased conductance of the membrane and reverses at the same potential
as the PSPs. GABA also reduces the PSPs evoked in the terminals, either by
movements of the FCO or by electrical stimulation of its nerve. The PSPs
and the effects of the GABA-evoked potentials are mimicked by the GABA
agonist muscimol. The PSPs are blocked reversibly by picrotoxin. The PSPs
and the GABA-evoked potentials both alter the excitability of an afferent
terminal by reducing the ability of the membrane to support an action
potential. It is suggested that the PSPs are depolarizing, inhibitory
potentials generated in the terminals of the afferents by central neurons
that release GABA, and that their role is to change the efficacy of the
afferent spikes at their first output synapses in the CNS. These
interactions could form a graded, gain control mechanism for synaptic
transmission at the afferent output synapses that is directly dependent on
the features of the mechanical movements of the joint.
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