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First, consider the cellular basis of long-term potentiation (LTP). Where in the brain does this occur and what happens? In your answer, include details of the neurotransmitters and receptors involved as well as what happens at the level of the receptor to enable LTP. Also, describe the changes that occur in both the presynaptic and post-synaptic cells as a result of LTP.
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Neuropsychiatric Disease and Treatment 2018:14 17371746

Neuropsychiatric Disease and Treatment Dovepress

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1737

O r i g i N a l r e s e a r c h

open access to scientific and medical research

Open access Full Text article

http://dx.doi.org/10.2147/NDT.S163756

changes in synaptic plasticity are associated with
electroconvulsive shock-induced learning and
memory impairment in rats with depression-like
behavior

Qibin chen1

li ren1

su Min1

Xuechao hao2

hengsheng chen3

Jie Deng1

1Department of anesthesiology,
The First affiliated hospital of
chongqing Medical University,
chongqing, 2Department of
anesthesiology, West china hospital
of sichuan University, chengdu,
sichuan, 3Ministry of education Key
laboratory of child Development
and Disorders, china international
science and Technology cooperation
Base of child Development and
critical Disorders, chongqing Key
laboratory of Pediatrics, chongqing,
Peoples republic of china

Background: Accompanied with the effective antidepressant effect, electroconvulsive shock
(ECS) can induce cognitive impairment, but the mechanism is unclear. Synaptic plasticity is

the fundamental mechanism of learning and memory. This study aimed to investigate the effect

of ECS on synaptic plasticity changes in rats with depression-like behavior.

Methods: Chronic unpredictable mild stress procedure was conducted to establish a model of
depression-like behavior. Rats were randomly divided into the following three groups: control

group with healthy rats (group C), rats with depression-like behavior (group D), and rats with

depression-like behavior undergoing ECS (group DE). Depression-like behavior and spatial

learning and memory function were assessed by sucrose preference test and Morris water test,

respectively. Synaptic plasticity changes in long-term potentiation (LTP), long-term depression

(LTD), depotentiation, and post-tetanic potentiation (PTP) were tested by electrophysiological

experiment.

Results: ECS could exert antidepressant effect and also induced spatial learning and memory
impairment in rats with depression-like behavior. And, data on electrophysiological experiment

showed that ECS induced lower magnitude of LTP, higher magnitude of LTD, higher magnitude

of depotentiation, and lower magnitude of PTP.

Conclusion: ECS-induced learning and memory impairment may be attributed to postsyn-
aptic mechanism of LTP impairment, LTD and depotentiation enhancement, and presynaptic

mechanism of PTP impairment.

Keywords: electroconvulsive therapy, learning, memory, synaptic plasticity, electrophysiology

Introduction
Depression has been ranked as the third disease burden in the world, and .1 million

people commit suicide each year due to depression.1,2 Although antidepressants are the

first-line treatment for depression, approximately one-third of patients, especially with

major or refractory depression, are not responsive to the medication.3 Electroconvulsive

therapy (ECT) is conducted as the most effective treatment for those with major or

drug-resistant depression. Nevertheless, accompanied with its excellent treatment

effect, ECT can induce learning and memory impairment, which is a major limitation

in the clinical use of ECT.4 Unfortunately, the underlying mechanism of learning and

memory impairment induced by ECT is still poorly understood.

Persistent neural modifications are widely regarded as the cellular basis for learning

and memory.5 Synaptic plasticity is the fundamental mechanism of neural modifications,

correspondence: su Min
Department of anesthesiology, The
First Affiliated Hospital of Chongqing
Medical University, No 1 Youyi road,
Yuzhong District, chongqing 400016,
Peoples republic of china
Tel/fax +86 23 8901 1068
email [emailprotected]

Journal name: Neuropsychiatric Disease and Treatment
Article Designation: Original Research
Year: 2018
Volume: 14
Running head verso: Chen et al
Running head recto: Learning and memory impairment in rats with depression-like behavior
DOI: 163756

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chen et al

and synaptic plasticity supporting learning and memory

process involves persistent changes in synaptic efficacy

such as long-term potentiation (LTP) and long-term depres-

sion (LTD).6,7 Although LTP is remarkable for its stability,

accumulative evidence revealed that LTP could be reversed if

applied shortly after LTP induction and this form of synaptic

plasticity was named as depotentiation.8 Depotentiation has

been reported in hippocampus9,10 and other brain regions

closely related to learning and memory, such as prefrontal

cortex11 and amygdala.12 Thus, it is universally accepted that

LTP, LTD, and depotentiation conduct as opposing mecha-

nisms that maintain a dynamic range of synaptic efficacy and

keep synaptic homeostasis.13,14 Our previous study found that

electroconvulsive shock (ECS, an analog of ECT to animals)

could induce LTP impairment.15 However, whether LTD

or depotentiation contributes to ECT-induced learning and

memory impairment is still unknown.

Virtually, all synapses are mediated by short-lived and

long-lasting process. Thus, besides the long-term modifica-

tions of synaptic plasticity, changes in short-term synaptic

plasticity also have an important role in learning and memory.

Post-tetanic potentiation (PTP) is a widespread form of

short-term synaptic plasticity, which suggests that synaptic

efficacy is enhanced for tens of seconds to minutes after

high-frequency stimulation (HFS) with a train of hundreds

of pulses.16 Furthermore, it has been proved that presynaptic

transmitters release is reflected by PTP.17 Our previous study

found that ECS-induced learning and memory impairment

was attributed to imbalance of hippocampal Glu/GABA.18

However, it is still unclear whether PTP is involved in the

learning and memory impairment induced by ECT. Besides,

how transmitter release influences the learning and memory

function in the model of ECS necessitates further study.

In this study, using behavioral test and electrophysi-

ological experiments, we investigate the effects of ECS on

learning and memory as well as the potential roles of LTP,

LTD, depotentiation, and PTP in this process.

Methods
animals
Healthy adult male Sprague Dawley rats (weight 200250 g,

aged 23 months) were obtained from the Laboratory Animal

Center of Chongqing Medical University. All rats were

housed at standard condition (temperature at 22C2C,
humidity at 62%3%, and 12/12 h lightdark cycle) in the
animal room. The rats were kept for 7 days acclimation

period before experiment. All experiment protocols were

approved by the Ethical Committee of the First Affiliated

Hospital of Chongqing Medical University (No 2017-004)

and conducted according to National Institutes of Healths

Guild for the Care and Use of Laboratory Animals.

rats model of depression-like behavior
As previously described, chronic unpredictable mild stress

(CUMS) procedure was conducted to establish a model of

depression-like behavior in rats.19 All rats except for those

in group C were housed in individual cages and exposed the

following stress: food deprivation for 24 h, water depriva-

tion for 24 h, continuous lighting for 24 h, tailing pinching

for 1 min, 5 min swimming in the cold water of 4C, 5 min
swimming in the hot water of 45C, shaking for 20 min,
damp sawdust for 24 h, and cages tilting to 45 for 24 h.
To avoid habituation and provide an unpredictable feature

to the stressors, all the stressors were randomly scheduled

and repeated within 4 weeks.

experiment groups and treatment
Rats were randomly divided into the following three groups:

group C includes the healthy rats without any treatment,

group D includes the depression-like behavior rats and treated

with sham ECS, and group DE includes the depression-like

behavior rats and treated with ECS. A total of 32 rats were

included for each group. ECS was conducted via bilateral

ear clip electrodes with a Niviqure ECS system (Nivique

Meditech, Bangalore, India) on the basis of following

parameters: bidirectional square wave pulses, 0.8 A in

amplitude, 1.5 ms in width, 125 Hz in frequency, and 0.8 s

in duration, and 120 mC charge. Sham ECS was conducted

as the same process with ECS but without currents. The ECS

or sham ECS was conducted once daily for 7 days.

sucrose preference test
Sucrose preference test is widely accepted to test anhedo-

nia, which is one of the core symptoms of depression to

evaluate the depression-like behavior in rats. The test was

conducted as previously described.20 The test was com-

pleted within 72 h. In the first 24 h, rats were kept with two

bottles of 1% sucrose solution to adapt sucrose consump-

tion. In the second 24 h, rats were kept with one bottle of

1% sucrose solution and one bottle of sterile water. In the

third 24 h, after water and food deprivation for 23 h, all

rats were kept with two identical and preweighed bottles

for 1 h. One bottle was filled with 1% sucrose solution, and

another bottle was filled with sterile water. After 30 min

free drinking, the position of two bottles was exchanged

to prevent the position preference. The sucrose preference

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learning and memory impairment in rats with depression-like behavior

percentage (SPP) was calculated as the following formula:

SPP (%) = sucrose consumption (g)/(water consumption [g] +
sucrose consumption [g]) 100%.

Morris water maze
It is well received that hippocampus-dependent spatial

learning and memory function of rats can be assessed by

Morris water maze.21 A circle pool (150 cm in diameter and

50 cm in height) was filled with water colored by black ink,

and a submerge platform (11 cm in diameter) was provided

below the surface of the water with ~12 cm. The pool
was divided into four quadrants, and each rat was placed

into the water randomly at one of the four quadrants to find

the hidden platform within 60 s. If the rats did not find the

platform within 60 s, they were guided to the platform with

a stick and stayed on the platform for 15 s. Each rat was

placed into the water gently from four different quadrants

once a day for 5 consecutive days. The time to find the plat-

form for each quadrant was defined as escape latency, and

average time from four quadrants of the consecutive 5 day

was analyzed. On the sixth day, the platform was removed

and rats were placed into water to swim with a limitation

of 60 s. Space exploration time, defined as swimming time

in the platform quadrant of each rat, was recorded. Escape

latency, space exploration time, and swimming speed based

on the swimming track recorded by a video track system

program (Zhenghua Instruments, Anhui, China) were ana-

lyzed. A plain experimental timeline for all behavior tests

is shown in Figure 1A.

hippocampal slice preparation
Rats were anesthetized by 2% pentobarbital sodium, and the

brain was removed gently. Hippocampal slices (400 m thick)
were cut by a vibratome (NVSLM1; WPI, Sarasota, FL, USA)

in 0C4C cutting solution oxygenated with the mix gas of

95% O
2
and 5% CO

2
. Cutting solution was configured as

follows (in millimolar): 3 KCl, 1.25 NaH
2
PO

4
, 26 NaHCO

3
,

0.4 vitamin C, 2 sodium pyruvate, 2 sodium lactate, 10 glucose,

220 sucrose, 1 MgCl
2
, 1 CaCl

2
, 1 MgSO

4
(pH 7.37.4; osmotic

pressure 300310 mOsmol/L). Slices were incubated in a

chamber filled with oxygenated recording solution at 34C
for 60 min and then incubated in identical solution at 24C
for at least 60 min before recording. Recording solution was

comprised as follows (in millimolar): 124 NaCl, 3 KCl, 1.25

NaH
2
PO

4
, 26 NaHCO

3
, 0.4 vitamin C, 2 sodium pyruvate,

2 sodium lactate, 10 glucose, 1 CaCl
2
, 1 MgSO

4
(pH 7.37.4;

osmotic pressure 300310 mOsmol/L).

electrophysiological experiment
A single hippocampal slice was placed in the recording cham-

ber and was continuously perfused with oxygenated record-

ing solution. A bipolar stimulating electrode was placed in

the stratum radiatum of CA3 region, and a glass micropipette

(resistance 23 M) filled with filtrated recording solution
was placed in the stratum radiatum of CA1 region to record

the field excitatory postsynaptic potentials (fEPSPs). Stimula-

tion intensity to evoke baseline fEPSPs was set as ~50% of
the intensity, which elicited the maximal response. As previ-

ously described, after 30 min stable baseline fEPSPs record-

ing, LTP was induced by an HFS with the parameter of 400

pulses at 100 Hz.22 To assess the magnitude of LTP, the mean

value for the slope of fEPSPs recorded at 2040 min after

stimulation was calculated and expressed as a percentage

of the mean value of the initial baseline slope of fEPSPs.

Depotentiation was induced as previously described.23 After

successful LTP induction, the same slice received a low-

frequency stimulation (LFS) (900 pulses at 1 Hz) to induce

depotentiation (depotentiation = [percentage of potentiation
after LFS 100] 100/[percentage of potentiation before
LFS 100]). For LTD induction, after stable baseline fEPSPs

CUMS
Day

SPT MWM ECS SPT MWM

28 29 31 32 36 37 43 44 46 47 51

SPT ECS EP

CUMS
Day

28 29 31 32 38 39

Figure 1 Time overview of the study.
Notes: (A) The time schedule for behavior test. (B) The time schedule for electrophysiological experiment.
Abbreviations: cUMs, chronic unpredictable mild stress; ecs, electroconvulsive shock; eP, electrophysiological experiment; MWM, Morris water maze; sPT, sucrose
preference test.

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chen et al

recording for 30 min, LTD was induced by a LFS (900 pulses

at 1 Hz).23 The calculation of LTD was similar as that of

LTP. All the poststimulation fEPSPs of LTP, depotentiation

and LTD were recorded for 60 min. PTP was induced as

previously described with minor modification.24 After 30 s

stable baseline fEPSPs recording, PTP was induced by an

HFS (400 pulses at 400 Hz) and the poststimulation fEPSPs

were recorded for 100 s. The mean value for the slope of

fEPSPs recorded at 5 s after stimulation was calculated, and

PTP was expressed as a percentage of the mean value of the

initial baseline slope of fEPSPs. All electrophysiological data

were recorded and analyzed by Axon Instruments system

(MultiClamp 700B amplifier, Digidata 1200 transverter,

pCLAMP 9.2 software; Molecular Devices LLC, Sunnyvale,

CA, USA). A scheduled timeline for electrophysiological

experiment is shown in Figure 1B.

statistical analysis
Statistical analysis was performed with SPSS (Version 17.0;

SPSS Inc., Chicago, IL, USA). All data were expressed

as mean SD. Statistical significance was determined by
repeated measures analysis of variance (data of escape latency

from Morris water maze). The other data were analyzed by

one-way analysis of variance, followed by Bonferroni cor-

rection to compare differences between the groups. P,0.05

was considered statistically significant.

Results
along with the antidepressant effect, ecT-
induced learning and memory impairment
First, we want to clear the effect of ECS on behavior

changes. Eight rats in each group were used to behavior test.

Depression-like behavior was tested by sucrose preference

test. As shown in Figure 2A, group D and group DE shown

lower SPP than group C after CUMS procedure (F=42.102,
post hoc test, P,0.001 and ,0.001, respectively). After ECS

treatment, SPP of group DE was higher than that of group D

(F=36.695, post hoc test, P,0.001); however, it showed no
difference compared with group C (post hoc test, P=0.810).
Spatial learning and memory function was tested by Morris

water maze. There was no difference in the comparison of

swimming speed for each group (data were not shown).

Escape latency decreased gradually during the 5 days training

for the three groups. However, rats in group DE spent more

0
C D DE

Groups

Sp
ac

e
ex

pl
or

at
io

n
tim

e
(s

)

Group DE

100
A B

0
Before treatment

Su
cr

os
e

pr
ef

er
en

ce
pe

rc
en

ta
ge

Es
ca

pe
la

te
nc

y
(s

)

After treatment

Days
0 1 2 3 4 5

*,#

* * *

Group C
Group D
Group DE

Group C
Group D

Figure 2 effects of ecs on depression-like behavior (A) and spatial learning and memory function (B and C).
Notes: Sucrose preference percentage is the test index of sucrose preference test, and lower sucrose preference percentage indicated more significant depression-like
behavior. escape latency and space exploration time are the test index of Morris water maze, and longer escape latency and shorter space exploration time indicated worse
learning and memory performance. group c, control group with healthy rats; group D, rats with depression-like behavior; group De, rats with depression-like behavior
undergoing ecs. *P,0.05 compared with group c; #P,0.05 compared with group D.
Abbreviation: ecs, electroconvulsive shock.

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learning and memory impairment in rats with depression-like behavior

time to find the platform than other two groups (F=111.803,
post hoc test, P,0.001 and ,0.001, respectively). Further-

more, escape latency of group D was longer than that of

group C (post hoc test, P=0.001) (Figure 2B). Data of space
exploration time suggested that group DE spent least time

to swim in the platform quadrant (F=17.394, post hoc test,
P,0.001 and 0.027, respectively). What is more, group D

showed shorter space exploration time than group C (post

hoc test, P=0.004) (Figure 2C).

ecs-induced lTP impairment and
depotentiation enhancement
To illuminate the underlying electrophysiological mecha-

nisms of learning and memory impairment induced by ECS,

LTP and depotentiation were assessed. Morris water maze

itself was a process of learning and memory. To prevent

the potential effect of Morris water maze on subsequent

electrophysiological assessment, another eight rats in each

group were included. As shown in Figure 3, baseline fEPSP

of group DE (fEPSP slope, 0.2060.196, F=85.683, post hoc
test, P,0.001) was higher than that of group C and group D.

No difference was found in the comparison of baseline

fEPSP between group C (fEPSP slope, 0.1180.014) and
group D (fEPSP slope, 0.1000.009, post hoc test, P=0.053),
although the baseline fEPSP was lower in group D. For LTP

test, group DE (normalized fEPSP slope, 129%4%) showed
lower magnitude of LTP than group D (normalized fEPSP

slope, 166%5%, F=119.934, post hoc test, P,0.001) and
group C (normalized fEPSP slope, 184%8%, post hoc
test, P,0.001). Compared with group C, the magnitude of

LTP was lower in group D (post hoc test, P,0.001). For

depotentiation test, ~50% LTP was reversed by LFS in
group C (normalized fEPSP slope, 42%7%). Compared
with group C, depotentiation was enhanced in group D

(normalized fEPSP slope, 69%5%, F=83.438, post hoc
test, P,0.001) and group DE (normalized fEPSP slope,

89%5%, post hoc test, P,0.001). Furthermore, group DE
exhibited stronger depotentiation than group D (post hoc

test, P,0.001).

ecs-induced lTD enhancement
LTD is another important form of synaptic plasticity and

also plays a central role in learning and memory. In our

experiment, group DE (normalized fEPSP slope, 58%5%)
exhibited higher magnitude of LTD compared with group D

(normalized fEPSP slope, 68%7%, F=12.438, post hoc test,
P=0.025) and group C (normalized fEPSP slope, 77%7%,

post hoc test, P,0.001). What is more, compared with

group D, the magnitude of LTD was lower in group C (post

hoc test, P=0.025) (Figure 4).

ecs-induced PTP impairment
LTP, LTD, and depotentiation are forms of postsynaptic

plasticity; however, we wanted to clear whether presynaptic

plasticity, such as PTP, was related to the learning and

memory impairment induced by ECS. As shown in Figure 5,

the magnitude of PTP of group DE (normalized fEPSP slope,

121%9%) was lower than that of group C (normalized
fEPSP slope, 150%7%, F=23.927, post hoc test, P,0.001)
and group D (normalized fEPSP slope, 140%5%, post hoc
test, P,0.001). Compared with group C, the magnitude of

PTP was lower in group D (post hoc test, P=0.034).

Discussion
The present study confirmed that along with the antidepres-

sant effect, ECS induced learning and memory impairment

in the rats model of depression-like behavior. ECS induced

synaptic plasticity changes including LTP impairment, LTD

and depotentiation enhancement, and PTP impairment in

rats with depression-like behavior, leading to learning and

memory impairment.

It has been proved that measures, such as learned

helpless,25 olfactory bulbectomy,26 maternal separation,27 and

CUMS,28 can induce depression-like behavior of rats. In our

study, depression-like behavior model was constructed by

CUMS because this model can better simulate the process

of the depression induced by environmental stress, which is

one of the most common pathogeneses of depression.29 Anhe-

donia is one the central symptoms of depression and can be

assessed by SPP for rats. In line with other study,30 our results

revealed that SPP decreased significantly after CUMS proce-

dure and ECS increased the SPP in depression-like behavior

model of rats. Additionally, we found that ECS could increase

the baseline fEPSP, which was defined as LTP-like changes

and considered as the underlying mechanism of antidepres-

sant of ECS.31,32 The trend of baseline fEPSP was consistent

with the results of SPP, indicating successful model construc-

tion and antidepressant effect of ECS.

In Morris water maze test, we found rats with depression-

like behavior undergoing ECS exhibited learning and

memory impairment. LTP and LTD are two common electro-

physiological forms of synaptic plasticity. In our experiment,

we found that ECS induced LTP impairment. In the test of

LTD, to our surprise, the magnitude of LTD in group DE was

larger than that in group D, indicating that ECS induced LTD

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chen et al

enhancement. Briefly, ECS induced LTP inhibition and LTD

enhancement. Accumulative evidence suggested that LTD or

LTP induction could be influenced by the history of synaptic

activity. This form of regulation of synaptic plasticity has

been named as plasticity of plasticity or metaplasticity,

which reveals that prime synaptic activation will suppress

subsequent LTP and facilitate LTD via LTD/LTP threshold

sliding to right.33 In the present study, ECS could induce

300

200

fE
PS

P
sl

op
e

(p
er

ce
nt

ag
e

of
b

as
el

in
e)

100

0
30 20 10 0 10 20 30 40 50

Time (min)

100 Hz, 400 pulses 1 Hz, 900 pulses

60 70 80 90 100110 120130140

Group C

1 2 3
B

300

200

fE
PS

P
sl

op
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30 20 10 0 10 20 30 40 50

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60 70 80 90 100 110 120130 140

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Figure 3 effects of ecs on lTP and depotentiation.
Notes: Baseline fePsPs were recorded for 30 min, and poststimulation fePsPs of lTP and depotentiation were recorded for 60 min. (AC) lTP and depotentiation were
recorded in each group. Original traces of fePsP were recorded, and baseline trace (trace 1), post-hFs trace (trace 2), and post-lFs trace (trace 3) were exhibited. scale
bar was set as 5 ms for the horizontal line and 1 mV for the vertical line. statistical analysis of baseline fePsP (D), lTP (E), and depotentiation (F) for different groups.
group c, control group with healthy rats; group D, rats with depression-like behavior; group De, rats with depression-like behavior undergoing ecs. *P,0.05 compared
with group c; #P,0.05 compared with group D.
Abbreviations: ECS, electroconvulsive shock; fEPSPs, field excitatory postsynaptic potentials; LTP, long-term potentiation; LFS, low-frequency stimulation; HFS, high-
frequency stimulation.

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learning and memory impairment in rats with depression-like behavior

baseline fEPSP increase, indicating synaptic activation

by ECS.31 And, our previous study also found that ECS

could upregulate the expression of pT305-CaMKII, which

is closely related to LTD/LTP threshold regulation.34 All

these results strongly suggested that ECS-induced learning

and memory impairment could not be simply explained by

synaptic plasticity. To the best of our knowledge, alternation

of regulatory capacity of synaptic plasticity or metaplasticity

contributes to learning and memory impairment induced by

ECS indeed.35

In our study, it was confirmed that rats with depression-

like behavior also exhibited learning and memory impairment

coincided with LTP impairment and LTD enhancement. Thus,

it is eligible to receive that learning and memory impairment

induced by depression and ECS involved in the regulation

of metaplasticity. In addition, our results revealed that more

serious LTP impairment and LTD enhancement were found

in group DE. In consideration of previous finding that stress

could induce LTP impairment and LTD enhancement,35,39 a

reasonable explanation is that stress of different intensities

induces different magnitudes of LTP impairment and LTD

enhancement. Acute strong enough stress, such as electronic

stimulation with ECS, will induce serious LTP impairment

and LTD enhancement; however, chronic or mild stimulation,

Figure 4 effects of ecs on lTD.
Notes: Baseline fePsPs were recorded for 30 min, and poststimulation fePsPs were recorded for 60 min. (AC) lTD was recorded in each group. Original traces of fePsP
were recorded, and baseline trace (trace 1) and poststimulation trace (trace 2) were exhibited. scale bar was set as 5 ms for the horizontal line and 1 mV for the vertical line.
(D) statistical analysis of lTP for different groups. group c, control group with healthy rats; group D, rats with depression-like behavior; group De, rats with depression-
like behavior undergoing ecs. *P,0.05 compared with group c; #P,0.05 compared with group.
Abbreviations: ECS, electroconvulsive shock; fEPSPs, field excitatory postsynaptic potentials; LTD, long-term depression;

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