Clinical and Experimental Pharmacology and Physiology (2008) 35, 447– 453 doi: 10.1111/j.1440-1681.2008.04913.x
Blackwell Publishing Asia Original Articles
Intraspinal control of sympathetic and motor outflow AK Goodchildet al.
CONTROL OF SYMPATHETIC, RESPIRATORY AND SOMATOMOTOR
OUTFLOW BY AN INTRASPINAL PATTERN GENERATOR
Ann K Goodchild, Bart T M van Deurzen, Cara M Hildreth and Paul M Pilowsky
Macquarie University Neuroscience Centre, Australian School of Advanced Medicine,
Macquarie University, New South Wales, Australia
SUMMARY
1. Sympathetic and somatic motor outflow results from the
summation of excitatory and inhibitory inputs arising from
intra- and supra-spinal origins. Here we determined the contri-
bution of intra- and supra-spinal GABAergic inputs, utilizing
GABA-A receptors, in producing sympathetic and somatic motor
outflow.
2. Spinal GABA-A receptor blockade, with bicuculline or
picrotoxin injected intrathecally at T9, increased the level and
lability of arterial pressure, sympathetic (splanchnic and cervical
sympathetic) and motor (phrenic) nerve activity. Bursts of activity
occurring irregularly, at low frequency were seen in all nerves.
3. C1 spinal transection abolished phrenic nerve activity and
reduced sympathetic nerve activities and arterial pressure.
Intrathecal bicuculline-induced bursting in sympathetic and
motor (phrenic, sciatic and brachial) nerves was similar to that
seen prior to C1 transection. Thus supraspinal control of
sympathetic and somatomotor outflow is not dependent on
GABA-A receptors.
4. Bicuculline-induced effects on phrenic nerve activity were
eliminated after C8 spinal cord transection and regular phrenic
rhythm resumed indicating that bicuculline was not acting
directly on phrenic motoneurons.
5. Bicuculline evoked similar bursting characteristics in both
sympathetic and motor nerves attributable to increased excita-
bility of spinal cord neurons. The bursting patterns evoked were
often coincident in sympathetic and motor nerves suggesting a
common site of origin.
6. These data suggest there is intraspinal coupling between
multiple sympathetic and motor outflows in the adult rat spinal
cord in vivo. Cervicothoracic spinal cord generator/s perhaps in
the form of interneuronal networks, utilizing GABA-A and
glutamate receptors, can simultaneously drive functionally
independent nerves.
Key words: intraspinal pattern generator, sympathetic,
somatomotor, respiratory.
INTRODUCTION
The summed contribution of multiple excitatory and inhibitory
inputs to sympathetic preganglionic and somatic motor neurons
determines their final outputs. It is plausible to suggest that altering
the balance of these inputs to sympathetic preganglionic neurons
(SPN) may contribute to conditions such as hypertension. Neuro-
transmitters mediating inhibitory effects include glycine and GABA,
1,2
as well as peptides such as enkephalin
3
and amines such as noradren-
aline and serotonin.
4,5
Here we focus on the GABAergic inhibition
of sympathetic and motor nerve activity at the level of the spinal cord.
Anatomical, physiological and pharmacological evidence indi-
cates that GABA inhibits SPN and motoneurons. GABA immuno-
reactive terminals innervate SPN
6
and motoneurons;
7
GABA receptors
including GABA-A receptors are found on SPN
8
and motoneurons.
9,10
Iontophoresis of GABA or bicuculline, a GABA-A receptor antag-
onist, onto identified SPN reduces or increases their activity,
respectively.
1,11
GABAergic innervation of SPN and motoneurons originate
both intra- and supra-spinally.
11–17
We previously demonstrated that
spinal GABAergic pathways are not involved in the sympathetic
baroreflex;
18
nevertheless, they do provide a tonic inhibition of the
sympathetic nervous system.
18,19
Viral labelling studies indicate
that spinal interneurons control sympathetic outflow.
20
Specifically
GAD67 positive presympathetic neurons exist in and around the
central autonomic area which, when activated, can inhibit SPN.
16
Similarly, electrical stimulation of the dorsolateral funiculus or
ventrolateral medulla evokes fast inhibitory post synaptic potentials
in SPN which can be blocked in 37 per cent of cases by bicuculline.
11,21
In the present study, we quantified the contribution of supra- and
intraspinal GABAergic inputs to sympathetic outflow by comparing
the effects of spinal GABA-A receptor blockade before and after
spinal cord transection. Spinal pattern generators are activated by a
variety of stimuli and produce a bursting activity in motor outputs.
22–25
There is some evidence for coupling between sympathetic and
somatic motoneurons at the spinal level in the in situ perfused
trunk-hindquarters adult mouse preparation.
26
Consequently, we
determined whether or not such coupling exists in the adult rat
in vivo and, if so, the potential location of this coupling. We measured
multiple sympathetic and motor outputs and determined whether
or not they were activated coincidently by GABA-A receptor
inhibition, both before and after transection at different levels of the
spinal cord. The role of glutamate receptors in the coordinated
Correspondence: A/Professor Ann Goodchild, Macquarie University
Neuroscience Centre, Australian School of Advanced Medicine, Dow
Corning Building, 3 Innovation Rd, Macquarie University, New South
Wales 2109, Australia. Email: ann.goodchild@vc.mq.edu.au
Presented at the IVth Franco-Australian Meeting on Hypertension,
Northern Territory, Australia, September 2007. The papers in these proceed-
ings have been peer reviewed.
Received 10 October 2007; revision 18 December 2007; accepted 21
December 2007.
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Asia Pty Ltd