NEUROETHOLOGY
Food wanting is mediated by transient activation of
dopaminergic signaling in the honey bee brain
Jingnan Huang^1 †, Zhaonan Zhang^1 †‡, Wangjiang Feng^1 †, Yuanhong Zhao^1 †, Anna Aldanondo^2 ,
Maria Gabriela de Brito Sanchez^2 , Marco Paoli^2 , Angele Rolland^2 , Zhiguo Li^1 , Hongyi Nie^1 , Yan Lin^1 ,
Shaowu Zhang^3 , Martin Giurfa1,2,4§, Songkun Su^1 §
The biological bases of wanting have been characterized in mammals, but whether an equivalent
wanting system exists in insects remains unknown. In this study, we focused on honey bees, which
perform intensive foraging activities to satisfy colony needs, and sought to determine whether
foragers leave the hive driven by specific expectations about reward and whether they recollect
these expectations during their waggle dances. We monitored foraging and dance behavior and
simultaneously quantified and interfered with biogenic amine signaling in the bee brain. We show
that a dopamine-dependent wanting system is activated transiently in the bee brain by increased
appetite and individual recollection of profitable food sources, both en route to the goal and during
waggle dances. Our results show that insects share with mammals common neural mechanisms for
encoding wanting of stimuli with positive hedonic value.
T
he study of how brains encode pleasure
( 1 , 2 ) has uncovered the neural and
molecular underpinnings of hedonic
(i.e., pleasant) experiences such as
reward. Psychological components in
the processing of appetitive rewards have
been identified ( 3 ) and traced to dissociable
circuits in the mammalian brain ( 1 ): (i)“liking,”
which refers to the actual pleasurable impact
of reward consumption; (ii)“wanting,”which
refers to the motivation to reach the reward;
and (iii)“learning,”which includes the im-
plicit and explicit information about reward
acquired through individual experience ( 4 ).
In mammals, the process of wanting is me-
diated by neural systems that include meso-
limbic dopamine ( 1 , 5 ).
Despite the fact that invertebrates exhibit
sophisticated reward-seeking behaviors ( 6 ),
the existence of an equivalent wanting system
driving food search remains unknown. Honey
beesareanattractiveorganismforthestudy
of this topic owing to their intensive foraging
activities, their developed social organiza-
tion, and the presence of a symbolic code for
information transfer about appetitive rewards
( 7 )knownasthewaggledance,whichconveys
information about direction and distance of
profitable food sources ( 8 ). The existence of
this code allows us to explore whether, besides
communicating vectorial information point-
ing toward a food source, dancers transiently
recollect the hedonic properties of the ex-
ploited food source. Does a wanting system
drive foragers to profitable food sources and
do waggle dances reactivate this system through
the reminiscence of the reported food source?
To answer these questions, we monitored
foraging and dance behavior of identified
foragers and simultaneously quantified and
interfered with biogenic amine signaling in
the bee brain during key phases of foraging
and communication cycles. We demonstrate
that dopamine levels increase in the brain of
active dancing foragers both during dance
initiation and upon departure toward an at-
tractive food source. Individual hunger also
elevates dopamine levels in the brain of
foragers, thereby enhancing the hedonic value
of sucrose solution and improving appetitive
olfactory learning and memory retrieval. We
thus provide evidence of the existence of a
dopamine-based wanting system in the bee
brain that is triggered by both individual
hunger and personal recollection of the hedonic
value of food sources in the context of the
waggle dance.
We first trained honey bees (Apis mellifera)
from an observation hive to collect sucrose
solution from an artificial feeder. Trained,
tagged bees flew regularly between the hive
and the feeder for a period of 3 days. On day
three, bees consistently reporting the pres-
ence of the feeder via regular waggle dances
were identified. On day four, these bees were
captured in different contexts and situa-
tions. At the feeder, tagged dancers were
captured either upon arrival and before they
started feeding or ~1 min after landing and
starting feeding on the available sucrose solu-
tion. Within the hive, dancers were capturedeither immediately after dance initiation, upon
dance ending (typically 50 to 60 s after dance
start), or when departing for the food source
(typically 10 to 20 s after dance end). We also
collected“cessation”dancers, that is, bees that
danced when the feeder was available but
stopped dancing after the feeder was kept em-
pty for 30 min.
Captured bees were immediately frozen in
liquid nitrogen. High-performance liquid chro-
matography was performed on individual
brains to quantify biogenic amine levels (nano-
grams per brain). Reliable measurements
across all experimental conditions were ob-
tained for dopamine (DA) and serotonin [5-
hydroxytryptamine (5-HT)]. A highly significant
interaction was found between the factors
“biogenic amine”and“behavioral condition”
(Fig. 1A) (F4,130= 15.53,P< 0.0001). Whereas
serotonin did not change with the phase of the
foraging cycle or dance, significantly higher
levels of dopamine were observed upon arrival
at the food source before the bee started feed-
ing and during waggle dance initiation (Tukey
tests,P< 0.001). Although dopamine levels
decreased at the end of dancing, foragers
arrived at the feeder with increased levels of
this amine. This increase was present upon
departure from the hive, as shown by dopamine
levels of foragers flying regularly between the
hive and the feeder over the course of 3 days
and captured on day four at the hive entrance
after dance end and when preparing to leave
the hive (Fig. 1B,“hive departure”). Equivalent
levels of dopamine were found in these bees
upon landing at the feeder (Fig. 1B,“feeder
arrival”). Serotonin levels remained lower in
both groups of bees. As a result, the inter-
action between the factors“biogenic amine”
and“behavioral condition”was not significant
(F1,90= 0.12,P= 0.73). A significant variation
was found for“biogenic amine”(F1,90= 261.32,
P< 0.0001) but not for“behavioral condition”
(F1,90= 0.49,P=0.49).Overall,theseresults
show that brain levels of dopamine increase
when foragers start dancing in the hive to
convey information about profitable food sources
but then transiently decrease toward the end
of the dance. Departure toward the reported
food source is again accompanied by an in-
crease of dopamine brain levels, whereas food
ingestion at the goal decreases levels until the
next dancing event. These fast, transient acti-
vations of the dopaminergic system could be
indicative of an enhanced appetitive motivation
upon food finding and recollection of food value
through initiation of waggle dances.
The increased levels of dopamine in the
brain of foragers may have been influenced
by their 3-day cumulative flight experience
prior to biogenic amine quantification. We
therefore wondered whether the first expe-
rience with a profitable food source already
enhanced dopamine levels. Marked bees were508 29 APRIL 2022•VOL 376 ISSUE 6592 science.orgSCIENCE
(^1) College of Animal Sciences (College of Bee Science), Fujian
Agriculture and Forestry University, Fuzhou 350002, China.
(^2) Centre de Recherches sur la Cognition Animale, Centre de
Biologie Intégrative (CBI), University of Toulouse, CNRS,
UPS, 31062 Toulouse cedex 9, France.^3 Australian Research
Council Centre of Excellence in Vision Science, Research School
of Biology, College of Medicine, Biology and Environment, The
Australian National University, Canberra, ACT 2601, Australia.
(^4) Institut Universitaire de France (IUF), Paris, France.
*Corresponding author. Email: [email protected] (M.G.);
[email protected] (S.S.)
†These authors contributed equally to this work.
‡Present address: Laboratoire Évolution et Diversité Biologique
(EDB), UMR 5174, University of Toulouse, CNRS, UPS, 31062
Toulouse cedex 9, France.
§These authors contributed equally to this work.
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