a SciTechnol journal Research Article
Journal of Spine &
Neurosurgery
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Ahmed et al., J Spine Neurosurg 2013, 2:3
http://dx.doi.org/10.4172/2325-9701.1000115
International Publisher of Science,
Technology and Medicine
Spinal Cord Injury-Induced
Discharges Modify the Function
of Glutamatergic System and
Improve Ground and Skilled
Locomotor Control
Zaghloul Ahmed
1,3
*, Ahmed Hawash
3
and Andrzej Wieraszko
2,3
Abstract
Background: Recent data demonstrate that enhanced activity,
induced by spinal cord injury (SCI) may accelerate functional
recovery. This study was design to verify this assumption.
Methods: The effects of spinal cord injury with or without
pharmacological suppression of injury-induced activity were
investigated. In vivo method tested weekly locomotor activity of
the animals during 7-week post-injury period. In vitro techniques
characterized neuronal activity and properties of glutamatergic
system.
Results: The sciatic nerve activity during SCI was categorized
into sequentially occurring phases. The frst phase, represented
by mechanically-induced compound action potential, was followed
by the second phase of high frequency discharges lasting
approximately 2 min. These two phases were accompanied by
enhanced glutamate effux. The third phase lasting about 15 min
with no discharges was followed by a hyperactive fourth phase
with spasms and increased spontaneous activity. The application
of lidocaine over the spinal cord before injury attenuated phasic
activity. The ability of glutamatergic system to release glutamate
in vitro 2 h, 24 h, and three weeks after the injury (chronic stage)
from animals treated, or not treated with lidocaine was reduced, or
elevated, respectively. The effciency of glutamate uptake system in
the animals not treated with lidocaine was elevated 2 h after injury
and diminished later. In animals treated with lidocaine, the decline
in the effciency of glutamatergic system 2 h after the injury was
followed by an increase. The expression of glutamatergic AMPA
receptors in lidocaine-treated animals continued to rise from 2 h
after the injury through a chronic stage. The expression of AMPA
receptors in animals not treated with lidocaine was attenuated 2
and 24 h after the injury but elevated in the chronic stage. Blocking
injury-induced activity with lidocaine impaired locomotion recovery.
Conclusion: Neural discharges following the onset of SCI have
benefcial effects on functional recovery.
Keywords
Spinal cord; Injury-induced activity; Recovery; Lidocaine; Plasticity;
Glutamate; Behaviour
*Corresponding author: Zaghloul Ahmed, Associate Professor, Department
of Physical Therapy, 2800 Victory Boulevard, Staten Island, NY10314, USA,
E-mail: zaghloul.ahmed@csi.cuny.edu
Received: February 22, 2013 Accepted: June 20, 2013 Published: June 24,
2013
Abbreviations
AMPA: α-Amino-3-ydroxy-5-methyl-4-isoxazolepropionic acid;
BMS: Basso muscle scale; CSI: Spinal cord injury; CNS: Central ner-
vous system; D-Asp: 2,3
3
H-D-Aspartic acid; LTP: long-term poten-
tiation; mCAP: Mechanically-induced compound action potential;
NMDA: N-methyl –D-aspartic acid; VGCC: Voltage gated calcium
channel
Introduction
Te injury of the spinal cord evokes intense neuronal activity
of the spinal neurons. It has been always assumed that this
excessive activity, correlated with a massive release of excitatory
neurotransmitter, glutamate would impair functional recovery
[1]. Tis assumption constituted a base for developing many
pharmacological treatments for acute spinal cord injury (SCI) aimed
at reduction of this hyperactivity. However, the idea of detrimental
efects of hyperactivity is challenged by the data demonstrating
that neuronal activity following injury may be benefcial for tissue
regeneration [2] and functional recovery [3,4] activating intrinsic
neuronal mechanism.
It is well known that brief but intense activity in the nervous
system may lead to long-lasting physiological and structural changes
in neurons. Examples include long-lasting increase in synaptic
efciency expressed as Long-Term Potentiating (LTP) [1], rapid
changes of intrinsic neuronal excitability [5-10], enhanced sensitivity
of postsynaptic membranes at individual synapses [11], and fnally an
increase in the number of active synapses, silent prior to enhanced
activity [8]. All these changes represent neuronal plasticity which has
been recognized as the most important phenomenon involved not
only in the mechanisms of memory [12], but also recently implicated
as one of the processes contributing to recovery afer damage in the
central nervous system (CNS) [13].
Te spinal cord injury-induced discharges propagate quickly
along spinal nerves and were shown to be correlated with long-term
alterations in the spinal neurons and modifcation of behaviour.
Among others, an increase in the expression of Fos protein [14],
the voltage gated calcium channel (VGCC) [15], and triggering of
autotomy (self-injury) [1,16,17] have been reported. Although these
discharges are routinely observed as spasms at the onset of SCI in
animals, their quantifcation, characteristics, and their efects on
behavioural recovery are rarely investigated.
Most of spinal cord injuries are incomplete, sparing some
functional connections [18] which could constitute anatomical
substrate for functional recovery. We hypothesized that SCI
by triggering an intense neuronal activity [15] would activate
mechanisms involved in just described mechanisms of neuronal
plasticity. Subsequently, the efcacy of spared connections between
the injured spinal neurons would be enhanced initiating long-term
processes leading ultimately to a better recovery. In order to evaluate
the role of neuronal activity in the recovery process we compared
the efects of spinal cord injury in animals, or in the tissue from the
animals expressing injury-induced activity with the preparations
where post-injury activity was attenuated by application of lidocaine.