ISSN: 2167-0501 BCPC, an open access journal Psycho- and Neuropharmacology Biochem & Pharmacol
Research article Open Access
Shin et al., Biochem & Pharmacol 2013, S1
DOI: 10.4172/2167-0501.S1-006
Introduction
Seizures results from uncontrolled, synchronous cortical activity
[1], which is thought to be caused by synaptic hyperexcitability [2].
Excessive excitatory glutamate release or reduced inhibitory GABA
release has been implicated in hyperexcitability and uncontrolled
neuronal activity, resulting in seizures and ultimately epilepsy. Epilepsy
is characterized by spontaneous, recurrent seizures. When the balance
of inhibition-excitation is disrupted, epileptiform seizures develop
[3,4]. GABA release plays a vital role in maintaining a sensitive balance
of excitation-inhibition. GABA receptor antagonists have been found to
yield epileptogenic seizures [5] and enhanced GABA receptor-mediated
auto-inhibition can prevent hyperexcitability [6].
Animal models have proven to be efective in studying epilepsy in
humans [7]. Te kindling model is a physiologically-relevant model
of epileptogenesis [8]. Kindling is accomplished through repeated
electrical stimulation to discrete structures in the brain [9], which
leads to a state of persistent hyperexcitability [10]. Te frst stimulation
typically evokes a local afer discharge, which is of relatively short
duration and elicits minimal behavioral efects. However, with repeated
stimulations, seizures progress in duration, severity and distribution
[11,12], transitioning from focal, non-overt seizures to generalized
motor seizures [10]. Kindling not only results in generalization of
seizure activity, but also results in a permanent state of excitability
due to plasticity, or complex reorganization of circuitry [11]. Kindling
facilitates determinations regarding site of action [8], and allows for
the unambiguous study of anticonvulsant drugs [13], as no other drugs
are present in the brain to complicate interpretations regarding specifc
drugs efects, as is ofen the case with chemically-induced seizures.
Such is the case with stimulation of the perforant path, the primary
excitatory neocortical input to the dentate gyrus of the hippocampus
[14]. It is well-known that repeated stimulation of the perforant path
for several days induces sub-clinical, and ultimately, full-clinical
seizures. In this kindling model of epilepsy-induction, current is
administered directly to the perforant path, allowing neural circuitry
to behave independently of drug or other physiological elements. Te
dentate gyrus is susceptible to seizures because of its intrinsic circuitry
that allows oscillatory feedback excitation. Presumably, when GABA
inhibition is compromised, feedback-excitation via recurrent excitatory
interneurons becomes open-loop, resulting in an oscillation of synaptic
and neuronal activity. Tese afer discharges have shown to elicit
spreading of uncontrolled neuronal fring to other areas of the CNS
with subsequent stimulations to the perforant path.
Because of their inherent ability to rapidly connect and synchronize
networks of neurons, gap junction (GJs) have stimulated a lot of recent
interest in epilepsy research. Gap junctions are pores constructed
between cells from approximately 20 members of the connexin (Cx)
protein family by aggregation of six Cx proteins, forming a connexon
which associates with a connexon on a neighboring cell [15].
Tese pores allow for the coupling of membrane voltages between
neighboring neurons [16], thereby providing a means for intercellular
*Corresponding author: Scott C Steffensen, Department of Psychology (SWKT
1050), Brigham Young University, Provo, UT 84602, USA, Tel: (801) 422-9499;
Fax: (801) 422-0602; E-mail: scott_steffensen@byu.edu
Received March 02, 2013; Accepted April 15, 2013; Published April 18, 2013
Citation: Shin SI, Andersen DJ, Hansen DM, Yorgason JT, Schilaty ND, et al. (2013)
Connexin-36 Knock-Out Mice have Increased Threshold for Kindled Seizures:
Role of GABA Inhibition. Biochem & Pharmacol S1: 006. doi:10.4172/2167-0501.
S1-006
Copyright: © 2013 Shin SI, et al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and
source are credited.
Abstract
Blockade of gap junctions (GJs) has been shown to reduce seizures in different epilepsy models. Gap junction-
mediated, electrically-coupled neuronal networks have been implicated in neuronal synchronization, which is the
hallmark of seizure activity. To further understand the role of GJs in seizures, in particular hippocampal seizures, we
evaluated electrophysiological responses in the dentate gyrus subfeld of the hippocampus, including GABA-mediated
recurrent inhibition, seizuregenic stimulation, and seizure activity in response to perforant path kindling in Cx36 knock-
out (KO) mice compared to wild-type (WT) controls. In anesthetized mice, Cx36 KO mice were characterized by
enhanced GABA-mediated recurrent inhibition. Stimulation of the perforant path at 10 Hz for 10 sec (i.e., 100 pulses)
markedly enhanced population spike (PS) amplitudes and reduced paired-pulse GABA-mediated inhibition during the
stimulation, induced an after discharge for approximately 10 sec at 7-10 sec into the stimulation, and suppressed PS
amplitudes postictally for 5-10 min in both KO and WT mice. Repeated epochs of 10 Hz for 10 sec stimulation of the
perforant path at 20 min intervals resulted in progressive and persistent disinhibition of paired-pulse responses in
WT, but not KO mice. In freely-behaving seizure studies, stimulation of the perforant path (10 Hz for 10 sec) once/day
resulted in progressive Stage I-IV seizures in both WT and KO mice. Once Stage IV was achieved, another Stage IV
seizure could be elicited each day with the same behavioral response (i.e., Stage V). The threshold for kindled seizures
was signifcantly greater in KO mice compared to WT controls for most stages of seizures. The Cx36 antagonist
mefoquine (MFQ) and the typical anticonvulsant pentobarbital reduced Stage IV seizures in both WT and KO mice.
Knock-out mice were more sensitive to the anti-epileptic effects of the typical anti-convulsant pentobarbital (20 mg/
kg). Taken together, these fndings support the emerging view that reduction in GJ-mediated GABA electrical coupling
reduces seizures, perhaps through enhancement of GABAergic feedback inhibition, which results from the uncoupling
of the GABA recurrent interneurons from the resistive load that is inherent in their electrical connectivity.
Connexin-36 Knock-Out Mice have Increased Threshold for Kindled
Seizures: Role of GABA Inhibition
Samuel I Shin, Dallin J Andersen, Micah Hansen D, Jordan T Yorgason, Nathan D Schilaty, David D Busath and Scott C Steffensen*
Department of Psychology and Neuroscience Center, Brigham Young University, Provo, UT 84602, USA
B
i
o
c
h
e
m
i
s
t
r
y
&
P
h
a
r
m
a
c
o
l
o
g
y
:
O
p
e
n
A
c
c
e
s
s
ISSN: 2167-0501
Biochemistry & Pharmacology: Open
Access