SummaryA new study reveals an unanticipated role for social context in driving group behavior of a solitary species to a sensory stimulus and is mediated by mechanosensory neurons signaling touch interactions among individuals

Frye, Mark A.

Wasserman, Sara M.

Elsevier - Publisher Connector 

Group Behavior: Social Context Modulates Behavioral Responses to Sensory Stimuli 

A new study reveals an unanticipated role for social context in driving group behavior of a solitary species to a sensory stimulus and is mediated by mechanosensory neurons signaling touch interactions among individuals

Wasserman, Sara M

Frye, Mark A

eScholarship - University of California

Group Behavior: Social Context Modulates Behavioral Responses to Sensory Stimuli

Current Biology
DispatchesNewmethods used to analyze genomic
data, such as PSMC, are a rich resource
for probing various questions, including
the presumed effects of climatic
fluctuations on various taxa. Indeed,
while these data can only tell us so
much, our ignorance of these remote
historical times is ebbing. The study of
Nadachowska-Brzyska et al. [3]
represents thirty-eight small steps
towards a more holistic understanding
of how organisms have responded to
environmental changes in the past.
Hopefully the addition of new genomic
data frommany other species will provide
an even more in-depth treatment of these
important questions.
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46, 919–925.Group Behavior: Social Context Modulates Behavioral
Responses to Sensory StimuliSara M. Wasserman and Mark A. Frye
Howard Hughes Medical Institute, Department of Integrative Biology and Physiology, University of California, Los Angeles, CA 90095, USA
Correspondence: smwasser@ucla.edu (S.M.W.), frye@ucla.edu (M.A.F.)
http://dx.doi.org/10.1016/j.cub.2015.03.052
A new study reveals an unanticipated role for social context in driving group behavior of a solitary species to a
sensory stimulus and is mediated by mechanosensory neurons signaling touch interactions among
individuals.A hallmark of the brain is that a singular
input does not always elicit the same
output; rather a given input might produce
a variety of outputs depending on the
current internal behavioral, and external
states of the animal. This makes sense,
as in order to generate a contextually
appropriate behavioral response, an
organism must not only objectively
discriminate salient sensory stimuli from
background noise, but also must assign
value or valence to those stimuli, and it is
these subjective evaluations that dependon the context or ‘state’ of the individual.
While there exists a strong foundation of
experimental and theoretical evidence
across species for collective behavioral
dynamics aiding in the navigation of
sensory cues [1–3], we have a relatively
poor understanding of the molecular and
circuit machinery that drive such
interactions. A recent study by Ramdya
et al. [4] adds to the growing evidence for
external state modulation of behavior by
showing how social context modulates
reactions to a characteristic sensorysignal within the solitary vinegar fly
Drosophila melanogaster.
Ramdya et al. [4] discovered a peculiar
‘herd effect’ in flies exposed to carbon
dioxide (CO2), which has been shown to
drive a robust aversive escape response
in walking flies [5,6]. To their surprise, they
found that solitary flies only weakly avoid
CO2, and that only a group of flies strongly
avoid the CO2. This finding is broadly
reminiscent of a classic study on human
group behavior in which subjects were
asked to take a written test. Smoke was2015 Elsevier Ltd All rights reserved R467
Current Biology
Dispatchesthen pumped through the ventilation
system. If there was only one test subject,
75% of the time the subject calmly left the
room and reported the smoke. For a test
group of three or more, only 10% of the
time did somebody get up and report the
smoke, even though the room became
hazy with smoke that provoked coughing
[7]. Ramdya et al. [4] use the CO2
behavioral paradigm alongside
computational modeling, genetic
mutations, neuronal silencing, and
optogenetic activation to begin to dissect
apart the molecular and neuronal
mechanisms that enable a sensory
stimulus to elicit differential behavioral
outputs in a population-density
dependent manner.
Ramdya et al. [4] developed an
automated behavioral assay whereby
they could observe freely-walking
individuals or groups of flies presented
with air on one side and CO2 on the other
side of a two-choice olfactory arena. Flies
were left to wander around in the arena,
and the authors measured the fraction of
time an animal spent on the air side of the
arena versus the CO2 side. Interestingly,
flies that were tested individually spent
very little time avoiding the CO2. When
tested in a group, however, as the
population density increased so too did
the time spent avoiding the odor.
Additionally, the authors revealed that, at
the population density that drove peak
aversion, flies moved in a more uniform
direction away from the odor source.
In order to gain a better understanding
of whether individuals could be driving the
observed group behavior, Ramdya et al.
[4] next looked more closely at the
locomotion patterns of singular flies and
observed that most flies began walking
away from CO2 only after they came
within contact of another fly, termed an
‘Encounter Response’. As would be
expected, the number of Encounter
Responses increased with population
density, and bouts of walking initiated by
such an encounter were significantly
longer in duration than bouts initiated
spontaneously by solitary flies. This
finding led Ramdya et al. [4] to
hypothesize that inter-fly interactions are
responsible for generating the ‘herd’
aversion to CO2 observed in a group of
flies.
Ramdya et al. [4] next devised a
computational simulation incorporatingR468 Current Biology 25, R448–R469, June 1three observations from the behavioral
experiments: that flies initiate more
spontaneous bouts of walking in the
presence of an aversive odor; that flies are
more likely to turn and retreat when
entering the odor zone from the air zone;
and that an Encounter Response is
initiated when a stationary fly comes into
close contact with another fly. Their
compound model recapitulated the
collective behavior observed
experimentally, and modulating the
probability of an Encounter Response
alone could abolish and even invert
(aversion to attraction) collective
behavior. This computational and
experimental evidence led the authors to
predict that the inter-fly interaction is the
cornerstone of the group avoidance
response.
How do these inter-fly interactions
drive herd aversion to CO2? Walking flies
initiated Encounter Responses in
stationary flies through leg touches,
which resulted in a stereotyped walking
reaction depending upon which leg was
contacted. Ramdya et al. [4] tried various
manipulations to the visual and chemical
environment, but the only sensory
modality manipulation that caused a
disruption of Encounter Response
frequency was genetic ablation of the
NOMPC [8,9] mechanosensory channel,
adding support to the observation
that inter-fly touch interactions drive
group behavior. To confirm that
mechanical stimulation of the leg was
by itself sufficient to elicit Encounter
Responses, they substituted a magnet-
controlled metallic disc in place of a
second fly. Walking responses elicited
by the disc were indistinguishable
from those elicited by normal fly–fly
Encounter Responses, suggesting that
mechanosensory stimulation is indeed
sufficient to generate Encounter
Responses, implicating somatotopic
neural circuits that relay touch stimuli
to the brain centers controlling
locomotion.
To study the underlying neural circuit,
Ramdya et al. [4] found that genetically
silencing leg mechanosensory neurons
resulted in a significant decrease in
Encounter Response frequency,
suggesting that these structures are alone
driving the ‘herd’ effect. The authors then
used optogenetics to activate the
mechanosensory structures in the leg and, 2015 ª2015 Elsevier Ltd All rights reservedobserved Encounter Response-like
locomotion, confirming that these
structures are not only necessary for the
herd effect to occur, but also sufficient to
cause it. How can a mechanosensory
stimulus cause the group-mediated
aversion to CO2? The authors reckoned
that either touch increases awareness to
the olfactory stimulus or touch elicits an
odor-independent ‘following reaction’ to
the group. To discriminate these two
possibilities, they genetically inactivated
the known CO2 sensing receptors
[6,10,11] and found, surprisingly, that
when intermingled within genetically
wild-type confederates, even the
CO2-anosmic flies avoided CO2 in a
group-size dependent manner.
Onewonders whether the flies aremore
apt to generally follow one another around
than to specifically avoid CO2, or whether
reactions to this odorant are strongly
context-dependent. Previous work has
shown that CO2 elicits behavioral
reactions ranging from aversion [5,6] to
attraction [12,13] to responses in between
[14]. The spectrum of value assignments
mirrors the ecological roles that CO2 is
known to play in the daily life of the fly,
ranging from indicating the presence of an
attractive food source on the wing [15] to
signaling danger as a co-indicator of fly
stress pheromone [5,16]. Because CO2
has the potential to evoke different value
assignments, it makes for an ideal
candidate stimulus with which to examine
the potential effects of social context as a
measure of how external contextual state
can modulate the value and salience of
sensory information.
Ramdya et al. [4] used an elegant
combination of tools to reveal a novel
circuit that drives collective behavior in
the solitary fly, but their results leave open
the question of how the cascade is
initiated in the first place. Indeed, they
indicate that some flies are more sensitive
to the stimulus than others and therefore
begin to walk more readily, which would
initiate collective aversion. Also,
sensitivity to the odorant is not necessary
for the ‘herd’ response by individuals.
Perhaps there is some sort of ‘first
responder’ effect at play, which provokes
the herd. It might be interesting to
compare CO2 reactions using
physiological approaches to determine
whether a range of sensitivity exists
across individuals that might therefore
Current Biology
Dispatchesbecome first responders. It is important to
keep in mind that different states, such as
flight, alter neuromodulator levels in the
brain that change the gain of sensory
circuits such as motion detecting neurons
[17,18] and may even confer CO2
sensitivity to an as yet unidentified novel
CO2 detector [12]. Future work could
investigate how CO2-anosmic flies know
the direction to walk away. It would be
exciting to find that flies touch specific
legs of sedentary flies to prod their
locomotor direction depending upon the
location of the odor source. Finally, it is
possible and probable that this type of
group effect extends to other sensory
modalities as motion-elicited walking
responses of flies weaken as population
density decreases ([19] and unpublished
data). This study sets the stage for using
the fly to further investigate the
molecules, neurons, and circuits that
permit social context tomodulate sensory
behaviors.
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Group Behavior: Social Context Modulates Behavioral Responses to Sensory Stimuli

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