Current Biology
Dispatches
unsupervised methods for parsing
behavior as a whole typically reveal so
many clusters that the path forward is less
clear.) Thus, the use of unsupervised
methods in finding the fast pulse note
represents a standout example of how new
statistical approaches can reveal
biological phenomena hiding in plain sight.
REFERENCES
1. Shorey, H.H. (1962). Nature of the sound
produced by Drosophila melanogaster during
courtship. Science 137, 677–678.
2. von Schilcher, F. (1976). The function of pulse
song and sine song in the courtship of Drosophila
melanogaster. Anim. Behav. 24, 622–625.
3. Clemens, J., Coen, P., Roemschied, F.A.,
Pereira, T.D., Mazumder, D., Aldarondo, D.E.,
Pacheco, D.A., and Murthy, M. (2018).
Discovery of a new song mode in Drosophila
reveals hidden structure in the sensory and
neural drivers of behavior. Curr. Biol. 28, 2400–
2412.
4. Fabre, C.C.G., Hedwig, B., Conduit, G.,
Lawrence, P.A., Goodwin, S.F., and Casal, J.
(2012). Substrate-borne vibratory
Social Behavior: A Neural Circuit for Social Behavior in
Zebrafish
Gonzalo G. de Polavieja and Michael B. Orger
Champalimaud Research, Champalimaud Centre for the Unknown, Avenida Brası́lia s/n, 1400-038 Lisbon, Portugal
Correspondence: gonzalo.polavieja@neuro.fchampalimaud.org (G.G.d.P.), michael.orger@neuro.fchampalimaud.org (M.B.O.)
https://doi.org/10.1016/j.cub.2018.06.065
A new study on the zebrafish has discovered a population of forebrain neurons necessary for social orienting,
providing a foundation for dissecting social brain networks in this powerful vertebrate model.
Navigating the many social signals at, say,
a dinner party requires huge information
processing power. Not understanding if
someone is shy or on edge, or how
interested the other guests are in different
topics of conversation, might quickly lead
to testy exchanges, raised tempers and a
spoiled evening. Many other species
similarly depend on social stimuli to
decide which action to take. A very fast
change of direction of a conspecific, for
example, may indicate the presence of
some danger, while other social signals
can indicate conflicts over resources
and an imminent fight, or mating
R828 Current Biology 28, R826–R845, August 6, 2018 ª 2018 Elsevier Ltd.
communication during courtship in Drosophila
melanogaster. Curr. Biol. 22, 2180–2185.
5. Coen, P., Clemens, J., Weinstein, A.J.,
Pacheco, D.A., Deng, Y., and Murthy, M.
(2014). Dynamic sensory cues shape song
structure in Drosophila. Nature 507, 233–237.
6. Ritchie, M.G., Yate, V.H., and Kyriacou, C.P.
(1994). Genetic variability of the interpulse
interval of courtship song among some
European populations of Drosophila
melanogaster. Heredity 72, 459–464.
7. Ding, Y., Lillvis, J.L., Cande, J., Berman, G.J.,
Arthur, B.J., Xu, M., Dickson, B.J., and Stern,
D.L. (2017). Neural changes underlying rapid
fly song evolution. bioRxiv, https://doi.org/10.
1101/238147.
8. Markow, T.A. (1987). Behavioral and sensory
basis of courtship success in Drosophila
melanogaster. Proc. Natl. Acad. Sci. USA 84,
6200–6204.
9. Ejima, A., and Griffith, L.C. (2008). Courtship
initiation is stimulated by acoustic signals in
Drosophila melanogaster. PLoS One 3, e3246.
10. Fernández, M.P., Chan, Y.B., Yew, J.Y., Billeter,
J.C., Dreisewerd, K., Levine, J.D., and Kravitz,
E.A. (2010). Pheromonal and behavioral cues
trigger male-to-female aggression in
Drosophila. PLoS Biol. 8, e1000541.
opportunities. The specialized nature of
the computations needed to extract
relevant information from social stimuli
raises the question of whether there exist
neuronal substrates dedicated to
processing social cues. A core social
behavior network, consisting of
anatomically and functionally connected
regions implicated in many different social
behaviors, has been described in
mammals [1], and appears to be
conserved across reptiles, birds, and
teleost fish [2]. Shared neuroanatomical
and molecular features across taxa
provide the opportunity to study, in the
11. Trott, A.R., Donelson, N.C., Griffith, L.C., and
Ejima, A. (2012). Song choice is modulated by
female movement in Drosophila males. PLoS
One 7, e46025.
12. Tauber, E. (2002). The effect of male competition
on the courtship song of Drosophila
melanogaster. J. Insect. Behav. 15, 109–120.
13. Demir, E., and Dickson, B.J. (2005). fruitless
splicing specifies male courtship behavior in
Drosophila. Cell 121, 785–794.
14. von Philipsborn, A.C., Liu, T., Yu, J.Y., Masser,
C., Bidaye, S.S., and Dickson, B.J. (2011).
Neuronal control of Drosophila courtship song.
Neuron 69, 509–522.
15. Berman, G.J., Choi, D.M., Bialek, W., and
Shaevitz, J.W. (2014). Mapping the
stereotyped behaviour of freely moving fruit
flies. J. R. Soc. Interface 11, pii: 20140672.
16. Todd, J.G., Kain, J.S., and de Bivort, B.L.
(2017). Systematic exploration of
unsupervised methods for mapping behavior.
Phys. Biol. 14, 015002.
17. Klibaite, U., Berman, G.J., Cande, J., Stern, D.L.,
and Shaevitz, J.W. (2017). An unsupervised
method for quantifying the behavior of paired
animals. Phys. Biol. 14, 015006.
most experimentally tractable systems,
fundamental circuit mechanisms at work
in vertebrate social behavior. In a step
towards this goal reported in this issue of
Current Biology, Stednitz et al. [3] have
identified a genetically defined population
of neurons in the forebrain of zebrafish
that are indispensable for social orienting.
What is the relevance of these new
results? Among teleost species, zebrafish
currently offer a comprehensive array of
advantages for the analysis of neural
circuits. Genetic tools allow the
visualization and spatially and temporally
targeted manipulation of different neuronal
Current Biology

Dispatches

subpopulations [4]. Their small size and

transparency in the larval stage make it
possible to image whole brain activity at
cellular resolution [5,6], and this has even
been achieved in freely swimming animals
[7]. Their social behavior in the lab is rich:
they school and shoal, fight or mate in
simple setups that allow quantitative
measurements [8]. Individuals can actively
observe and learn from the behavior of
others [9]. They can learn to discriminate
pigment patterns [10], and the visual
recognition of conspecifics involves
binding of features such as form and
motion in a specific manner that suggests
dedicated processing of social cues [11].
Aggressive social interactions are used to
establish social hierarchies and
neurogenetic approaches have identified
subnuclei in the habenula involved in the
underlying computations [12].
Nevertheless, relatively little is known
about the form and function of circuits
underlying most of the social behaviors in
zebrafish and the model has yet to be
exploited systematically for a study of
the brain circuits implicated in social
behavior. The application of the zebrafish
model has probably been hindered by
the fact that the most precise tools for
imaging and manipulating neurons are
applicable in the larva, whereas rich social
behaviors are most evident in the adult.
This gap is closing, however. Systematic
analysis of the ontogeny of social
behaviors indicates that they do in fact
emerge very early in development [13,14],
while developments in neuroscience and
imaging methods increasingly allow
experiments in juveniles and adults.
For Stednitz et al. [3] to harness the
power of zebrafish, they needed to
control social stimuli. Social behaviors, by
their very nature, are challenging to study
because the triggering stimulus is another
behaving animal, over which the
experimenter has only limited control.
This problem can be overcome by
employing robotic mimics [15] or video
projections of fish [16]. Such approaches
can be very fruitful, but may not fully
replicate the rapid and rich interactions
offered by a natural conspecific. Stednitz
et al. [3] set out to develop an assay in
which social behaviors could be elicited in
a precisely timed and repeatable manner.
They separated two fish using a window
that could be switched electronically
between an opaque and a transparent
A
Social
orienting
B
Intact
brain
Figure 1. A population of forebrain neurons is indispensable for social orienting in zebrafish.
(A) Adult zebrafish separated by a transparent partition approach each other and show social orienting
behavior. (B) Stednitz et al. [3] ablated a subset of neurons in ventral telencephalon, resulting in a
reduction of approach and social orienting. (Figure credit: Gil Costa.)
form. When the two fish first see each
other, they approach the barrier and view
each other at a characteristic distance
and orientation (Figure 1A). This behavior
lasts only a few minutes, allowing a period
of social investigation to be isolated
from other behaviors. Interestingly, an
important trigger for this orienting
response was the behavior of the other
fish. When one fish was treated with a
drug targeting dopaminergic signaling,
which impaired its orienting response, the
untreated partner fish also failed to orient,
even when the treated fish was
constrained to swim near the barrier.
This rapid and reliable assay gave
Stednitz et al. [3] the starting point needed
to begin probing the underlying neural
substrates, but where should one begin
looking for social brain networks in
zebrafish? One lesion study in goldfish
pointed, albeit indirectly, to the ventral,
but not dorsal, telecencephalon as
necessary for shoaling behavior [17], and
the teleost homologue of the lateral
septum, one component of the social
behavior network, is thought to reside in
this area [2]. Stednitz et al. [3] first
performed a series of manual lesions at
different dorsoventral locations in the
telencephalon. Consistent with the
observations on goldfish shoaling, more
ventral lesions impaired the social
orienting behavior, while more dorsal
lesions had no effect in their assay.
Social
orienting
Forebrain
lesion
Current Biology
While mechanical lesions can help to
distinguish the roles of broadly defined
brain regions, they have limited resolution,
and no specificity in terms of cell types.
Gal4 driver lines allow for more targeted
manipulations of defined neural
populations [4]. Transgenic lines targeting
particular areas can now be identified from
searchable atlases, in which expression
patterns have been registered to a
standard reference brain [18]. From one
such collection, Stednitz et al. [3] found
a line whose expression was specific
to a group of neurons in the ventral
telencephalon. The labeled neurons are
mostly cholinergic and express the same
transcription factor as a population found
in the medial septal nucleus of mice. The
authors used this line to drive expression
of an enzyme that generates a toxic
product when a chemical substrate is
added to the water, allowing the neurons
to be ablated at a controlled time point.
Ablation of these neurons impaired the
fishes’ social orienting behavior
(Figure 1B), whereas the same treatment
applied to other selected forebrain
populations had no observable effect.
Identifying a genetically targetable
population of neurons required for social
orienting behavior is an important
advance, but there is still a lot to
understand about their role in the brain’s
social behavior network. Tracing the
neurons’ projections and identifying

Current Biology 28, R826–R845, August 6, 2018 R829


where their inputs and outputs are located
will be critical to confirming what
anatomical region they belong to, and
how they fit into a broader circuit for
processing social information. Another
key question is what facet of the behavior
the neurons are involved in. Could they,
for example, be responsible for extracting
social cues from visual stimuli, or for
controlling the fishes’ interest in social
interaction? Interestingly, neurons in the
septum of chicks have been shown to
respond to the appearance of
conspecifics only when they move in a
naturalistic way [19], suggesting a role in
visual processing of social cues.
Social attraction is observed already
during the first weeks of life in zebrafish,
at time points where the brain is still
accessible for non-invasive calcium
imaging approaches, and it will be
exciting to discover if the current results
can be extended to these earlier stages
[13,14]. A proposed feature of the social
behavior network is that different social
contexts and behaviors are not
processed by separate substrates, but
are associated with distinct patterns of
activation distributed across all the nodes
in the network [1], and gene expression
analysis in zebrafish has provided support
for this idea [20]. It will therefore be
interesting to know if ablation of these
neurons affects the expression of other
social behaviors such as aggression and
courtship. The work of Stednitz et al. [3]
makes it possible to begin addressing
these questions, and to dissect the neural
circuit mechanisms of social behavior in a
simple vertebrate model.
REFERENCES
1. Newman, S.W. (1999). The medial extended
amygdala in male reproductive behavior.
A node in the mammalian social behavior
network. Ann. N.Y. Acad. Sci. 877, 242–257.
2. O’Connell, L.A., and Hofmann, H.A. (2012).
Evolution of a vertebrate social decision-
making network. Science 336, 1154–1157.
3. Stednitz, S.J., McDermott, E.M., Ncube, D.,
Tallafuss, A., Eisen, J.S., and Washbourne, P.
(2018). Forebrain control of behaviorally-driven
social orienting in zebrafish. Curr. Biol. 28,
2445–2451.
4. Kawakami, K., Asakawa, K., Hibi, M., Itoh, M.,
Muto, A., and Wada, H. (2016). Gal4 driver
transgenic zebrafish. Adv. Gen. 95, 65–87.
5. Ahrens, M.B., Orger, M.B., Robson, D.N., Li,
J.M., and Keller, P.J. (2013). Whole-brain
functional imaging at cellular resolution using
R830 Current Biology 28, R826–R845, August 6, 2018 ª 2018 Elsevier Ltd.
light-sheet microscopy. Nat. Methods 10,
413–420.
6. Portugues, R., Feierstein, C.E., Engert, F., and
Orger, M.B. (2014). Whole-brain activity maps
reveal stereotyped, distributed networks for
visuomotor behavior. Neuron 81, 1328–1343.
7. Kim, D.H., Kim, J., Marques, J.C., Grama, A.,
Hildebrand, D.G.C., Gu, W., Li, J.M., and Robson,
D.N. (2017). Pan-neuronal calcium imaging with
cellular resolution in freely swimming zebra fish.
Nat. Methods 14, 1107–1114.
8. Orger, M.B., and de Polavieja, G.G. (2017).
Zebrafish behavior: opportunities and
challenges. Annu. Rev. Neurosci. 40, 125–147.
9. Abril-de Abreu, R., Cruz, J., and Oliveira, J.F.
(2015). Social eavesdropping in zebrafish:
tuning of attention to social interactions. Sci.
Rep. 5, 11–14.
10. Engeszer, R.E., Ryan, M.J., and Parichy, D.M.
(2014). Learned social preference in zebrafish.
Curr. Biol. 14, 881–884.
11. Neri, P. (2012). Feature binding in zebrafish.
Anim. Behav. 84, 485–493.
12. Chou, M.-Y., Amo, R., Kinoshita, M., Cherng,
B.-W., Shimazaki, H., Agetsuma, M., Shiraki,
T., Aoki, T., Takahoko, M., Yamazaki, M., et al.
(2016). Social conflict resolution regulated by
two dorsal habenular subregions in zebrafish.
Science 352, 87–90.
13. Dreosti, E., Lopes, G., Kamp, A.R., and Wilson,
S.W. (2015). Development of social behavior
in young zebrafish. Front. Neural Circuits 9, 1–9.
Neuroscience: A Mechanism
for Rhythmic Sampling in Vision
Ayelet N. Landau
Departments of Psychology and Cognitive Sciences, The Hebrew University of Jerusalem,
Jerusalem, Israel
Correspondence: ayelet.landau@mail.huji.ac.il
https://doi.org/10.1016/j.cub.2018.05.081
Ongoing perception ebbs and flows rhythmically. Understanding the
source and scope of this phenomenon is an important step in unraveling
the foundations of sensory processing. A new study demonstrates that
local neuronal interactions generate rhythmic brain activity and
correspond to rhythmic performance patterns on a visual-detection task.
Researchers in the fields of psychology
and neuroscience often debate different
taxonomies and definitions for attention
[1]. In physiology, the act-by-act
consequences of attention can readily be
described in the visual cortex and revolve
Current Biology
Dispatches
14. Hinz, R.C., and de Polavieja, G.G. (2017).
Ontogeny of collective behavior reveals a
simple attraction rule. Proc. Natl. Acad. Sci.
USA 114, 2295–2300.
15. Butail, S., Polverino, G., Phamduy, P., Del
Sette, F., and Porfiri, M. (2014). Influence of
robotic shoal size, configuration, and activity
on zebrafish behavior in a free-swimming
environment. Behav. Brain Res. 275, 269–280.
16. Stowers, J.R., Hofbauer, M., Bastien, R.,
Griessner, J., Higgins, P., Farooqui, S., Fischer,
R.M., Nowikovsky, K., Haubensak, W., Couzin,
I.D., et al. (2017). Virtual reality for freely moving
animals. Nat. Methods 14, 995–1002.
17. Shinozuka, K., and Watanabe, S. (2004).
Effects of telencephalic ablation on shoaling
behavior in goldfish. Phys. Behav. 81,
141–148.
18. Marquart, G.D., Tabor, K.M., Brown, M.,
Strykowski, J.L., Varshney, G.K., LaFave,
M.C., Mueller, T., Burgess, S.M., Higashijima,
S., and Burgess, H.A. (2015). A 3D searchable
database of transgenic zebrafish Gal4 and Cre
lines for functional neuroanatomy studies.
Front. Neural Circuits 9, 11.
19. Mayer, U., Rosa-Salva, O., Morbioli, F., and
Vallortigara, G. (2017). The motion of a living
conspecific activates septal and preoptic
areas in naive domestic chicks (Gallus gallus).
Eur. J. Neurosci. 45, 423–432.
20. Teles, M.C., Cardoso, S.D., and Oliveira, R.F.
(2016). Social plasticity relies on different
neuroplasticity mechanisms across the brain
social decision-making network in zebrafish.
Front. Behav. Neurosci. 10, 16.
around two key concepts: competition
and bias [2]. When neurons in the visual
cortex encounter a cluttered scene, the
different stimuli compete for the sensory
neurons’ response. If we were to ‘listen’ to
(measure) a visually responsive neuron, it