DIFFERENCES IN STRIATAL SPINY NEURON ACTION POTENTIALS
BETWEEN THE SPONTANEOUSLY HYPERTENSIVE AND
WISTAR-KYOTO RAT STRAINS
T. L. PITCHER, J. R. WICKENS AND J. N. J. REYNOLDS*
Basal Ganglia Research Group, Department of Anatomy and Struc-
tural Biology, School of Medical Sciences, University of Otago, PO Box
913, Dunedin 9054, New Zealand
Abstract—The spontaneously hypertensive rat (SHR) and the
Wistar-Kyoto (WKY) inbred rat strains display behavioral dif-
ferences characterized by relative increases and decreases
in levels of activity. Both strains have subsequently been
utilized as animal models of hyperactive and hypoactive be-
havioral traits. The etiology of these behavioral characteris-
tics is poorly understood, but may stem from alterations in
the physiology of selected neural circuits or catecholamine
systems. This study investigated the cellular properties of
neurons from three genetically related strains: the SHR;
WKY; and Wistar (WI). In vivo intracellular recordings were
made under urethane anesthesia from spiny projection neu-
rons in the striatum, a brain area involved in behavioral acti-
vation. Results obtained from 71 spiny projection neurons
indicate that most cellular properties of these neurons were
very similar across the three strains. However, the amplitude
and half-duration of both spontaneously occurring and cur-
rent-evoked action potentials were found to be significantly
different between the SHR and WKY strains with neurons
from the SHR firing action potentials of relatively greater
amplitude and shorter duration. Action potential parameters
measured from the WI rats were intermediate between the
two other strains. These differences in action potentials be-
tween two behaviorally distinct strains may reflect altered
functioning of particular membrane conductances. © 2007
IBRO. Published by Elsevier Ltd. All rights reserved.
Key words: SHR, WKY, striatum, urethane-anesthetized, in-
tracellular recording.
The spontaneously hypertensive rat (SHR) was developed
as an inbred strain to model aspects of human hyperten-
sion (Okamoto et al., 1972). During the selective breeding
for high blood pressure, a number of behavioral character-
istics were also fixed in the SHR genome. Some of these
behavioral characteristics resemble those displayed in at-
tention deficit hyperactivity disorder (ADHD) (Sagvolden et
al., 1993, 1998). Interestingly, another genetically related
strain, the Wistar-Kyoto (WKY) also displays abnormal
behaviors and has subsequently been proposed as a
model of depression (Pare, 1994; Malkesman et al., 2006).
These strains are generally described as being hyperac-
tive (SHR) and hypoactive (WKY), thus being at the oppo-
site ends of the behavioral continuum.
The etiology of these behavioral anomalies is not
known. However, some characteristics may be explained
by alterations in dopamine functioning within the CNS
(Viggiano et al., 2003). Alterations have been reported in
both the SHR and WKY dopaminergic systems (Kujirai et
al., 1990; Linthorst et al., 1991; Kirouac and Ganguly,
1993; Russell et al., 1995; Watanabe et al., 1997; Jiao et
al., 2003; Mill et al., 2005). Whether a direct consequence
of this altered dopamine function or not, differences in the
physiology of brain areas involved in generating behavioral
output could underlie the behavioral differences reported in
these strains.
The basal ganglia is a neural circuit intimately involved
in motor activity. The input nucleus of the basal ganglia,
the striatum (caudate nucleus and putamen) receives ex-
tensive inputs from widespread areas of the cortex (Mc-
George and Faull, 1989). Cortical information is processed
in the striatum and output signals are sent via the spiny
projection neurons to either the globus pallidus external
segment (indirect pathway) or the globus pallidus internal
segment (entopeduncular nucleus in rodents) or substantia
nigra pars reticulata (direct pathway). Information is then
relayed through the thalamus to the motor areas of the cor-
tex. Information processing in the striatum is important for
selection and initiation of motor sequences. Disruption of the
striatal circuits, such as after the loss of dopaminergic inputs
in Parkinson’s disease or degeneration of striatal neurons in
Huntington’s disease, results in disorders dominated by mo-
tor abnormalities. Thus, variation in normal spiny projection
neuron activity, mediated by alterations in cellular properties
may also affect information flow through the basal ganglia
and therefore, motor activity.
The present study utilized in vivo intracellular recording
techniques to investigate the cellular properties of striatal
spiny projection neurons in three rat strains: the SHR, a
commonly used model of ADHD-like behaviors; the WKY,
the normotensive genetic control for SHR and the standard
albino Wistar (WI) strain. The purpose of the study was to
investigate if there were, at the cellular level, physiological
correlates to behavior.
EXPERIMENTAL PROCEDURES
Experimental subjects
Animals from the SHR, WKY and WI strains were obtained from
the University of Otago Animal Facility (Dunedin, New Zealand).
*Corresponding author. Tel: +64-3-4795781; fax: +64-3-4797254.
E-mail address: john.reynolds@stonebow.otago.ac.nz (J. N. J. Reyn-
olds).
Abbreviations: ADHD, attention deficit hyperactivity disorder; AHP,
afterhyperpolarization; ANOVA, analysis of variance; SHR, spontane-
ously hypertensive rat; WI, Wistar; WKY, Wistar-Kyoto.
Neuroscience 146 (2007) 135–142
0306-4522/07$30.00+0.00 © 2007 IBRO. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuroscience.2007.01.003
135