Björn Brembs

[[![ResearchBlogging.org](https://www.researchblogging.org/public/citation_icons/rb2_mid.png){decoding="async"
style="border: 0;"}](https://www.researchblogging.org)]{style="float: left; padding: 5px;"}Until
1986, it was thought that so-called [optomotor
responses](https://en.wikipedia.org/wiki/Optomotor_response){target="_blank"},
i.e., the tendency of all animals and humans to follow moving visual
stimuli with their eyes or their bodies, were a prerequisite for gaze or
trajectory stabilization: whenever the scenery in your gaze moves, you
adjust gaze or body orientation to compensate for the shift. The main
concept was that these behaviors were responses to external stimuli,
e.g., shift to the left elicits a counter movement to compensate for the
shift. Without such simple input-output processes, it was thought, it
would be impossible to maintain course or gaze. However, in 1986, [Wolf
and
Heisenberg](https://www.nature.com/nature/journal/v323/n6084/abs/323154a0.html){target="_blank"}
reported on experiments in *Drosophila* fruit flies with drastically
reduced optic lobes, the primary visual processing centers of insects.
These flies with the double mutation *rol* (reduced optic lobes) *sol*
(small optic lobes, see figure 1) were incapable of performing optomotor
responses to rotating stimuli, but nevertheless fixated a stripe in
their frontal visual field if they were allowed to control the position
of that stripe with turning maneuvers that were simultaneously recorded.
In other words, the flies could not see in which direction the stripe
was moving, but nevertheless managed to move the stripe in a way that
fixated it preferentially in front of the flies. Further experiments
showed that the only way the flies could possibly accomplish this feat
is by 'trying out' which turning maneuver led to the stripe staying in
the frontal part of their visual field -- an operant (or, as one would
also say today, goal-directed) behavior. For more details on this and
two related classic experiments from the Heisenberg lab see "[The
Importance of Being
Active](https://bjoern.brembs.net/downloads/?download=16 "The importance of being active")".

::: {#attachment_133 .wp-caption .alignright style="width: 160px"}
[![rolsol](https://bjoern.brembs.net/wp/wp-content/uploads/2013/05/rolsol-150x150.jpg){.size-thumbnail
.wp-image-133 decoding="async" aria-describedby="caption-attachment-133"
width="150"
height="150"}](https://bjoern.brembs.net/wp/wp-content/uploads/2013/05/rolsol.jpg)

Fig. 1: Side by side comparison of the brains of wild type (WT) and rol
sol double mutant flies (click to enlarge).
:::

Now [Bahl *et
al.*](https://www.nature.com/neuro/journal/v16/n6/full/nn.3386.html){target="_blank"}
in the lab of [Alexander
Borst](https://www.neuro.mpg.de/borst){target="_blank"}
[(](https://www.neuro.mpg.de/borst){target="_blank"}a [graduate student
of
Heisenberg](https://neurotree.org/neurotree/tree.php?pid=8061){target="_blank"}'s
from 1982-84) have not only replicated this seminal study, they have
done so in an impressively sophisticated and meticulous manner, avoiding
many if not all of the methodical problems of the original experiments
and adding exciting new findings to our body of knowledge along the way.
Their fabulous publication constitutes a shining example of the power of
combining today's genetic technology with state-of-the-art behavioral
physiology and computational modeling. Technically, it doesn't get any
better than that in our field today. A major procedural concern with the
1986 Wolf & Heisenberg paper had always been that none of the potential
side-effects of the drastic double mutation *rol sol* were known.
Granted, the optic lobes were vanishingly tiny in these mutants (see
figure 1) and almost any visual capability seemed like a surprise, but
which other processes were affected and in what way was completely
unknown. Rather than almost ablating the entire optic lobes of the
flies, Bahl *et al.'*s genetic manipulations specifically affected only
two sets of interneurons, T4/5, in the flies' visual system which the
[Borst lab had previously
reported](https://dx.doi.org/10.1007/s00359-012-0716-3){target="_blank"}
as abolishing all optomotor responses. Not only was it known that these
highly specific manipulations abolished optomotor responses, it was also
known why this happened: these neurons are a crucial component of the
fly's visual motion detector. Thus, these flies were exclusively
motion-blind and all other faculties were unaltered. Amazingly, despite
this highly specific manipulation, these flies behaved exactly like the
*rol sol* flies: they did not respond to moving visual cues, but when
allowed to control a black stripe with turning maneuvers, they kept the
stripe in their frontal visual field. The authors not only replicated
this aspect of the flies' behavior, they also did so using walking
flies, while the original study had examined flying flies, thus
extending and generalizing the findings of Wolf and Heisenberg.
Moreover, the authors found out, by careful and detailed dissection of
the flies' behavior, that optomotor responses improve fixation by
increasing the tendency of the fly to move the stripe to the front of
its visual field. For more details see the original publication or an
[excellent news-type article by Masson &
Goffard](https://dx.doi.org/10.1038/nn.3411){target="_blank"}. This
news-article also emphasizes, btw, the relevance of fly work for our
general understanding of gaze stabilization even in vertebrate systems.

::: {#attachment_134 .wp-caption .alignleft style="width: 160px"}
[![Fig. 2: "Inverting goggles" experiment. Whenever the tethered fly
attempts a turning maneuver, the fly\'s visual panorama is rotated in
the same direction. In the depicted example, a right turning maneuver
leads to a rotation of the panorama to the right. In this situation, any
attempts of the fly to follow the stripe will lead to a catastrophic
feedback of increasing speed of the stripe and yaw torque of the fly in
the same direction. Nevertheless, flies learn to generate turning
maneuvers in the opposite direction in order to establish a zero net
rotation of the stripe (optomotor balance). Fly drawing courtesy of
Reinhard
Wolf.](https://bjoern.brembs.net/wp/wp-content/uploads/2013/05/inversegoggles-150x150.jpg){.size-thumbnail
.wp-image-134 decoding="async" aria-describedby="caption-attachment-134"
width="150"
height="150"}](https://bjoern.brembs.net/wp/wp-content/uploads/2013/05/inversegoggles.jpg)

Fig. 2: "Inverting goggles" experiment. Whenever the fly attempts a
turning maneuver, the fly's visual panorama is rotated in the same
direction. Fly drawing by R. Wolf.
:::

Very much like Wolf & Heisenberg in 1986, Bahl *et al.* come to the
conclusion that there is, in addition to the well-studied optomotor
system, a less well-studied position system that acts in parallel during
object fixation/course control. Specifically, and this is where they
differ markedly from Wolf & Heisenberg, the authors assume that both
systems operate according to more or less fixed input-output rules,
i.e., "turn left on stimuli moving to the left" or "turn right if the
bar is on the right". However, the single most critical condition in the
experiments by Wolf & Heisenberg was the one where a right turn of the
fly led to a rotation of the visual field to the right, instead of to
the left (the '[inverting
goggles](https://www.grand-illusions.com/acatalog/Reversing_Goggles.html){target="_blank"}'
experiment, see figure 2). The *rol sol* flies showed no difference in
stripe fixation between both conditions, whereas control flies took much
longer to fixate the stripe under 'inverting goggles' conditions. This
decisive experiment showed that "turn right when the stripe is on the
right" (i.e., the conclusion Bahr *et al.* arrive at) cannot explain
fixation in these motion blind flies. Had the *rol sol* flies performed
this function exclusively, they would not have been able to fixate the
stripe. The same then also holds for the flies from Bahr *et al.*: if
their flies also fixate the stripe equally well in the regular as well
as the inverted situation, their entire explanation for their results
falls apart. Regrettably, Bahl *et al.* did not perform this very
crucial, essential experiment, not in their flies, nor in the computer
model they derived from their data. Hopefully, their next publication
will contain these exciting experiments.

**UPDATE**: I have visited Axel Borst's lab yesterday and they are
working on the inverting goggles experiment. For now, the flies have
trouble stopping the stripe from rotating at all, so there may be some
technical problems using walking flies instead of flying flies for this
kind of experiment, or simply the right parameters have not been found,
yet. Either way, as I speculated, they are working on it!

------------------------------------------------------------------------

[Bahl, A., Ammer, G., Schilling, T., & Borst, A. (2013). Object tracking
in motion-blind flies [Nature Neuroscience,
16]{style="font-style: italic;"} (6), 730-738 DOI:
[10.1038/nn.3386](https://dx.doi.org/10.1038/nn.3386){rev="review"}]{.Z3988
title="ctx_ver=Z39.88-2004&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.jtitle=Nature+Neuroscience&rft_id=info%3Adoi%2F10.1038%2Fnn.3386&rfr_id=info%3Asid%2Fresearchblogging.org&rft.atitle=Object+tracking+in+motion-blind+flies&rft.issn=1097-6256&rft.date=2013&rft.volume=16&rft.issue=6&rft.spage=730&rft.epage=738&rft.artnum=http%3A%2F%2Fwww.nature.com%2Fdoifinder%2F10.1038%2Fnn.3386&rft.au=Bahl%2C+A.&rft.au=Ammer%2C+G.&rft.au=Schilling%2C+T.&rft.au=Borst%2C+A.&rfe_dat=bpr3.included=1;bpr3.tags=Biology%2CNeuroscience%2CBehavioral+Biology%2C+Ecology%2C+Evolutionary+Biology%2C+Genetics%2C+Zoology%2C+Behavioral+Biology%2C+Computational+Biology%2C+Genetics+%2C+Zoology%2C+Behavioral+Neuroscience%2C+Computational+Neuroscience"}  
[Wolf, R., & Heisenberg, M. (1986). Visual orientation in motion-blind
flies is an operant behaviour [Nature, 323]{style="font-style: italic;"}
(6084), 154-156 DOI:
[10.1038/323154a0](https://dx.doi.org/10.1038/323154a0){rev="review"}]{.Z3988
title="ctx_ver=Z39.88-2004&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.jtitle=Nature&rft_id=info%3Adoi%2F10.1038%2F323154a0&rfr_id=info%3Asid%2Fresearchblogging.org&rft.atitle=Visual+orientation+in+motion-blind+flies+is+an+operant+behaviour&rft.issn=0028-0836&rft.date=1986&rft.volume=323&rft.issue=6084&rft.spage=154&rft.epage=156&rft.artnum=http%3A%2F%2Fwww.nature.com%2Fdoifinder%2F10.1038%2F323154a0&rft.au=Wolf%2C+R.&rft.au=Heisenberg%2C+M.&rfe_dat=bpr3.included=1;bpr3.tags=Biology%2CNeuroscience%2CBehavioral+Biology%2C+Genetics%2C+Zoology%2C+Behavioral+Neuroscience%2C+neurogenetics"}


Until 1986, it was thought that so-called optomotor responses, i.e., the tendency of all animals and humans to follow moving visual stimuli with their eyes or their bodies, were a prerequisite for gaze or trajectory stabilization: whenever the scenery in your gaze moves, you adjust gaze or body orientation to compensate for the shift.

Messaggi di Rogue Scholar

Dissecting a fly’s course control system