Altered neuronal activity in the primary motor cortex and globus pallidus
after dopamine depletion in rats
☆
Min Wang
a,
⁎, Min Li
a,1
, Xiwen Geng
a,1
, Zhimin Song
b
, H. Elliott Albers
b
, Maoquan Yang
a
, Xiao Zhang
a
,
Jinlu Xie
a
, Qingyang Qu
a
, Tingting He
a
a
Key Laboratory of Animal Resistance of Shandong Province, College of Life Science, Shandong Normal University, Jinan 250014, People's Republic of China
b
Center for Behavioral Neuroscience, Neuroscience Institute, Georgia State University, Atlanta, GA 30302, United States
abstract article info
Article history:
Received 11 September 2014
Received in revised form 9 November 2014
Accepted 10 December 2014
Available online 18 December 2014
Keywords:
Parkinson's disease
Local field potential
Motor cortex
Globus pallidus
Basal ganglia
Microelectrode
The involvement of dopamine (DA) neuron loss in the etiology of Parkinson's disease has been well documented.
The neural mechanisms underlying the effects of DA loss and the resultant motor dysfunction remain unknown.
To gain insights into how loss of DA disrupts the electrical processes in the cortico-subcortical network, the pres-
ent study explores the effects of DA neuron depletion on electrical activity in the primary motor cortex (M1), on
the external and the internal segment of the globus pallidus (GPe and GPi respectively), and on their temporal
relationships. Comparison of local field potentials (LFPs) in these brain regions from unilateral hemispheric DA
neuron depleted rats and neurologically intact rats revealed that the spectrum power of LFPs in 12–70 Hz (for
M1, and GPe) and in 25–40 Hz (for GPi) was significantly greater in the DA depleted rats than that in the control
group. These changes were associated with a shortening of latency in LFP activities between M1 and GPe, from
several hundred milliseconds in the intact animals to close to zero in the DA depleted animals. LFP oscillations
in M1 were significantly more synchronized with those in GPe in the DA depleted rats compared with those in
the control rats. By contrast, the synchronization of oscillation in LFP activities between M1 and GPi did not differ
between the DA depleted and intact rats. Not surprisingly, rats that had DA neuron depletion spent more time
along the ladder compared with the control rats. These data suggest that enhanced oscillatory activity and in-
creased synchronization of LFPs may contribute to movement impairment in the rat model of Parkinson's disease.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
The basal ganglia form a complex network that processes cortical in-
formation important for movement and cognition [1–3]. Alterations of
neuronal activity in the basal ganglia and cortices have been reported
in patients with Parkinson's disease (PD) as well as in animal models
of PD [4–11]. These changes in neuronal activity are believed to mediate
many of the dysfunctional effects seen in PD because they impact the
circuits connecting the basal ganglia and the cortex [10,12–14]. Howev-
er, the specific pathological changes that occur with DA loss in oscilla-
tion activity and functional connectivity from the cortex to the basal
ganglia remain poorly understood.
The transmission of rhythmic cortical activity from the cortex to the
basal ganglia has been studied in anesthetized rats [15,16]. An increase
in discharge oscillations at 1 Hz from the basal ganglia is observed in
anesthetized rats with unilateral DA depletion. This activity is coherent
with the 1 Hz oscillatory firing patterns dominant in the cortex [17,18].
Transmission from the cortex to the basal ganglia has also been studied
in rats using electrical stimulation of the motor cortex. After DA deple-
tion, the cortical stimulation induces a long disinhibition in GPe,
which is transmitted to GPi and generates an abnormally strong long
inhibition in GPi, which then generates a strong and long excitation in
the thalamic projection sites that are transmitted to the motor cortex
with incorrect information [19,20].
Simultaneous behavioral recordings and chronic microelectrode
neural recordings in awake and behaving rodents hold great promise
to study the neural bases of behavior and the information transmission
between the cortex and the basal ganglia. Some studies suggest that
increases in the synchronization between the subthalamic nucleus or
substantia nigra to cortex, or the external segment of the globus pallidus
facilitate the emergence of special range activity in the cortex after DA
loss [10,11,21–23]. These observations led to our general hypothesis
that DA neuron loss alters the magnitude of the electrical activities in
Journal of the Neurological Sciences 348 (2015) 231–240
☆ Supporting grant: This study was supported by the Natural Science Foundation of
Shandong Province (No. ZR2010CM055) and the Science and Technological Project of
Shandong Province (Nos. 2011GGB01004 and 2010GGX10133).
⁎ Corresponding author at: Department of Anatomy and Physiology, College of Life
Science, Shandong Normal University, 250014, People's Republic of China. Tel.: +86
15615614667.
E-mail address: wangmin78@yahoo.com (M. Wang).
1
Contributed equally.
http://dx.doi.org/10.1016/j.jns.2014.12.014
0022-510X/© 2014 Elsevier B.V. All rights reserved.
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