A neonicotinoid pesticide affects the firing properties of ... · The locust (Locusta migratoria) is one of the most devastating agricultural pests due to its ability to form high-density,
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• Imidacloprid alters the response of the DCMD to looming stimuli
• Agonizes nAChRs on the DCMD or upstream neurons (LGMD,
sensory cells)
• Bimodal response types:
• Responders: four phases of imidacloprid effect
• Non-responders: pre-response and recovery phases only
• Phases of imidacloprid effect:
• Pre-response: resembles control approaches, characterized by a
short decay phase, and maximum firing rate ~ 0.03s before TOC
• Hyperexcitation: high frequency, tonic firing of DCMD, not in
response to stimulus
• No response: DCMD ceases firing for a period
• Recovery: DCMD responds to stimulus, but PSTH characterized
by long decay phase, later peak time, and lower maximum rate.
• Long decay phase suggests imidacloprid alters inhibitory network.
• Future research:
• Rising phase of PSTH (appears to shorten in recovery phase)
• Longer-term effects of imidacloprid and metabolites
Since their introduction in the 1990s, neonicotinoids have been
commercialized as a miracle pesticide with low toxicity to mammals, low
risk of bioaccumulation, high toxicity to target insects, and convenient
function as systemic pesticides.1 Recently neonicotinoids have been
receiving negative attention due to their effects on non-target organisms,
especially birds and bees.2 Neonicotinoids are nicotine mimics, and act as
agonists to nicotinic acetylcholine receptors (nAChRs) present on insect
neurons.3
The locust (Locusta migratoria) is one of the most devastating agricultural
pests due to its ability to form high-density, mobile swarms.4 While the
locust is not a typical target organism for neonicotinoid pesticides, it is a
model organism in neuroethology. Two widely studied pairs of neurons,
which code visual information from each of the locust’s eyes and synapse
downstream with muscles involved with flight and jumping, are especially
sensitive to looming stimuli.5-7 Each lobula giant movement detector
(LGMD) receives visual information from the sensory cells of the
ommatidia, and synapses directly with the descending contralateral
movement detector (DCMD) at a one-to-one ratio.8
The present study aimed to determine if the neonicotinoid imidacloprid has
an effect on the response of the DCMD to a looming stimulus. If
imidacloprid binds to the DCMD or other upstream neurons, then the firing
rate and other response parameters may be altered.
1. INTRODUCTION
4. FIRING PROPERTIES
3. RAW TRACES & PERISTIMULUS TIME HISTOGRAMS 5. HISTOGRAM SHAPE PROPERTIES
6. SUMMARY
7. ACKNOWLEDGEMENTS & REFERENCESAcknowledgements
Funding provided by Department of Biology at the University of Saskatchewan for the summer of
2014. Thank you to Glyn McMillan for countless hours of advice and guidance.
References1. Bonmatin, J. M., et al. (2015). Environmental fate and exposure; neonicotinoids and fipronil. Environ. Sci. Pollut. Res. 22, 35–67.
2. Main, A. R., Headley, et al. (2014). Widespread use and frequent detection of neonicotinoid insecticides in wetlands of Canada’s Prairie Pothole Region. PLoS One 9,
e92821.
3. Tomizawa, M. and Casida, J. E. (2005). Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45, 247–68.
4. Burrows, M. (1996). The neurobiology of an insect brain. New York, NY: Oxford University Press Inc.
5. Judge, S. and Rind, F. (1997). The locust DCMD, a movement-detecting neurone tightly tuned to collision trajectories. J. Exp. Biol. 200, 2209–2216
6. Gabbiani, F., Krapp, H. and Laurent, G. (1999). Computation of object approach by a wide-field, motion-sensitive neuron. J. Neurosci. 19, 1122–1141.
7. Gray, J. R., Robertson, R. M. and Lee, J. K. (2001). Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response
to head-on visual stimuli in locusts. J. Comp. Physiol. A Sensory, Neural, Behav. Physiol. 187, 115–129.
8. Rind, F. C. (1984). A chemical synapse between two motion detecting neurones in the locust brain. J. Exp. Biol. 110, 143–167.
A neonicotinoid pesticide affects the firing properties of a looming-sensitive neuron in Locusta migratoria
Rachel Parkinson and John R. Gray, Dept. Biology, University of Saskatchewan
0
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-1.5 -1 -0.5 0 0.5
Fre
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ikes
/s)
Time Relative to TOC (s)
Decay phase
Peak
Peak width
at half height
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-1.5 -1 -0.5 0 0.5
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ikes
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Pre-response
Hyperexcitation
Recovery
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Control
A B
C A: Raw trace and peristimulus time histogram (PSTH)
for a control loom. Maximum firing rate, peak time,
peak width at half height (Pw½h), and decay phase
marked.
B: Raw traces and PSTH overlays for three phases of
imidacloprid effect: pre-response (resembles control);
hyperexcitation; (sporadic firing); and recovery. Not
pictured: no response phase (inactivity of DCMD).
C: PSTH overlays of one recovery phase loom from
each animal (n=23) and all control looms (T01)
(n=96). Recovery phase characterized by a long decay,
lower peak, and slightly later peak time for the
recovery looms.
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200
T01 T02 T03 T04 non T04 respond.0
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T01 T02 T03 T04
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-0.06
-0.04
-0.02
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0.02
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T01 T02 T03 T04 non T04 respond.
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C
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T01 T02 T03 T04 non T04 respond.
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T01 T02 T03 T04
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Max.
firin
g r
ate
(%
mea
n c
on
trol)
0 20 40 60 80 0 20 40 60 80Approach time (minutes)
0 20 40 60 80Approach time (minutes)
# S
pik
es (
% m
ean
con
trol)
# S
pik
es (
% m
ean
con
trol)
250
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50
0
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Max.
firin
g r
ate
(n
orm
.)
Treatment Group
Treatment Group
T01 T02 T03 T04 non T04 respond. T01 T02 T03 T04 non T04 respond.
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0
0.15
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tim
e r
elati
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o T
OC
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OC
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T01 T02 T03 T04Treatment Group
T01 T02 T03 T04
T01 T02 T03 T04 T01 T02 T03 T04
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Approach time (minutes)
Dec
ay
ph
ase
(%
mea
n c
on
trol)
T01 T02 T03 T04 non T04 respond.
0 20 40 60 80
Approach time (minutes)
T01 T02 T03 T04Treatment Group
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wid
th a
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alf
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ase
(%
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trol)
T01 T02 T03 T04 T01 T02 T03 T04 A B
A: Pw½h for all animals, normalized as a percent of the mean of T01, versus approach time, and
means (top). T04 responders display a decrease in Pw½h within 10 minutes of injection, followed by a
partial or full recovery. Significance of is denoted by alternate letter (bottom).
B: Decay phase for all animals versus approach time, and mean (top). Throughout T04 the decay phase
lengthens for all animals (bottom)
120
80
40
0Pw
½h
(%
mean
con
trol)
a a a ab
a a a
b
a aa
ab
a abb
c
d
aa a
b
2. METHODS
A
B
C
Treatment Description# approaches
(2.5 min apart)
T01 After 20 minutes acclimation 5 (0-10 min)
T02 After piercing cuticle with
microsyringe
5 (12.5-22.5 min)
T03 After injecting 200 µl saline 5 (25-35 min)
T04 After injecting 200 ng
imidacloprid in 200 µl saline
15 to 20 (37.5 min
onwards)
Injection
site
A: Maximum firing rate per approach, normalized as
a percent of the mean of T01, versus approach time.
Bimodal responses occurred (means plotted). Half of
animals experienced a sharp decrease in firing rate
within 10 minutes of injection of imidacloprid,
which then recovered to near or slightly lower than
pre-injection rates (top). Means of each group in
bold. Significance denoted by alternate letter
(bottom).
B: Number of spikes (normalized) versus approach
time for all animals, and mean (top). Similar
bimodal response types observed, but with increased
variability between treatment groups (bottom).
C: Peak time in relation to TOC as a function of
approach time for all animals, plus mean.
Throughout T04 peak time approaches TOC, with
the median of T04 significantly later than all other
groups (bottom).
DCMD
recordings
Stimulus
generation
LCD
projector
Video signal
Synch.
pulses191.5 cm
12 cm
Locust
Rear projection
dome screen
Data collection
and analysis
Rigid tetherSingle hook electrode
0º
180º
600 cm
90º7 cm
300 cm s-1
Approach time (minutes)
140
100
60
20
0
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