YSM Issue 95.1

Biomedical Engineering
FEATURE
BOMB-SNIFFING INSECTS
DECODING ODOR-EVOKED NEURAL RESPONSES IN LOCUSTS
BY ELISA HOWARD
Have you ever considered hijacking an insect? While this
may seem like an absurd idea, the notion of exploiting
an organism for its biological attributes is not all that
foreign. Take, for instance, the use of canaries in coal mines
during the 1900s. The canary acquires oxygen both when it
inhales and exhales, and this double dose of air results in the
bird’s increased vulnerability to carbon monoxide and other
poisonous gases. Thus, the health of the canary provided a means
for coal miners to understand the safety of their environment.
Professor of Biomedical Engineering Baranidharan Raman
and colleagues at the Washington University in St. Louis aim
to harness nature’s incredible biology for a different purpose:
hijacking the locust olfactory system to engineer
bomb-sniffing insects. “Through evolutionary
processes, biology has come up with these
amazing small-molecule detectors
that are present in your nose, my
nose, as well as locusts,” Raman
said. In locusts, the approximately
fifty thousand olfactory receptor
neurons (ORNs) of each antenna
convert odorants into neural signals
that funnel into the antennal lobe. “Why
not use the insect as a sensor, tap into the
neural signals while the insect is interacting
with the environment, and use those neural
signals to understand whether chemical A or
chemical B is present?” Raman asked.
In previous work, the researchers implanted electrodes to
record neural signals in the antennal lobe. They demonstrated
that those neural responses provide a fingerprint to discern
between explosive and non-explosive vapors in addition to
different types of explosive vapors. In a recent study published
in Proceedings of the National Academy of Sciences, Raman
and his team investigated how locusts recognize a particular
odorant regardless of stimulus history, dynamics, and
context. “You can smell coffee in a coffee shop, grocery shop,
or restaurant. It smells the same whether you are on the coast
or in the driest of the Sahara Desert,” Raman said. The same
is true for locusts, but how?
In the presence of an odorant, neural signals from
ORNs of the antenna drive the activity of cholinergic
projection neurons (PNs) and GABAergic local
neurons (LNs) of the antennal lobe. PNs and LNs
reformat the signal, resulting in intricate spiking patterns
among PN ensembles. Those PN patterns encode
odor intensity and identity. To test the locust’s
invariant stimulus recognition ability, the
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researchers conditioned the insects through methods
resembling that of Russian physiologist Ivan Pavlov. In the
presence of a food reward, locusts automatically open
their sensory maxillary palps. After the presentation of
an odorant followed by a food reward in six training
trials, the locusts learned to open their maxillary palps
in response to the odorant alone.
Raman and colleagues examined changes in palp
opening—an indicator of odorant recognition—in
response to perturbations, including varied stimulus dynamics,
altered stimulus history, the existence of competing cues, and
differences in ambient conditions. The results support the
hypothesis that locusts detect an odor regardless of such
perturbations. “Now we know the behavior is stable.
How stable are the neural responses?” Raman
questioned. The researchers recorded the
activity of antennal lobe PNs and found much
variability in odor-evoked firing for singleneurons
and cell ensembles. “There was
no single feature that was reliable and
robust that allowed this perception of an
odor to remain constant independent of
all these perturbations,” Raman said.
To decode the neural responses,
Raman and colleagues used a linear
classifier. The classifier assigns a weight to each
neuron and successfully predicts the presence
of an odor if the sum of weighted neurons
exceeds a threshold value. In investigating how the classifier
works, they discovered two different ensembles of neurons in the
locust olfactory system: ON neurons, active in the presence of the
stimulus, and OFF neurons, active in the absence of the stimulus.
The classifier assigns positive weights to the ON neurons and
negative weights to the OFF neurons. “When you combine the
activity of all the ON neurons while subtracting the activity
of the OFF neurons, if that sum is above a certain threshold
value, the odor is present. Simple as that,” Raman said. In fact,
a classification scheme using only ternary weights—positive one
for ON neurons, zero for non-responders, and negative one for
OFF neurons—enables robust odor recognition.
Uncovering more of locust olfaction through the study of
ON and OFF neurons, Raman and his team are one step closer
to exploiting biology’s expertise to hijack the insect olfactory
system. Next time you try to squash a bug, look closer: bombsniffing
insects are an innovation of the near future. ■
ART BY ANASTHASIA SHILOV
March 2022 Yale Scientific Magazine 25