Journal of Neuroscience, Vol 10, 20-33, Copyright © 1990 by Society for Neuroscience
Prolonged enhancement of anterior thalamic synaptic responsiveness by stimulation of a brain-stem cholinergic group
D Pare, M Steriade, M Deschenes and D Bouhassira
Laboratoire de Neurophysiologie, Faculte de Medecine, Universite Laval, Quebec, Canada.
This study describes the effects of brain-stem cholinergic laterodorsal
tegmental (LDT) stimulation on the synaptic responsiveness of anterior
thalamic (AT) neurons. A sample of AT cells, physiologically identified by
their short-latency (less than 6.5 msec) response to mammillary body (MB)
stimulation, was recorded in unanesthetized, chronically implanted cats and
in urethane-anesthetized cats. In chronic experiments, LDT stimulation
evoked a short-latency (10-20 msec) excitation in most AT cells. Moreover,
brief LDT trains (3 shocks at 300 Hz, every 3 sec) enhanced the
responsiveness of AT cells to both MB (orthodromic) and cortical (ortho-
and antidromic) stimuli. This effect did not vary as a function of the
interval between LDT conditioning and MB or cortical testing shocks, but as
a function of the number of trials. The effects of LDT stimuli resisted
reserpine treatment (0.75 mg/kg), suggesting that they were not dependent
on the coactivation of monoaminergic fibers. Finally, LDT trains did not
suppress inhibitory processes in AT neurons when conditioning-testing
intervals were longer than 60 msec. Intracellular recordings performed in
urethane-anesthetized cats revealed that LDT stimulation induced a
short-latency depolarization which increased with membrane
hyperpolarization and was associated with an increase in apparent membrane
conductance. Usually, isolated LDT trains did not evoke lasting changes in
membrane potential or conductance. However, when LDT trains were applied
every 3 sec, they gradually decreased the apparent membrane conductance
without altering the membrane potential. This conductance change had a time
course similar to the LDT-induced potentiation of responsiveness observed
in the chronic experiments. In some neurons, LDT conditioning trains also
induced a marked increase in the probability of fast prepotentials being
triggered by subthreshold MB or cortical orthodromic volleys. In order to
distinguish the cumulative effects of repeated LDT trains from the possibly
slow time course of LDT influences, we studied the effects of a unique 1
sec LDT train (at 30 Hz) on the synaptic responsiveness of AT cells
recorded extracellularly in reserpine-treated, urethane- anesthetized
animals. Such LDT trains induced a 2.9-fold increase in synaptic
responsiveness, reaching its peak 40-50 sec after the LDT train and lasting
up to 4 min. Iontophoretic application of the muscarinic blocker
scopolamine blocked these long-lasting potentiating effects of LDT stimuli.
Removal of cortical and basal forebrain inputs to the AT nuclear complex by
appropriate transections did not abolish the potentiating effects of LDT
trains.(ABSTRACT TRUNCATED AT 400 WORDS)