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First published online September 19, 2006
Journal of Experimental Biology 209, 3913-3924 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02438
Proprioceptive encoding of head position in the black soldier fly, Hermetia illucens (L.) (Stratiomyidae)
Department of Entomology, Cornell University, Ithaca, NY 14853, USA
Author for correspondence (e-mail:
cg23{at}cornell.edu)
Accepted 11 July 2006
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Summary |
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Key words: mechanoreception, prosternal organ, insect, neck, posture, ill-posed problem
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). In insects, head posture may be encoded by a variety of
proprioceptors that appear to have evolved independently a number of times
among different orders (Peters,
1962), with the most widespread condition being small fields of
mechanoreceptive hairs located on the anterior end of the second lateral
cervical sclerite [e.g. Plecoptera
(Wittig, 1955), Orthoptera
(Goodman, 1959), Mantodea
(Pringle, 1938) and
Hymenoptera (Lindauer and Nedel,
1959)]. In some other groups [e.g. Odonata
(Mittelstaedt, 1950;
Fuldner, 1954-1955), Dermaptera
(Popham, 1960), Coleoptera
(Korschelt, 1924) (C.G.,
unpublished)] hair fields are located in different areas of the cervical
region simply as clusters of one to several dozen hairs grouped together in
the arthrodial membrane. Another condition exists in Diptera, the true flies,
in which the hair plates were first described
(Lowne, 1870) from the blow
fly, Calliphora (=Musca) vomitoria, as a pair of
bilaterally symmetrical, separated groups of hairs (
100 hairs each)
located on cephalad extensions of the presternum, the anteriormost sclerite in
the ventral cervical region. These hair plates have been termed the prosternal
organ (PO) and the morphology described by Lowne is similar for other muscoid
flies (Peters, 1962;
Preuss and Hengstenberg, 1992;
Gilbert and Bauer, 1998). In
more primitive flies, the hair plates are anteriorly fused along the sagittal
midline (Peters, 1962) and in
the most primitive flies in which the PO has been found (family: Anisopodidae)
it is present as a single midline cluster of hairs
(Gilbert and Edgecomb,
1996).
Although the location of such proprioceptive hair fields varies among
insects, they are all assumed to similarly monitor head position to provide
feedback for control of head posture
(Mittelstaedt, 1950;
Lindauer and Nedel, 1959) and
to provide information about the direction of gaze important for visually
guided behaviors (Mittelstaedt,
1957; Poteser et al.,
1998). In flies, sensory feedback about position of the head is
required for proper alignment of visual fields of motion-sensitive neurons
involved in optomotor control of flight
(Kern et al., 2006). Such
feedback is important for maintaining stability of the head, as well as
interpreting visual translation during head saccades. The mechanistic function
of proprioceptive feedback is best studied in the PO of higher Diptera,
principally Calliphora erythrocephala (Calliphoridae) and
Neobellieria (=Sarcophaga) bullata (Sarcophagidae)
(Liske, 1977;
Liske, 1978;
Horn and Lang, 1978;
Preuss and Hengstenberg, 1992;
Gilbert et al., 1995;
Gilbert and Bauer, 1998). After
unilateral shaving of the PO hairs (Preuss
and Hengstenberg, 1992) or section of the prosternal organ nerve
(Gilbert and Bauer, 1998),
flies compensate by rolling the head down to the operated side, as if to
equalize excitation of the hair plates on each side and the compensatory roll
disappears if both sides are operated. Unilaterally waxing down the hairs,
which presumably excites them, has the opposite effect, causing the flies to
roll their heads away from the waxed side, again balancing the excitation on
both sides (Preuss and Hengstenberg,
1992). Additionally, when a single hair plate is shaved, male
N. bullata flies cannot aerially capture female flies to mate, as do
sham operated males, indicating the male tracking behavior, and even sexual
fitness, can be limited by alteration of PO input (C.G. and M. Kim,
unpublished).
Each PO hair is singly innervated by a mechanosensory neuron
(Lowne, 1890-1892;
Richter, 1964) proposed to be
excited by deflection of the hair by the anteriorly placed contact sclerites.
In muscoid flies, when the head is at rest, approximately a dozen hairs on
each PO hair plate are deflected by the contact sclerites
(Preuss and Hengstenberg,
1992). Both Peters (Peters,
1962) and Preuss and Hengstenberg
(Preuss and Hengstenberg,
1992) proposed that differential deflection of hairs on both hair
plates encodes head position around the pitch and roll axes. For example,
pitch down provides bilaterally symmetrical stimulation, whereas roll provides
asymmetrical stimulation, i.e. increasing the number and angle of deflected PO
hairs on one side while reducing deflection of hairs on the other side.
Electrophysiological recordings of the PN during head pitch and roll, as well
as asymmetrical electrical stimulation of the PN, provide physiological
support for these functional hypotheses
(Gilbert et al., 1995).
To better understand the functional evolution of the cervical system
throughout the Diptera, we have examined the quantitative relationships
between head movements about the pitch, yaw and roll axes and the
physiological activity in the PN of the black soldier fly Hermetia
illucens (L.) (family: Stratiomyidae), a more primitive fly with
anteriorly fused hair plates. This fly has a world-wide distribution, chiefly
in warmer climes (Iide and Mileti,
1976; Sheppard et al.,
2002) and a lekking mating system that involves visual tracking
and complex flight behaviors, such as hovering and mid-air grappling
(Tomberlin and Sheppard,
2001). From morphological examinations, we determined that the
orientation of the PO hairs varies across the PO suggesting various
directional sensitivities across the hair plates. Electrical activity in the
PN is primarily tonic in response to changes in head position and the organ
responds to rotation around all three axes. Pitch down (up) results in
increased (decreased) firing of the PN. Yaw toward (away from) the recorded
side increases (decreases) activity in the PN. Roll down to the recorded side
results in increased PN excitation, but roll up does not change PN activity
relative to the resting rate. Furthermore, encoding of head position around
the pitch or roll, but not yaw, axis is affected by the position of the head
around the other two axes. These results are discussed in light of the
evolution of the PO from a single midline structure to a pair of separate hair
plates.
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Materials and methods |
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). Adult flies were fed sugar and water ad libitum.
In some cases, adults laid eggs on the larval medium, which allowed a second
generation of larger flies to be reared in the laboratory. A full rearing
protocol has been described (Sheppard et
al., 2002). Flies varied in size from 40-110 mg (wet mass) and
0.5-2.5 cm (body length), but only flies 
1.5 cm body length were used in
these experiments (Fig.
1A).
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) were counted as mechanoreceptors. To examine possible
effects of body size on number of hairs, the length of a hind femur of each of
the 20 flies was measured under a stereomicroscope fitted with an ocular
micrometer. To obtain an overview of the PO, flies were prepared for scanning
electron microscopy by freeze killing, desiccated for 3 days, mounted on
stubs, then sputtered with gold-palladium to a thickness of 45 nm, viewed
using a Zeiss DSM 960 scanning electron microscope at 3 kV, and photographed
digitally.
Head movements
Five male and three female flies ranging in wet mass from 60-100 mg were
prepared as follows. Flies were chilled on ice, then waxed on the dorsum of
the thorax to a toothpick using dental wax melted with a low-temperature
optical cautery (Acuderm, Fort Lauderdale, FL, USA), and finally positioned
ventral side up under a stereomicroscope. Two flags of paper cardstock were
waxed perpendicular to the surface of the fly's head in the midsagittal plane
(Fig. 1B,C): One short flag (1)
(mean mass of three flags=0.55 mg) was attached dorsally and a second flag (2)
(mean mass of three flags=1.05 mg) was attached anteriorly in the longitudinal
body axis. Flag 2 was twisted medially so as to have two perpendicular
surfaces for creating forced movements around the pitch and yaw axes. The
average wet mass of a fly's head is 5.00±0.34 mg (N=3). Flies
carrying flags appeared to move their heads normally in hovering flight and in
tethered situations. Thus, we assume that the flags did not significantly load
the neck. Moreover, none of the measurements reported here depend upon the
dynamics of head movement, which may be most affected by the added mass and
drag of the flags.
To rotate the fly's head by various amounts around the pitch, yaw and roll axes, puffs of air controlled by a Picospritzer II (General Valve, Fairfield, NJ, USA), using a MacAdios II SE A/D converter (GW Instruments, Cambridge, MA, USA) with Igor Pro 3.1 software on a Power Macintosh 7100/80av computer, were delivered through pulled glass capillary tubes (o.d. 1.0 mm; tip diameter approximately 5 µm) directed at the flags attached to the fly's head. Flies were positioned under a stereomicroscope so that both the head and an LED that was illuminated for the duration of the air puff could be viewed by a CCD color camera (NC-15D, NEC) through the microscope at 10x magnification and recorded on videotape using a modified Sony VCR (A. R. Vetter, Rebersberg, PA, USA). Images were digitized offline using MGI Video Wave 4.0 (Roxio, Santa Clara, CA, USA) and a video to digital converter (Real Networks, Seattle, WA, USA). Each frame of video (at least 4 min per fly) was extracted using Platypus Animator 5.4 (C Point Pty. Ltd., Para Hills, Australia).
A custom program written in Matlab 6.1 (Mathworks, Natick, MA, USA) was used to calculate angular head positions frame by frame from two digitized points on the posteroventral head capsule just to the left and right of the mouth in ventral view (Fig. 1C). Head yaw position could be measured directly as the angular difference between line segments joining the two digitized points in subsequent frames. Head pitch and roll were viewed indirectly and had to be computed by assuming that the head pivoted around the neck on a lever arm that was 0.65 the width of the mouth, as determined empirically from several flies. Change in pitch or roll resulted in translation or foreshortening, respectively, of the line segment between the digitized points. To calibrate the accuracy of the computed pitch and roll head positions, freshly killed flies (N=2) were positioned using the methods described above under the microscope together with a front-surface mirror, such that a direct view of the pitch or roll position, as well as the normal indirect view, was captured. Computed and directly measured positions were then determined for head pitch angles (±32°) and roll angles (±90°). The relationship between computed versus directly measured pitch angles was y=1.27x+0.8 (r2=0.87, N=261), while that between computed and directly measured roll angles was y=1.10x+4.6 (r2=0.97, N=272). Thus, the computed angles were slightly overestimated and all pitch and roll angles reported here have been decremented by these slopes to correct for the overestimate. The mirrors were not used during experiments to allow for greater magnification of the head, and thus increased precision. Digitizing error determined by repeated measurements of the same frame was less than 2.0°.
Physiological recordings of prosternal afferent activity
To gain access to the prosternal nerves (PN), after the air puff apparatus
was set up around the fly, a small patch of membranous cuticle immediately
posterior to the presternum was peeled away. Tracheae and fat body were gently
removed to reveal the paired PNs. Suction electrodes were fashioned from
pulled glass microfilament capillary tubes (o.d. 1.0 mm; tip diameter
approximately 5 µm) placed in a custom microelectrode holder with an
Ag/AgCl pellet and Luer port (E. M. Wright, Guilford, CT, USA) advanced by a
micromanipulator. A ground electrode was formed by painting a line of Pelco
colloidal silver (Ted Pella, Redding, CA, USA) along the side of the capillary
tube to nearly 0.5 mm from the tip and wrapping a few turns of silver wire (75
µm diameter) around the upper shaft of the capillary tube in contact with
the silver paint. Electrodes were filled with insect saline
(Strausfeld et al., 1983) and
a single PN was sucked up into the capillary tube by a 10 ml syringe attached
through tubing to the Luer port of the holder. Electrical activity was
recorded in the left PN in four flies (three males, one female) and in the
right PN in the other four flies (two males, two females). Only recordings
with extracellular spikes of at least 100 µV were used. The signal was
passed through a differential AC amplifier (A-M Systems, Everett, WA, USA) and
recorded via a MacAdios II SE A/D converter (GW Instruments,
Cambridge, MA, USA) on a Power Macintosh 7100/80av computer running Igor Pro
3.1 at a sampling rate of 50 kHz. Raw extracellular recordings were converted
offline into text format and analyzed in Matlab.
Analysis of physiological activity
Since video recordings of head position had a temporal resolution of 30
fps, the voltage of the extracellular recordings, which typically consists of
compounded action potentials, was also integrated over 33 ms bins
(Fig. 2). To allow comparison
across flies, values of integrated spiking activity were normalized for each
fly by dividing by the largest integrated activity value for that fly. A
`resting' activity level for each fly averaged across all frames in which the
fly's head was at rest was then subtracted from all the normalized integrated
activity levels. Thus, data are presented as relative increases or decreases
of PN activity. The PO is assumed to be bilaterally symmetrical and data are
presented as though all activity was recorded on the left side. Head angles
are calculated such that both yaw towards and roll down to the side of the
recorded PN were considered positive and pitch up is positive.
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Temporal analysis
To examine the temporal properties of PN activity, sequences were selected
in which head position around all three rotational axes was different from
rest, but held at a constant (plateau) position for at least eight data points
(264 ms). Concurrent PN activity was plotted over time during the plateau and
examined for phasic properties by linear regression. Head positions preceding
the plateau may have affected any temporal properties of the PN activity, as
hair plates in some insects exhibit phasic firing only when maximally
deflected and excited (Pringle,
1938; Liske,
1989), thus the plateaus were separately analyzed according to the
23 different combinations of increasing or decreasing pitch, yaw
and roll angles that could precede any period of constant head position.
Statistical analyses
All statistical analyses were performed in Matlab 6.1. To test whether data
from all eight flies could be pooled, the basic relationships between pure
pitch, yaw and roll head angles with spiking activity in the PN were compared
using one-way ANCOVA models. After the relationships were determined to be
relatively consistent across flies, the data were pooled, including both males
and females, and the entire range of head angles and PN activities of the
eight flies were analyzed as a whole.
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Encoding head position around each rotational axis
Extracellular recordings of activity in the PN in H. illucens
typically consist of spikes of various amplitude that compound on one another
when the PO is stroked or when the head is moved
(Fig. 2A), which is similar to
afferent activity of cervical hairs in flesh flies
(Gilbert et al., 1995) and
mantids (Liske, 1989). To
verify that data from all eight flies could be pooled, relationships between
pure head pitch, yaw and roll angles and PN activity were compared across
individuals (Fig. 4). The
relationships are significantly different among flies (ANCOVA;
P<0.001), however, multiple comparison tests of the slopes
indicate that the majority of the slopes among flies are not significantly
different from one another. Considering this variation, the relationships
exhibited in the pooled data are consistent with data from individuals. There
are no significant differences between the sexes in any portion of this
analysis.
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Around each axis, rotation in one direction increases PN activity from the resting level, whereas rotation in the opposite direction tends to decrease activity (but see roll below). However, the relationships and the angular range of head rotation vary for each axis (Fig. 4). Around the pitch axis the angular range of rotation is ±40° with pitch down (up) leading to increased (reduced) excitation of prosternal afferents (slope: -0.0072 act °, r2=0.48, N=2055, P<0.05). Thus, encoding of pitch is bidirectional and laterally symmetrical. Around the yaw axis the fly has limited mobility with an angular range of ±30°, although only a limited range of angles, ±15°, is evident in this figure, which shows variation in pure yaw, i.e. when pitch and roll are held close to rest. Yaw angles were occasionally larger in other sequences in which pitch and roll positions of the head also varied. Yaw rotations of the head toward (away from) the recorded side lead to increases (decreases) in excitation (slope: 0.0127 act °, r2=0.34, N=747, P<0.001). Thus, encoding of yaw is also bidirectional, but is laterally asymmetric.
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Interactions among pitch, yaw and roll
Since natural head posture may be a combination of rotations around several
axes, we investigated whether rotation around one axis could influence the PN
response to movements around another axis. For example, to examine the
influence of pitch on roll, we analyzed sequences in which yaw angles were
constant, i.e. within 2.5° of rest, and pitch angles were held constant at
several increments, e.g. 0.99°, 18.2° (rest), and 23.2°, while a
range of roll angles (N100) was tested at each pitch increment
(Fig. 6A-C). Then, the slope of
the relationship between PN activity and roll angle for each constant pitch
increment was plotted against that pitch value and a linear regression
calculated (Fig. 6D). If pitch
angle has no effect on the relationship of PN activity to roll, the slope of
the regression in Fig. 6D
should be flat, but this is not the case (slope=0.0002;
r2=0.42, P=0.0001), indicating that head pitch
angle strongly influences how the PO encodes head roll. The greater the pitch
up of the head, the steeper the slope of PN activity versus head roll
angle, i.e. the PO becomes more sensitive to roll when the head is pitched up.
Similar analyses were performed for many combinations of pitch, yaw and roll
to examine interactions among the axes. Several such linear regressions were
statistically significant (P<0.05)
(Table 1). Specifically, the
encoding of roll is affected by varying pitch (as described above) or yaw
angles, although the effect of increasing yaw is to decrease the sensitivity
of the PO to roll. Moreover, the relationship of PN activity versus
roll, which was shown above to be unidirectional when head position around the
other two axes is at rest, can be seen to be bidirectional when pitch is not
at rest.
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The foregoing analyses investigated relationships among PN activity and head position around each of the axes while position around a given axis was held constant. Flies, however, may move their heads simultaneously in all three directions with each having an effect on PN activity, and four-dimensional plots of the data reveal the complexity of these relationships (Fig. 7). The same general trends are evident in the three-dimensional data as are found in the one and two-dimensional analyses. Namely, PN activity varies negatively with pitch, i.e. pitch down leads to increased activity. PN activity varies positively with roll and yaw, but while the roll trend was apparent, the positive yaw trend was not clear in this three dimensional view and may be obscured by the other two directions.
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Temporal properties of prosternal organ afferents To investigate
whether the PN afferents respond tonically or phasically to head rotation, PN
activity was regressed against time for sequences in which head position was
held constant for intervals at least 264 ms and up to 1.4 s
(Fig. 8). For tonic activity,
the regression slopes should not differ from zero and for phasic activity
slopes should be significantly negative. Each of the 23 possible
conditions of head rotation preceding the plateau position, e.g. pitch
excitatory, roll inhibitory, yaw excitatory, etc was tested (N=6-25).
The average slopes within each condition were not significantly different from
zero (t-tests, P>0.05), with the exception of the
condition in which the change in pitch and yaw were inhibitory and the change
in roll was excitatory (N=25). Thus, generally PN activity is tonic
during periods of stable head position, but one condition revealed a slightly
phasic response. A closer look at the raw data suggests that individual, large
spiking units may fire phasically, while the remaining units fire tonically
(Fig. 2A), but we have not yet
separately analyzed individual units. The presence of phasic units among tonic
activity is very similar to sensory recordings of cockroach hair plates
(Pringle, 1938) or mantid
cervical hair plates (Liske,
1989).
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) and Axymyiidae (C.G., personal observation), in which the PO
is a single midline cluster of hairs. Anisopodidae has been considered to be
the sister taxon to the higher monophyletic suborder Brachycera
(Oosterbrook and Courtney,
1995). Among taxa in the lower Brachycera, where Stratiomyidae is
placed (Yeates, 2002;
Yeates and Wiegman, 1999), the
structure of the PO is quite variable compared to that among the advanced taxa
in the higher Brachycera, in which the PO comprises two widely separated
groups of hairs (Peters,
1962). In the lower Brachycera, the morphology is transitional
between a single cluster of hairs and two separated clusters. In some
families, such as Bombyliidae, both anteromedially fused and completely
separated hair plates are present (Yeates,
1994). This transitional morphology may be a response to selection
for increased precision or sensitivity in encoding head positions around some
axes, particularly roll, which could be accomplished by increased separation
of the left and right hair fields.
Directional selectivity of the PO may also be increased by two other
morphological properties: (1) the hair sockets and (2) the contact sclerite.
The asymmetrically raised cuticular collar or lip around each hair socket in
H. illucens appears to provide a physical barrier that limits the
directional deflection of each hair and thus imparts directional sensitivity
to individual PO sensory neurons. Such has been demonstrated for similar
appearing sockets of cervical hairs in honey bees
(Thurm, 1964), cercal hairs in
cockroaches (Camhi and Tom,
1978), and the bristles of the head in muscoid flies
(Theiß, 1979), although
Gaffal et al. (Gaffal et al.,
1975) caution that asymmetries of internal structures, such as the
socket septum, although related to external socket asymmetries, may be
sufficient to provide the directional sensitivity. The orientation of the
sockets varies across the PO, as in higher flies (C.G. and R. M. Burger,
unpublished). In H. illucens more lateral hairs have anterolateral
collars associated with restricting bending in the lateral direction and
permitting bending obliquely toward the midline of the PO. More medial hairs
have the collar more directly anterior and hairs would bend more readily
toward the posterior. Thus, there may be an incipient directional map laid out
by the differential orientation of the sockets across the PO in this fly, as
has been demonstrated for many macular type proprioceptive organs that sense
the orientation to gravity in invertebrates and vertebrates
(Schöne, 1975).
Another morphological mechanism to increase the directional precision of
the PO to head posture is a specialization of the posterior surface of the
contact sclerite (CS), which is covered by microtrichia
(Fig. 3C) that appear similar
to the `armored' membrane located around the leg, head-thorax, and
head-proboscis joints in many other brachycerous flies
(Gorb, 1997;
Gorb, 2001). Such membrane is
composed of spine- or scale-like protuberances, which can be used to fold
regions of membrane in specific spatial relation to one another based on how
the microtrichia link together (Gorb,
2001). The microtrichia on the H. illucens CS are spaced
quasi-regularly at a slightly narrower width than the PO hairs. Thus, the CS
microtrichia could act as a comb that temporarily engages the hairs of the PO
during a given head rotation to further constrain the deflection axis of the
hair during a particular rotation of the head. As the head returns to its
resting posture, the microtrichia would disengage the PO hairs. A similar
mechanism may exist in higher flies, such as Calliphoridae
(Preuss and Hangstenberg,
1992) and Sarcophagidae (C.G. and R. M. Burger, unpublished), that
also have a hirsute posterior margin of the contact sclerite.
Encoding of head position by the prosternal organ
Sensory afferent neurons of the PO of H. illucens respond to
rotation of the head about all three rotational axes: pitch, roll and yaw.
Their responses to pitch, and to some extent roll, validate the biomechanical
model of PO function developed by Peters
(Peters, 1962) and expanded by
Preuss and Hengstenberg (Preuss and
Hengstenberg, 1992). As the head pitches down, both left and right
contact sclerites would depress PO hairs further than their resting position
thereby increasing excitation, whereas pitch up would release some hairs from
their deflected resting position thereby decreasing excitation and producing a
bidirectional code for pitch angle. The present electrophysiological results
from H. illucens quantitatively support this model prediction over a
range of ±40° of pitch for a relatively primitive fly with a
single, anteriorly fused hair plate. The response, however, is not
symmetrical; i.e. the dynamic range for pitch down from 0° to -40° is
larger than that for pitch up from 0° to +40°. This bidirectional
asymmetry probably reflects the fact that at rest only a few hairs of either
hair plate are depressed. Similar qualitative electrophysiological results
(Gilbert et al., 1995) have
been obtained from an advanced muscoid fly in which the PO comprises widely
separated hair plates and the CS area is a large proportion of the hair plate
area. In many flies of the lower Brachycera, however, including H.
illucens, the contact sclerites are little more than small, lightly
sclerotized patches or folds in the gular arthrodial membrane
(Fig. 3) (C.G., A.P. and R. S.
Edgecomb, unpublished). Nevertheless, some hairs are deflected and excited at
rest, as Preuss and Hengstenberg (Preuss
and Hengstenberg, 1992) proposed, and thus the encoding of pitch
is bidirectional in H. illucens. Many anteromedial hairs, however,
are probably never touched by the CS in any head posture, but during pitch
down are probably deflected by less differentiated midsagittal membrane.
The model for encoding roll proposes that some hairs of the PO are
stimulated at rest and as the head is rolled down to one side the hairs would
be unilaterally deflected by the CS, thereby increasing excitation.
Conversely, with roll up, hairs would be released from excitation, again
producing a bidirectional code for roll, as with pitch. Behavioral
(Preuss and Hengstenberg,
1992; Gilbert and Bauer,
1998) and electrophysiological
(Gilbert et al., 1995) results
provide qualitative support for this model prediction in muscoid flies with
separated hair plates. The present experiments on a more primitive fly with
fused hair plates reveal more quantitative detail. Some PO afferents are
active at rest and their excitation increases linearly in response to roll
down by as much as 90° at roughly the same rate as for pitch. Roll up,
however, leads only to a slight decrease in excitation from the resting level
that is relatively uniform across the range of head angles. This non-linearity
in bidirectional coding appears almost unidirectional. Clearly some hairs that
are deflected at rest are released from that deflection with roll up, but not
to the extent that they are with pitch up, which produces linear bidirectional
coding over the full dynamic range of head movement around that axis. With
roll up in the range from about -20° to -90°, the signal in the
afferents of one hair plate is ambiguous. Such ambiguity could have been the
substrate for natural selection that drove the separation of the hair plates
in more advanced flies of the higher Brachycera. We have preliminary data,
however, from a muscoid fly, Neobellieria bullata (Sarcophagidae)
that the encoding is also non-linear with a strong increase of excitation in
response to roll down for angles as large as 90° and only a small range,
0° to -15°, over which excitation is reduced for roll up
(Paulk et al., 2001).
Finally, the current functional model does not address how the PO could
encode yaw. Muscoid flies can move their heads around the yaw axis more than
±20° (Land, 1975;
van Hateren and Schilstra,
1999) and many other flies, including H. illucens, can as
well. It is not clear, however, how such movement would be transmitted to the
sensory hairs of the PO. Peters (Peters,
1962) did not discuss such a possibility, but Preuss and
Hengstenberg (Preuss and Hengstenberg,
1992) discuss the lack of yaw-specific kinematic effects of the CS
on the hairs of the PO. The only evidence until now that the PO may be
involved in encoding yaw comes from an experiment by Liske
(Liske, 1977). In tethered
flying muscoid flies he perturbed the head around yaw axis and subsequently
measured syndirectional flight torque. A control experiment described in his
unpublished thesis (Liske,
1978) documents the abolition of the syndirectional torque
response when the PO is ablated. Unfortunately, the prosternum also contains a
proprioceptive chordotonal organ, the tendon of which inserts on the
presternum very near the PO, and Liske is not explicit that it remained intact
after the excision of the PO (Liske,
1978). Thus, in muscoid flies head yaw may or may not be encoded
by the PO. In H. illucens however, the PO sensory afferents respond
bidirectionally to head yaw. They are more excited during movements of the
head toward the recorded afferents and less excited by movements in the
opposite direction.
The foregoing discussion of how the PO can bidirectionally (for the most
part) encode pure pitch, roll, and yaw begs the question of how head position
is unambiguously encoded when a given head position may be composed of
rotations around more than one axis. Some head postures, such as pitch up,
improve encoding of position around other axes, such as roll. The increased
sensitivity of roll in that case, may be due to the reduction of confounding
PN activity associated with pitch. Such interactions would allow greater
precision for roll, which has the most angular degrees of freedom and is
crucial to visual stabilization during saccadic turning
(van Hateren and Schilstra,
1999). Such functional speculations on the adaptive significance
of the interaction of multi-axis rotations, however, overlook the precise
biomechanics of the neck membrane and sclerites during head movements. We
tried to observe these, but the ventral cervical area in soldier flies is not
clearly visible with the head in normal posture. Another fly, such as an
asilid, with a relatively long neck would be more suitable for studying
cervical biomechanical interactions as the head rotates around several axes to
understand better which hairs are being bent when the head is in different
postures. Such a study may be necessary to understand the apparent ambiguity
in excitation caused by multi-axis head rotation.
A simple neural scheme could allow the CNS to disambiguate pitch and roll by taking the common afferent activity in the left and right hair plates to determine pitch and the remaining difference in bilateral afferent activity to determine roll. Adding rotation around a third axis, i.e., yaw however, creates an ill-posed problem for the CNS - the head has three degrees of rotational freedom, but only two bilateral sources of information in the PO. One solution would be for PO hairs to have regional specialization, rather than having all hairs equivalent and simply encoding more or less deflection on their side. There are several morphological characteristics of the PO consistent with regional specialization. First, the hairs closest to the midsagittal plane are located such that they are rarely, if ever, contacted by a CS. Perhaps these hairs are only deflected by the gular membrane and only encode pitch. This would allow the two lateral regions of the hair plates to encode rotation around only two axes. But the two axes are roll and yaw, which are the most ambiguous due to their lateral asymmetries. Second, the distribution of hair socket orientations also suggests that there may be regional specialization across the PO that could contribute to disambiguation of head position. More lateral hairs, with sockets oriented toward the midline, could be deflected during head yaw. Whereas more medial hairs, with sockets oriented more anteroposteriorly, could be deflected during pitch or roll. Such differentiation of socket orientation could be the substrate for regional specialization of sensory hairs to direct directionally appropriate compensatory responses, which have not yet been demonstrated in this fly. If regional groups of hairs encode different directions of head movement, one might expect that the sensory fibers project to different areas of the thoracic neuropil where they could contact the dendritic fields of motorneurons that innervate different neck muscles. We have made backfills from the PO of H. illucens (C.G., A.P. and R. S. Edgecomb, unpublished), but have not noticed any gross differences in the projection patterns of afferent axons. Thus, the means by which this primitive fly, as well as the higher flies, disambiguate the signals of the sensory afferents of the prosternal organ to produce directionally appropriate responses in visually guided behaviors remains an open question.
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References |
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