Motor output reflects the linear superposition of visual and olfactory inputs in Drosophila
Bioengineering, California Institute of Technology, Pasadena, CA 91125, USA
* Author for correspondence (e-mail: frye{at}caltech.edu)
Accepted 25 September 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: vision, olfaction, fruit fly, Drosophila, sensorimotor integration, sensory fusion, optomotor, multimodal integration
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The necessary interaction between visual and olfactory feedback might occur
at various levels within the nervous system. For example, integration of
multiple sensory modalities within the mushroom bodies is critical in
context-dependent learning during flight in Drosophila
(deBelle and Heisenberg, 1994).
Other higher order regions within the protocerebrum, such as the lateral horn,
also receive visual and olfactory input from primary sensory regions.
Alternatively, feedback signals may be integrated within specialized
descending networks that supply the flight motor within the thoracic ganglia.
Sensory fusion may arise within individual multimodal descending neurons or
may be distributed among parallel unimodal pathways. Notwithstanding the
anatomical locus of sensory fusion, understanding how vision and olfaction
interact to coordinate motor reflexes in Drosophila will accelerate
efforts to link molecular mechanisms to the systems-level neural processes
responsible for complex behaviors in flies and other animals.
In the present study, we investigated the interaction between olfactory and visual stimuli on the motor control of wing kinematics during flight. Our results show that flies exhibit robust and stereotyped bilateral increases in wingbeat amplitude and frequency when presented with a frontal stream of vinegar vapor. Patterns of lateral visual expansion elicit rapid, reflexive modulations of wing kinematics that direct flies away from an apparent collision. When presented with both sensory cues simultaneously, motor responses show linear superposition. We propose a model for how visual and olfactory feedback is structurally integrated within the musculoskeletal system to functionally bias Drosophila flight trajectories towards odor in free flight.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We tested flies' motor responses to visual and olfactory stimuli during
intact tethered flight within a tethered flight simulator. A detailed
description of this apparatus is available elsewhere
(Lehmann and Dickinson, 1997),
and only a brief account is given here. Flies were suspended between an
optical sensor and an infrared light-emitting diode
(Fig. 1A). The beating wings
cast a shadow onto the sensor. Associated electronic components track the
motion of both wings and measure the amplitude and total frequency of each
wing stroke. While tethered in place, flies attempt to steer by modulating the
difference between the left and right wingbeat amplitude (
WBA). To
create closed-loop conditions, the time varying
WBA signal is coupled
to the angular velocity of a visual pattern created by a cylindrical array of
green LEDs (Fig. 1A).
|
We allowed flies to control the velocity of an expanding flow field
centered laterally. Any change in WBA resulted in a vertically striped
pattern moving horizontally across the front and rear visual fields,
generating opposing poles of expansion and contraction
(Fig. 1C). The direction of
motion was inverted with respect to the
WBA signal (hence, a turn
directed away from the pole of expansion resulted in reduced expansion
velocity). Under these conditions, flies show a strong tendency to minimize
the velocity of the expansion/contraction. Periodically, we simulated a
collision stimulus by adding an impulsive bias to the closed-loop feedback
signal such that if the fly did not respond at all, the visual pattern would
expand from the right at constant velocity for the duration of the bias. This
stimulus regime generates robust and repeatable collision avoidance reflexes
composed of rapid changes in
WBA stroke amplitude.
To test the effects of steady-state odor cues on visually mediated
collision avoidance reflexes, we modified the flight arena to deliver a stream
of saturated vapor onto the fly's antennae
(Fig. 1B). A mass flow
controller (model 840; Sierra Instruments, Monterey, CA, USA) delivered a
constant velocity stream of air controlled by a solenoid valve to two 30-ml
vials containing either distilled water or a 15% solution of apple cider
vinegar. Dilute vinegar promptly attracts freely mobile Drosophila
but it does not necessarily evoke a generalized olfactory response. Saturated
water and vinegar vapor were delivered through separate tubes into a pair of
16-gauge hypodermic needles that were in turn sealed into the distal tip
section of a clear pipette tip. Thus, the tip of the pipette (4 mm long and
<1 mm3 in volume) served as a common pore through which the
parallel distribution system expelled saturated vapor. The pipette tip was
oriented along its long axis with respect to the fly's retina to minimize its
apparent size (less than 5°). The apparatus delivered a constant stream of
saturated vapor through the pipette tip, and the solenoid valve periodically
switched between the odor stimulus (vinegar) and an odor-free stimulus to
control for anemotactic cues. The delivery tubes were pre-loaded with
saturated vapor before the experiment to minimize the delay from the solenoid
switch to the delivery of vapor on the antenna. Restricting odor to separate
pathways until the final few cubic millimeters of the delivery system also
minimized stimulus delay and ensured a rapid onset of odor cues. Vapor was
delivered to the antennae at 280 mm s1, matching the average
airspeed of animals in free flight
(Tammero and Dickinson,
2002a). A brass tube placed behind the fly provided gentle suction
to remove residual odor stimuli. The tube was placed in the fly's visual blind
spot and the suction was not strong enough to affect wing kinematics. We
performed several control experiments to ensure that the delivery system did
not introduce large mechanical artifacts or side bias. There was no detectable
WBA or wingbeat frequency (WBF) response to water/water controls, and
switching the position of the vinegar and water vials produced identical
results (data not shown).
For decades, researchers have used tractable open-loop steady-state approximations of naturally dynamic sensory stimuli to study multisensory and sensorimotor integration. Such linear analyses are an integral first step towards a comprehensive understanding of sensorimotor processing by nervous systems. Future work should incorporate more naturalistic olfactory dynamics to examine sensory superposition in non steady-state conditions.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Flies show robust and repeatable motor responses to the presentation of an
attractive odor during tethered flight. The total amplitude of the right and
left wingbeat (the sum of WBA, hereafter referred to as WBA) as well as
wingbeat frequency (WBF) rise monotonically and, on average, reach
steady-state levels within 2.5 s following the onset of odor delivery
(Fig. 2A,B). At the termination
of the 10-s odor stimulus, WBF and
WBA responses decay along a slower
time course, returning to baseline after approximately 10 s. Rapid changes in
visually elicited
WBA subtly alter the time courses of
WBA and
WBF waveforms. There was no detectable WBA or WBF response to water/water
controls (data not shown).
The fine structure of motor responses is highlighted in
Fig. 2C. At the onset of a
stepwise bias in closed-loop feedback, the visual display expands from the
right. In response, flies decrease WBA within 300 ms in an effort to
turn away from the focus of visual expansion. The magnitude of expansion
velocity is rapidly reduced as the fly compensates for the bias and stabilizes
pattern motion. However, the flies are not able to completely overcome the
imposed bias, resulting in non-zero steady-state velocity
(Fig. 2Ci, arrow). At the
termination of the visual bias,
WBA returns to zero within
approximately 300 ms. Thus, the onset and offset of this visual reflex operate
on similar rapid time courses.
By contrast, motor responses to the presentation and termination of odor
pulses follow slow, asymmetric time courses. For visual closed-loop conditions
without visual bias, the onset of odor results in an increase in WBF that
approaches a steady-state level within 2 s
(Fig. 2B). In response to odor,
WBA first decreases then monotonically increases to a steady-state
level (Fig. 2Cii, arrow). We
have repeated these experiments several times. The initial downward transient
is a consistent feature of vinegar-elicited increases in
WBA. This
transient may result from mechanical constraints on power production within
the flight system (Lehmann and Dickinson,
2001
). The mechanical power imparted to the beating wings is
roughly proportional to the cubed product of
WBA and WBF and is limited
by several factors, including maximum wing amplitude and the performance
limits of flight muscle. We suspect that the transient decrease in
WBA
results from a time-lag between increased WBF, which is driven by changes in
small control muscles, and the regulatory pathway that can enhance mechanical
power output of the large power muscles.
In response to repeated stepwise presentation of a bias in image expansion
centered to the right, flies turn away from the focus of expansion by
tonically increasing the amplitude of the right wing and decreasing that of
the left (Fig. 3, top panel,
red lines). During concurrent presentation of odor, these changes in visually
mediated WBA are superimposed upon a bilateral elevation of
WBA
(Fig. 3, top panel, black
lines). Aside from the shift in baseline, neither the time course nor
magnitude of visually elicited steering reflexes (
WBA) are affected by
the presentation of odor (Fig.
3, bottom panel). These results suggest that the visual and
olfactory stimuli elicit independent motor responses. By visual inspection,
motor responses to the two stimuli presented together appear to represent the
sum of responses to stimuli presented in isolation
(Fig. 2B). To examine this
explicitly, we tested for linear superposition, in which the following
relationship must be satisfied:
![]() |
|
|
Visual feedback alters the time course of odor-off responses
The presentation of odor has no effect on either experimentally imposed
reflexive visual responses (Figs
3,
4iii) or closed-loop visual
control (Fig. 4ii). However, at
the termination of the odor stimulus, the time course of WBF and WBA
responses depends upon the visual conditions. This is indicated by a violation
of linear superposition immediately after the odor is switched off
(Fig. 4iii, end of trace). Just
before the odor pulse terminates, the
WBA and WBF responses are nearly
identical in the presence or absence of visual bias
(Fig. 5). However, after the
odor is switched off, these motor responses return to baseline much more
slowly in experimental treatments that include periodic visual bias
(Fig. 5, red lines). This
indicates that visual feedback somehow alters the time course of the odor-off
response.
|
To test whether constant visual feedback was sufficient to alter the time
course of the odor-off response, we compared responses to odor pulses during
unbiased visual closed-loop conditions with those presented in a motionless
arena of equal luminance. In the absence of visual feedback, odor pulses
elicit increases in mean WBA and WBF
(Fig. 6). Thus, visual motion
is not required for flies to generate typical motor responses to odor.
However, under visual closed-loop conditions, the odor responses are
substantially altered. Although the rise-time of the odor responses does not
differ significantly between the two treatments, the odor-elicited changes in
wing kinematics take considerably longer to return to baseline in the absence
of visual feedback (
WBA and WBF,
Fig. 6). These results suggest
that visual feedback somehow resets the system's motor responses to odor.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Free-flight odor-search behavior in Drosophila
Decreased WBA coupled with increased
WBA and WBF in response
to an odor cue (Fig. 2) could
result in both a decrease in saccade rate and an increase in forward velocity
in free-flight conditions. However, when encountering an odor source in still
air during free flight, flies do just the opposite, they saccade more
frequently and, as a result, their average flight velocity decreases
(Frye et al., 2003
). There are
several possible explanations for this apparent discrepancy. Here, we
stimulated flies with long, frontally directed odor pulses in order to examine
the influences of steady-state odor cues on dynamic visual reflexes. Of
course, flies do not normally encounter such experimentally tractable
conditions. Rather, odor responses in free flight are likely to represent
successive responses to the rapid onset, duration and offset of odor cues as
the fly repeatedly approaches, flies past and turns back towards the odor
plume. Therefore, an odor-dependent increase in free flight saccade rate may
be consistent with the elevated frequency of attempted turns observed between
odor pulses in tethered animals (Fig.
2). Flight velocity slows during a free flight saccade
(Fry et al., 2003
;
Tammero and Dickinson, 2002b
);
therefore, average flight velocity is reduced whenever an animal executes
frequent saccades, such as when approaching an odor source. Whether the
odor-dependent increases in WBA and WBF during tethered flight result in
increased forward thrust corresponding to increased free flight velocity
remains to be tested directly.
Underlying neural pathways
A striking feature of the flight control architecture in flies is vast
sensory-to-motor convergence. Feedback from tens of thousands of peripheral
sensory and central brain neurons is collected, integrated and ultimately
filtered through the activity of no more than 17 pairs of muscles that control
the steering motions of the wings. The flight control system is therefore
compacted into relatively few neurons, making flies particularly useful for
studying the neurobiology of complex behavior
(Frye and Dickinson, 2001).
Drosophila melanogaster, in particular, has emerged as a key model
system to investigate molecular-genetic, developmental and physiological
determinants of olfactory discrimination
(Stensmyr et al., 2003
;
Vosshall, 2000
), visual motion
detection (Barth et al., 1997
;
Gibbs et al., 2001
;
Juusola and Hardie, 2001
;
Wolf and Heisenberg, 1990
), as
well as associative learning and memory formation
(Connolly et al., 1996
;
deBelle and Heisenberg, 1994
;
Guo and Götz, 1997
;
Pascual and Preat, 2001
).
Recent advances in targeted genetic manipulations such as the pGAL4
enhancer-trap system (Brand and Perrimon,
1993
) have catalyzed the identification of anatomical sites of
multimodal integration (Ito et al.,
1998
), functional roles of central brain structures, and
sensorimotor synapses and peripheral sensory pathways involved in gross
locomotor performance (Kitamoto,
2001
; Strauss,
2002
).
Unfortunately, we are as yet unable to interpret many of these advances
within the framework of the systems-level neural mechanisms of multimodal
integration simply because many sensorimotor interactions in flies have not
been quantitatively characterized at the behavioral level. Those that have
been in Drosophila share a common theme flight behaviors are
orchestrated by parallel sensorimotor processes. For example, the descending
giant fiber initiates a flight escape response to visual stimuli
(Tannouye and Wyman, 1980;
Trimarchi and Schneiderman,
1995b
). A similar behavioral response to noxious olfactory stimuli
is mediated by a parallel, as yet unidentified, descending pathway
(Trimarchi and Schneiderman,
1995a
). During flight, patterns of visual expansion presented
laterally produce robust collision-avoidance steering maneuvers, whereas
expansion centered frontally evokes a landing reflex
(Tammero and Dickinson,
2002a
). The spatial and temporal tuning properties of these two
visual reflexes suggest that they are mediated by separate visuomotor
pathways. Additionally, temporal separation of mechanosensory and visually
mediated equilibrium reflexes enable the fly to detect and counteract
rotational disturbances over a wide range of angular velocities during flight
(Sherman and Dickinson,
2003
).
Neuromuscular mechanisms for visuo-olfactory sensorimotor
interactions in Drosophila
The linear superposition of visual and olfactory motor responses
(Fig. 4) may reflect a
confluence of sensory reflexes projecting along separate but parallel
sensorimotor pathways. Alternatively, sensory input may be fused within
individual neurons that preserve the linear independence of multimodal input.
In either case, specialized descending neurons (DNs) that carry input from the
brain to the thoracic flight motor neuropile undoubtedly play a central role
in coordinating visual and olfactory mediated flight behaviors. Tonic DN
activity is thought to organize and tune wingbeat synchronous mechanosensory
reflexes reverberating within the thorax to control flight muscles
(Heide, 1983). Aside from the
giant fiber system, physiological properties of premotor DNs in fruit flies
are completely unknown. However, in larger blowflies, a class of unidentified
premotor DNs shows receptive field specificity for patterns of visual
expansion centered frontally and might coordinate landing responses
(Borst, 1991
). In addition,
anatomically identified DNs in Sarcophaga show specificity for motion
within small patches of the visual space
(Gronenberg and Strausfeld,
1992
) and are thought to control visuomotor reflexes. Although
there is no evidence to date of parallel olfactory encoding in these neurons,
some do show multimodal processing. For example, spiking responses to visual
motion are gated by mechanosensory feedback generated by wind on the antennae
(Gronenberg and Strausfeld,
1990
). Comparative studies of analogues in other insects serve as
models to motivate future work in flies. Descending cells with inputs residing
within the deutocerebrum of gypsy moths (Lymantria dispar) show
amplified responses to visual motion that are gated by olfactory stimuli
(Olberg and Willis, 1990
). To
our knowledge, this is the only reported example of an identified descending
neuron that is selective for visual and olfactory cues. However, cells that
integrate visual and mechanosensory information in other insects are not
uncommon (Baader et al., 1992
;
Gronenberg et al., 1995
;
Olberg, 1981
;
Rowell and Reichert, 1986
).
Examining the physiological properties of as yet unidentified DNs in
Drosophila will help define physiological mechanisms of sensorimotor
superposition.
However, based on the functional organization of the musculoskeletal
system, we propose that visual and olfactory feedback is carried by separate
populations of DNs that project to distinct sets of wing control muscles
(Fig. 7). Flight muscles can be
roughly categorized into two groups (so-called direct and indirect) that
either insert directly at the wing base or move the wings indirectly by
deforming the thorax (Dickinson and Tu,
1997). The large powerful indirect flight muscles (IFMs) are not
controlled on a contraction-by-contraction basis. Rather, they are stretch
activated and create a myogenic rhythm through the mechanical resonance of
antagonistic pairs. Another set of smaller indirect control muscles are
thought to stiffen the thorax and vary its resonant properties, thus altering
the mechanical action of the IFMs to effect changes in wingbeat amplitude and
frequency. Whereas the indirect muscle groups do not coordinate cycle-by-cycle
changes in wing kinematics, tonic variation in neural drive is correlated with
gross changes in
WBA and WBF
(Heide, 1983
). We suggest that
the relatively slow odor-mediated changes in bilateral
WBA and WBF
(Fig. 2) are coordinated by
tonic descending input targeted to select indirect muscles.
|
Modulation of power muscle activity via descending pathways is
characteristically slow, operating on a time scale spanning hundreds of
individual wing strokes (Dickinson et al.,
1998), however Drosophila can turn by 90° within 40
ms, or about eight individual wing strokes
(Fry and Dickinson, 2003
).
Rapid changes in wing motion are coordinated by a specialized group of
synchronous (i.e. twitch-type) flight muscles that insert directly onto the
wing hinge. The wings beat so fast that steering muscles have only two neural
control parameters whether or not they fire at all within a cycle and
at what phase they do. For example, phase shifts in the timing of the first
basalare muscle, b1, are correlated with an elevation of the stroke plane,
whereas a spike in b2 causes an immediate increase in ipsilateral wingbeat
amplitude (Heide and Götz,
1996
; Lehmann and Götz,
1996
). The rapid changes in
WBA in response to lateral
expansion (Fig. 2) are most
likely coordinated by descending input that drives direct control muscles such
as b1 and b2. By contrast, the time course of odor responses suggests that
this pathway activates indirect control muscles, as well as the IFMs, to cause
slower changes in wing motion. This neuromuscular segregation of visual and
olfactory feedback is consistent with the near perfect linearity of these
systems at the level of behavioral responses. Functionally, such superposition
might bias an animal's body orientation, and as a consequence its flight
trajectory, towards visual features associated with attractive odors.
Whereas olfactory and visual responses are linearly superimposed for the onset and duration of odor cues, odor-mediated changes in wingbeat frequency and amplitude outlast the duration of the odor stimulus in the absence of visual feedback (Fig. 6). This is intriguing because it suggests that visual feedback somehow reconfigures or `resets' motor responses to odor. This phenomenon could also arise from visual and olfactory feedback targeting different groups of flight muscle motoneurons. For example, rapid, phasic stimulation of muscle b2 in response to visual motion could interfere with the effects of olfactory-elicited tonic stimulation of indirect tension or power muscles. The combined influence of the two motor patterns could return wingbeat amplitude to baseline levels. Thus, as an animal navigates a spatially varying odor plume during free flight, visual feedback may functionally enhance olfactory acuity by shutting down or resetting odor-mediated motor responses. Taken together, the results presented here reveal specific sensorimotor interactions that lay the groundwork for future electrophysiological and molecular-genetic analyses of sensory fusion for complex behavior in flies and other animals.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Baader, A., Schafer, M. and Rowell, C. H. F. (1992). The perception of the visual flow field by flying locusts a behavioral and neuronal analysis. J. Exp. Biol. 165,137 -160.
Barth, M., Hirsch, H. V., Meinertzhagen, I. A. and Heisenberg,
M. (1997). Experience-dependent developmental plasticity in
the optic lobe of Drosophila melanogaster. J.
Neurosci. 17,1493
-1504.
Borst, A. (1991). Fly visual interneurons responsive to image expansion. Zool. Jb. Physiol. 95,305 -313.
Brand, A. and Perrimon, N. (1993). Targeted
gene expression as a means of altering cell fates and generating dominant
phenotypes. Development
118,401
-415.
Connolly, J. B., Roberts, I. J. H., Armstrong, K., Kaiser, K.,
Forte, M., Tully, T. and O'Kane, C. J. (1996).
Associative learning disrupted by impaired Gs signaling in Drosophila
mushroom bodies. Science
274,2104
-2107.
deBelle, J. S. and Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263,692 -695.[Medline]
Dickinson, M., Lehman, F. and Chan, W. (1998). The control of mechanical power in insect flight. Am. Zool. 38,718 -728.
Dickinson, M. H. and Tu, M. S. (1997). The function of Dipteran flight muscle. Comp. Biochem. Physiol. A 116,223 -238.[CrossRef]
Fry, S. and Dickinson, M. (2003). The
aerodynamics of free-flight maneuvers in Drosophila.Science 300,495
-498.
Fry, S., Sayaman, R. and Dickinson, M. (2003).
The aerodynamics of free-flight maneuvers in Drosophila.Science 300,495
-498.
Frye, M. A. and Dickinson, M. H. (2001). Fly flight: a model for the neural control of complex behavior. Neuron 32,385 -388.[CrossRef][Medline]
Frye, M. A., Tarsitano, M. and Dickinson, M. H.
(2003). Odor localization requires visual feedback during free
flight in Drosophila melanogaster. J. Exp. Biol.
206,843
-855.
Gibbs, S. M., Becker, A., Hardy, R. W. and Truman, J. W.
(2001). Soluble guanylate cyclase is required during development
for visual system function in Drosophila. J. Neurosci.
21,7705
-7714.
Gronenberg, W., Milde, J. J. and Strausfeld, N. J. (1995). Oculomotor control in calliphorid flies organization of descending neurons to neck motor-neurons responding to visual-stimuli. J. Comp. Neurol. 361,267 -284.[Medline]
Gronenberg, W. and Strausfeld, N. J. (1990). Descending neurons supplying the neck and flight motor of Diptera physiological and anatomical characteristics. J. Comp. Neurol. 302,973 -991.[Medline]
Gronenberg, W. and Strausfeld, N. J. (1992). Premotor descending neurons responding selectively to local visual-stimuli in flies. J. Comp. Neurol. 316,87 -103.[Medline]
Guo, A. and Götz, K. G. (1997). Association of visual objects and olfactory cues in Drosophila.Learn. Mem. 4,192 -204.[Abstract]
Heide, G. (1983). Neural mechanisms of flight control in Diptera. In Insect Flight II, vol. Biona Report 2 (ed. W. Nachtigall), pp. 35-52. Stuttgart: G. Fischer.
Heide, G. and Götz, K. G. (1996).
Optomotor control of course and altitude in Drosophila melanogaster
is correlated with distinct activities of at least three pairs of flight
steering muscles. J. Exp. Biol.
199,1711
-1726.
Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D.
and Strausfeld, N. J. (1998). The organization of
extrinsic neurons and their implications in the functional roles of the
mushroom bodies in Drosophila melanogaster Meigen. Learn.
Mem. 5,52
-77.
Juusola, M. and Hardie, R. C. (2001). Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25 degrees C. J. Gen. Physiol. 117, 3-25.[Medline]
Kitamoto, T. (2001). Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47,81 -92.[CrossRef][Medline]
Lehmann, F. O. and Dickinson, M. H. (1997). The
changes in power requirements and muscle efficiency during elevated force
production in the fruit fly Drosophila melanogaster. J. Exp.
Biol. 200,1133
-1143.
Lehmann, F. O. and Dickinson, M. H. (2001). The
production of elevated flight force compromises manoeuvrability in the fruit
fly Drosophila melanogaster. J. Exp. Biol.
204,627
-635.
Lehmann, F. O. and Götz, K. G. (1996). Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster. J. Comp. Physiol. A 179,311 -322.[Medline]
Olberg, R. M. (1981). Parallel encoding of direction of wind, head, abdomen, and visual-pattern movement by single interneurons in the dragonfly. J. Comp. Physiol. 142, 27-41.
Olberg, R. M. and Willis, M. A. (1990). Pheromone-modulated optomotor response in male gypsy moths, Lymantria dispar L Directionally selective visual interneurons in the ventral nerve cord. J. Comp. Physiol. A 167,707 -714.
Pascual, A. and Preat, T. (2001). Localization
of long-term memory within the Drosophila mushroom body.
Science 294,1115
-1117.
Rowell, C. H. and Reichert, H. (1986). Three descending interneurons reporting deviation from course in the locust. II. Physiology. J. Comp. Physiol. A 158,775 -794.[Medline]
Sherman, A. and Dickinson, M. H. (2003). A
comparison of visual and haltere-mediated equilibrium reflexes in the fruit
fly Drosophila melanogaster. J. Exp. Biol.
206,295
-302.
Stensmyr, M., Giordano, E., Balloi, A., Angioy, A.-M. and
Hansson, B. (2003). Novel natural ligands for Drosophila
olfactory receptor neurons. J. Exp. Biol.
206,715
-724.
Strauss, R. (2002). The central complex and the genetic dissection of locomotor behavior. Curr. Opin. Neurobiol. 12,633 -638.[CrossRef][Medline]
Tammero, L. F. and Dickinson, M. H. (2002a).
Collision-avoidance and landing responses are mediated by separate pathways in
the fruit fly, Drosophila melanogaster. J. Exp. Biol.
205,2785
-2798.
Tammero, L. F. and Dickinson, M. H. (2002b).
The influence of visual landscape on the free flight behavior of the fruit fly
Drosophila melanogaster. J. Exp. Biol.
205,327
-343.
Tammero, L. F., Frye, M. A. and Dickinson, M. H.
(2004). Spatial organization of visuomotor reflexes in
Drosophila. J. Exp. Biol.
207,113
-122.
Tannouye, M. A. and Wyman, R. J. (1980). Motor
outputs of giant nerve fiber in Drosophila. J.
Neurophysiol. 44,405
-421.
Trimarchi, J. R. and Schneiderman, A. M. (1995a). Different neural pathways coordinate Drosophila flight initiations evoked by visual and olfactory stimuli. J. Exp. Biol. 198,1099 -1104.[Medline]
Trimarchi, J. R. and Schneiderman, A. M. (1995b). Initiation of flight in the unrestrained fly, Drosophila melanogaster. J. Zool. 235,211 -222.
Vosshall, L. B. (2000). Olfaction in Drosophila. Curr. Opin. Neurobiol. 10,498 -503.[CrossRef][Medline]
Wolf, R. and Heisenberg, M. (1990). Visual control of straight flight in Drosophila melanogaster. J. Comp. Physiol. A 167,269 -283.[Medline]