Spatio-temporal patterns of antennal movements in the searching cockroach
Department of Biology, Graduate School of Sciences, Kyushu University, Fukuoka 812-8581, Japan
* Author for correspondence (e-mail: jokadscb{at}mbox.nc.kyushu-u.ac.jp)
Accepted 19 July 2004
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: insect, cockroach, Periplaneta americana, antenna, voluntary movement, searching behavior
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Active movements of insect antennae have been described in relation to
visual input (Honegger, 1981;
Erber et al., 1993
;
Horseman et al., 1997
;
Ye et al., 2003
;
Lent and Kwon, 2004
),
olfaction (Suzuki, 1975
;
Rust et al., 1976
;
Erber et al., 1993
;
Lent and Kwon, 2004
) and
tactile sense (Saager and Gewecke,
1989
; Erber et al.,
1993
,
1997
;
Pelletier and McLeod, 1994
;
Ehmer and Gronenberg,
1997a
,b
;
Okada et al., 2002
). These
reports, however, focused on the antennal response to various external
stimuli. Basic antennal behavior, in terms of the spontaneous rhythmic
activity itself, has been described in little detail. Moreover, as most insect
antennae are able to move in any direction, their activity has rarely been
measured in three dimensions. To our knowledge, the only exception is a study
on the stick insect (Dürr et al.,
2001
), in which voluntary antennal movement during walking was
analyzed three-dimensionally.
Each antenna of the American cockroach Periplaneta americana used
in the present study consists of two mobile basal segments, the scape and the
pedicel, while the remaining long distal group of segment is collectively
called the flagellum (Seelinger and Tobin,
1981). The headscape joint is operated by a muscular system
inside the head capsule: a single levator and an antagonistic pair of abductor
and adductor muscles, and thus may possess two rotation axes for the
horizontal and vertical movements. The scapepedicel joint is operated
by a pair of levator and depressor muscles inside the scape, so can move only
vertically. In addition, the neck participates in displacements of the entire
antenna. Head movement itself is reducible to yaw, roll and pitch components.
Thus, the movement of the antennal tip has six degrees of freedom in total.
Vigorous antennal movements are observed during searching behavior,
exploratory locomotion for finding resources. The searching is divisible into
two clear phases, the walking and pausing states. In both cases, the pair of
antennae actively probes their surroundings.
The purpose of this study was to characterize the spatial and temporal
properties of antennal movement in the cockroach. Trajectories described by
the flagellum tip were classified into some spatial patterns. Spectral
analyses combined with joint manipulations revealed the temporal features and
gross kinematics about the antennal joints. Cross-correlation analysis between
the paired horizontal and vertical components at the antennal joints was used
to clarify that coupling between the right and left antennal motor systems can
flexibly change, depending on the animal's behavioral state. Preliminary
reports have appeared elsewhere in abstract form
(Okada et al., 2001;
Okada and Toh, 2002
).
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experimental apparatus
A tethered animal was placed on top of a treadmill formed from a
free-moving Styrofoam ball to allow walking
(Fig. 1) as described in our
previous report (Okada and Toh,
2000). Movements of the antennae and head were recorded
simultaneously by a set of three video cameras (30 Hz frame rate), positioned
directly above, in front and to one side of the animal's head. Images from the
cameras were processed by a video multi-viewer (MV-40E, For-A Co., Tokyo,
Japan) to synthesize them on a four-way split screen, and videotaped. The data
were replayed and stored on a PC as AVI-formatted files through a
video-capturing interface, and then translated to BMP-formatted sequential
still images (640x480 pixels) using video-editing software (Adobe
Premiere; Adobe Systems Inc., San Jose, CA, USA). Spatial resolution of each
video frame was at 125188 µm/pixel. To register the coordinates of
body parts, the still images were sequentially imported to a custom program
written in Microsoft Visual Basic (Microsoft Co., Redmond, WA, USA). The
positions of the appendages and head (see the following section for detail)
were manually plotted frame-by-frame (33.3 ms interval) to register their
two-dimensional coordinates on the PC screen. The data were saved as
Text-formatted files.
|
Data analysis
To measure the positions of the head and both antennae, the body and head
axes were defined as reference (Fig.
2). The body axis is identical with the animal's midline from the
top view, and from the lateral view it passes the center of the neck socket
and runs parallel to the ground. The head axis is identical with the
rostrocaudal axis of the head capsule from the top view, and perpendicular to
the major flattened part of the frons from the lateral view
(Fig. 2A). The intersection of
the body and head axes, always lying near the center of head, was defined as
the origin for measuring subsequent angular displacements of the head and the
both antennae.
|
Head movements were categorized into three rotations: the yaw, roll and pitch components. We focus here on the two prominent yaw and pitch components. The yaw was defined as deviation of the head axis from the body axis from the top view (Fig. 2Ai), and the pitch as that from the lateral view (Fig. 2Aii). The roll was defined as rotation of the dorsoventral axis of the head capsule from the perpendicular (Fig. 2Bii). Because spatial resolution of images was noisy around the head capsule, time-series of these head positions were smoothed with a sliding window width of three frames (100 ms) to reduce effects of errors due to the manual digitizing. This process may not affect the head components since their frequencies were usually at less than 1 Hz in the present experimental condition. In the following, the yaw and pitch components are also referred to as the horizontal and vertical components, respectively. In both the locomotory and non-locomotory searching, the maximum displacement in yaw and pitch often attained a 3540° deflection. By contrast, roll was more restricted, 15° at most. The head capsule itself may also translate without rotation, but its effect on the orientation of the antennal tip was thought to be quite small compared to the effects of head rotations. Thus, we took no account of such translatory head movements in this study.
The horizontal and vertical deflections in antennae were defined as, respectively, azimuth and latitude of the flagellum with respect to the head axis (Fig. 2Bi). Points for registering antennal position were set at about a half-length of the flagellum on the PC screen. For horizontal deflections, to the right to the head axis was defined as positive, to the left as negative. For vertical deflections, the upper side to the head axis was defined as positive, the lower side as negative. Transformation of antennal positions from Cartesian to polar coordinates was performed in Microsoft Excel. The horizontal angular position ranged usually from 30° to 120° for the right antenna and the opposite for the left one (120° to 30°). But occasionally, it jumped suddenly to extreme positions with large displacements (>100°/frame). This unusual antennal shift was undoubtedly an artifact coming from measurement error in which discrimination was insufficient between antennal and head components. Such errors mostly occurred in the prominent dorsoventral deflections of both the antenna and the head. Since the movements had serious effects on the spectral and cross-correlation analyses that were difficult to treat, we neglected these occasional shifts in the analyses.
Movements of the foreleg were measured as horizontal angular displacements of the tarsus from the body axis (Fig. 2Ai). The origin was set at the posterior end of the pronotum on the body axis. For the foreleg position, to the right to the body axis was defined as positive, and to the left as negative.
Spectral analyses on the rhythmic antennal movements were performed by
using the fast Fourier transformation (FFT) function of Origin (OriginLab Co.,
Northampton, MA, USA). Horizontal or vertical antennal positions for >30 s
weresampled, and processed by the FFT function. Cross-correlation analyses for
exploring couplings between a pair of time-series were also conducted using
Origin. Temporal sequences of antennal movements (2348 s samples) were
partitioned sequentially into blocks of 3 s (90 data points), and correlation
coefficients (r) were calculated for each block over a range of
±1 s (lags of 30 data points). The critical value was determined as
r=0.25, according to the number of data points used for the
calculation in each test block (N=60). In order to compare coupling
strengths between the locomotory and nonlocomotory states quantitatively, the
correlation index (CI) was employed, and defined as the average of the
correlation coefficients at zero time lag for a series of blocks.
Differences between two data groups were examined statistically by the Wilcoxon test or the MannWhitney U-test. A result was judged significant when P<0.05.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Spatio-temporal aspects of the antennal and head movements
Active movements of both the antenna and the head were observed regardless
of the searching mode (Fig. 3).
This indicates that there is no substantial difference in both the antennal
and head movements between pausing and walking. However, as their time courses
were compared carefully, some quantitative differences emerged (see the
following).
|
The waveforms of the horizontal components resembled each other for the right and left antennae, suggesting that large amplitude deflections occur simultaneously in both antennae (Fig. 3). The relationship in the pair was anti-phase, i.e. an outward movement (abduction) in one antenna accompanied by an inward movement (adduction) of the other, and vice versa for movement in the opposite direction. This relationship was surveyed by cross-correlation analyses (see below). Large horizontal deflections during walking often accompanied whole body turns (data not shown).
Fig. 4 shows the angular ranges and the central positions of antennal deflections in pausing and walking. The angular range is given by the maximum and minimum values for the horizontal or vertical component in each test, and consequently, the working range is given as a difference between the two extreme values. The central position is defined as a median in the time-series of the horizontal or vertical component in each test. For the horizontal component, large deflections were observed more frequently in the pausing state than when walking (Figs 3, 4). The mean angular ranges in pausing were from 27.7° to 113.3°, and from 116.4° to 17.7° for the right and left antennae, respectively (N=10) (Fig. 4A). By contrast, those in walking were narrowed by 20° to 30°, from 3.6° to 105.5° and from 106.1° to 4.6° for the right and left antennae, respectively (N=10) (Fig. 4B). The bilateral overlap formed around the horizontal center was apparently larger in pausing than in walking (45.4° versus 8.2°). When both the right and left antennae were handled together as 20 antennae from 10 animals, there was a highly significant difference in the working range between pausing and walking (Wilcoxon test, P<0.01). The mean central positions for horizontal components did not change largely between the two behavioral states. When the horizontal central positions were transformed to the absolute angular deviations from the body axis in order to deal equally with both right and left antennae, however, they shifted significantly to more medial/frontal positions by about 5° (P<0.05).
|
For the vertical component, the mean angular ranges also changed according to the search mode (Fig. 4); 42.5° to 94.8° (right, pausing) and 50.0° to 89.5° (left, pausing) versus 46.1° to 81.6° (right, walking) and 51.2° to 70.0° (left, walking) (N=10). A statistical test detected a significant difference in working ranges between pausing and walking (Wilcoxson test, P<0.01). This indicates that the arc of vertical deflections was narrower in walking by 1020° than in pausing. Another change of the vertical component emerged in the mean central position, 30.7° (right, pausing) and 18.9° (left, pausing) versus 4.1° (right, walking) and 2.2° (left, walking) (N=10). Both antennae thus point to a lower position in walking (P<0.01). In the pausing state, the right antenna tended to be more elevated by 1015° than the left antenna (Fig. 4A). This difference between both antennae was observed in nine animals out of ten, and was highly significant (P<0.01). By contrast, there was no such difference in the walking state (Fig. 4B, P>0.05), implying that the tendency in pausing is due to the antennal behavior itself, and not to any artifacts (e.g. incorrect setting of animals to the experimental apparatus). To characterize this biasing in the antennal posture, however, further careful experiments would be required, and this issue remains to be investigated.
The three head components (yaw, roll and pitch) did not exhibit definite rhythmicity in the periods examined (<48.0 s), but fluctuated largely while in the pausing state (Fig. 3). The mean angular ranges for the yaw in pausing and walking were from 21.1° to 24.7° and from 12.9° to 16.4°, respectively (N=10) (Fig. 4). The working ranges of the yaw components were significantly narrowed by around 15° during walking (Wilcoxon test, P<0.05), but there was no difference in the central position between two behavioral states. For the pitch component, the mean angular ranges in pausing and walking were from 24.0° to 16.5° and from 19.9° to 15.8°, respectively (N=10) (Fig. 4), and there was no difference in both the working ranges and the central positions between two states. The yaw deflections consistently corresponded with large horizontal deflections in both antennae, and also with intended body turns (data not shown). It was unclear whether there is some coordination among the three head components or not. In some cases, however, coordinated activities were observed in two or in all three of the head components (e.g. see Fig. 3A, shaded area).
To quantify differences in temporal aspects of antennal rhythmic movements according to the behavioral state, FFTs were performed on the horizontal and vertical components (Fig. 5). In pausing, power-spectra for the horizontal and vertical deflections exhibited their major peaks at <3 Hz and <4 Hz, respectively (Fig. 5A). While walking (Fig. 5B), the horizontal deflection was mostly suppressed at lower frequencies (<2 Hz). This reflects, as described above, a decrease in the large horizontal deflections during walking. For the vertical component, particular peaks additionally appeared around 4 Hz, suggesting that the movement became faster. Actually, the waveforms in walking are composed of faster and larger discrete sinusoids than in the pausing state (Fig. 5, insets, and more clearly in Fig. 3). Though frequency bands differed more-or-less, the same tendencies were observed in the horizontal and vertical components in 16 and 13 examples, respectively, out of 20 antennae from 10 animals. Forelegs moved rhythmically, mainly at 23.5 Hz, during walking (Fig. 5B). Nevertheless, there was no conspicuous peak in the spectra for both horizontal and vertical components at the corresponding frequency band (23.5 Hz). It is therefore unlikely that passive effects, for instance caused by inertia, were involved in the antennal movements.
|
Trajectory patterns of the antennal and head movements
Trajectories of antennal and head movements were depicted by
two-dimensional coordinates (Fig.
6). The most frequent trajectory of the antenna was a seemingly
random pattern, i.e. no apparent spatial regularity in either the pausing or
walking state (Fig. 6, Case 1).
This random pattern was observed bilaterally in 8 out of 10 animals. The area
scanned by an antenna in a constant period was narrower in the walking state
than when pausing, mainly because of a decrease in the horizontal deflection.
The head behavior was similar to that of the antenna: the trajectory had
little regularity, and the angular range of yaw deflections decreased during
walking.
|
Regularity of antennal trajectories, however, was observed bilaterally in the other two examples illustrated. In the second example (Fig. 6, Case 2), the trajectory was rather random in the pausing state, but changed to a loop-like pattern when the animal started to walk. The third example showed the loop-like pattern independent of the locomotory state (Fig. 6, Case 3). The loop-like trajectory was composed not only of the loop, but also of two other basic pattern elements (see Fig. 6B2).The first pattern was a simple loop consisting of four sequential phases: levation, abduction, depression and adduction. In the second pattern, the antenna described an arch, in which a single cycle was formed from six sequential phases: levation, abduction, depression, and again levation, adduction and then depression. The third pattern was a simple vertical line: dorsoventral movement around the anterior extreme position.
Kinematics of the antennal joints
The position of the antennal tip is controlled mainly by two basal joints,
the headscape (HS) and scapepedicel (SP) joints.
The former is like a Cardan joint with two rotation axes and moveable in both
horizontally and vertically, while the latter is a hinge and can move only
vertically. In order to characterize the kinematics of these joints
independently, and to examine the behavioral state-dependency about each joint
movement, we tried to record antennal movements in which either the HS
or SP joint was immobilized with glue. However, most of the treated
animals behaved differently from the normal ones: they were depressed in
locomotion with almost no antennal movement, and otherwise continued to walk
or run with little antennal movement and zigzag turn. We only collected four
examples of relatively normal searching for each behavioral mode in each
joint-fixing condition (16 samples from 8 animals in total).
Trajectories in the condition with only the SP joints free were repeated vertical excursions in both pausing and walking (Fig. 7A). In the walking state, positions of both antennae were lowered entirely by 2030°. Fig. 7C shows the mean angular ranges and central positions of the vertical component in both states (N=4). The averaged angular ranges in pausing were from 8.6° to 61.9° (right) and from 21.6° to 54.0° (left), while in walking from 26.6° to 58.4° (right) and from 34.5° to 48.2° (left). The averaged central positions in pausing were at 28.4° (right) and 19.4° (left), and those in walking were at 5.5° (right) and 5.6° (left). Considering both right and left antennae together (total 8 antennae from 4 animals), the working range was significantly wider when walking than that when pausing (Wilcoxon test, P<0.05). This result was inconsistent with that in the normal condition (Fig. 4). Considering the sample number analyzed (20 versus 8), the data for normal antennae may be more reliable. Alternatively, the behavior of the antenna itself might have changed as a result of the joint manipulation. For the central position, there was a significant difference between the two searching modes (P<0.05). Thus, the SP joint may be involved in searching mode-dependency of the antennal vertical position.
|
Antennae in the HS joint-free condition draw two-dimensional patterns that were rather simple compared to those of the normal antennae (Fig. 8A). In particular, the trajectories were formed mostly from circular-pattern units (see Fig. 8A, pausing). The average horizontal angular ranges in pausing were from 3.7° to 83.8° (right) and from 83.3° to 1.2° (left), and in walking from 2.2° to 78.2° (right) and from 82.7° to 12.0° (left) (Fig. 8C). There was a significant difference in the working range between the two behavioral states (Wilcoxon test, P<0.05, N=8), indicating that the horizontal arcs of antennae were narrower in the walking state. This result was consistent with those for normal antennae (see Fig. 4). The horizontal central position unchanged between the two states (P>0.05) in this condition, although it was slightly shifted in the normal antenna to medial/frontal position by about 5° during walking (Fig. 4). For the vertical component, the mean angular ranges in pausing were from 28.4° to 49.5° (right) and from 30.4° to 52.5° (left), and in walking from 37.8° to 35.0° (right) and from 33.7° to 36.7° (left) (Fig. 8C). Though the working range did not alter significantly, the central position was lowered by about 15° (P<0.05). The results indicate that the HS joint also participates in searching mode-dependency of the antennal vertical position as well as the SP joint.
|
Spectral analyses applied to antennal movements in joint-manipulated animals revealed their temporal aspects (Figs 7B, 8B). With only the SP joint free (Fig. 7B), the power-spectrum for the vertical movement had its major peaks at 1.53.5 Hz in pausing. When walking, the major peaks were distributed over wider range up to 4.5 Hz. These characteristics of the vertical component were similar to those in the normal antenna (compare with Fig. 5). The same analyses on the horizontal component revealed only minute peaks, but their distribution pattern closely resembled that for the vertical component (data not shown). This effect is simply due to contamination by the vertical component, probably because the rotation axis of the SP joint is not precisely horizontal in the present coordinate system. In the HS joint-free condition (Fig. 8B), spectra for both the horizontal and vertical deflections had their main components at lower frequency (<1 or <2 Hz).Spectral patterns for the horizontal deflection were analogous to those in the normal condition for both locomotory modes (see Fig. 5).
Couplings between the right and left antennal motor systems
It appeared from inspection of the time courses of antennal movements that
the right and left horizontal components are coordinated in anti-phase
(Fig. 3), but the exact details
are still unclear. For vertical deflections, no obvious rule could be deduced
from the time courses of a pair of antennae. To investigate whether movement
of the pair of antennae is coordinated or not, cross-correlation analyses were
performed. Correlation coefficients, whose values should indicate the extent
of coupling, were calculated every 3 s in order to investigate the dynamic
feature of the coupling.
Fig. 9 shows an example from the pausing state. The trajectory patterns for both antennae were rather random, as in most cases (Fig. 9A). In the correlation map, significant negative correlations in the horizontal component appeared as spots from place to place (Fig. 9B). The correlation spots were relatively broad along the time lag axis, and deviated from the center (zero time lag). The timing of the negative correlations seemed to correspond to large amplitude movements, where both antennae move in the same direction. These suggest that the horizontal motor systems couple between the right and left sides for large amplitude movement in an anti-phase manner. By contrast, the vertical components exhibited significant correlations only very sparsely on the correlation map, indicating that there is little or no correlation between the right and left vertical motor systems during pausing (Fig. 9C).
|
When the searching mode changed to walking, the areas scanned by both antennae decreased and shifted to lower position, but the trajectory pattern was still disordered (Fig. 10A). A cross-correlation analysis for the horizontal components revealed that significant negative correlations were concentrated at zero time lag (Fig. 10B), compared with the correlation map in pausing (Fig. 9B). This suggests that the horizontal deflections in both antennae coordinate more precisely with each other in anti-phase. A more notable change was observed in the correlation map for vertical components: significant positive correlations occurred continuously at zero time lag, with sharp peaks (Fig. 10C). The result strongly suggests that the tight couplings between the right and left vertical systems were in orthophase. Actually, the waves for the vertical component were strictly synchronized between both antennae (see inset at Fig. 10C). In the correlation map, there were some places that positive (yellow to red) and negative (blue to black) spots appeared to alternate along the ordinate (time lag axis), which may represent synchronized oscillations of both antennae at a constant frequency (about 3 Hz in the case of Fig. 10C).
|
Correlation indices (CIs) were calculated for the horizontal and vertical components in both pausing and walking, and their differences were tested statistically between both states (Table 1). Since coupling was correlated most clearly at zero time lag, the analysis was restricted to the correlation coefficient there. The results revealed for both components that there were significant differences between pausing and walking (MannWhitney U-test, P<0.05). Thus the couplings between the right and left antennal motor systems may alter, depending on the mode of searching behavior.
|
An application of coupling analyses to the joint-manipulated specimens
appears to provide more detailed information about the searching
mode-dependency of antennal movement, in that the dependency could be
specified as kinematics in each joint. We performed cross-correlation analyses
for four samples in each searching mode and for each joint treatment, but for
both the horizontal and vertical components these failed to detect any CI
differences between the two searching modes (MannWhitney
U-test, P>0.05). Although most of the treated animals
exhibited unusual behavior, as described above, we carefully selected samples
that could be regarded as normal. In our previous report
(Okada and Toh, 2000), similar
behavioral changes were described in animals with immobilized antennal joints.
Such treatment may affect the antennal motor system, and thus its coordinated
outputs would be impaired even if an animal appeared to be behaving
naturally.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The joint-manipulation experiments provided information on the temporal characteristics of the horizontal and vertical components in normal antennae. When only the SP joint could move in the nearly vertical plane, a major component of the power-spectrum appeared at faster frequency (see examples in Fig. 7B; <3.5 Hz in pausing, <4.5 Hz in walking). On the other hand, when only the HS joint was free, spectral peaks for the horizontal component were observed mainly at lower frequency in both states (Fig. 8B; <2 Hz in pausing, <1 Hz in walking). These spectral patterns in joint-manipulated conditions closely resembled those seen in the normal condition (compare with the corresponding spectra in Fig. 5). It is therefore likely that the horizontal movement of antennae originates almost entirely from the HS joint, the fast vertical movement (presumably at >2 Hz) mainly from the SP joint, and the slow vertical one (at <2 Hz) from both the SP and HS joints.
Investigations of spatial distribution about the antennal joints and the head clarified the extent to which these two components contribute to the total displacement of antennae. Large amplitude movements in the head yaw and pitch components were more frequent in the pausing state, which may serve for intermittent careful probing of the surroundings. Roll movements were particularly observed during leg grooming: large roll deflections often amounted to 90° from the dorso-ventral plane (J.O. and Y.T., personal observation). From our experience to date, the temporal relationship between the three head components remains unclear, and warrants further analysis.
Spatial characteristics of the antennal movements were represented in their trajectories. The most striking feature was that the area scanned by an antenna altered depending on the mode of searching. In the intermittent pausing state, the antenna covered a relatively large area. This global scanning might contribute to the sensitive discovery of chemical and physical cues from resources at various places. Head movement also participated in the careful scanning as mentioned above. While in the walking state, the scanning area narrowed, mainly because of a decrease in the horizontal deflection, and the entire vertical position lowered. The joint-immobilization experiments specified in part which joint is related to these searching-mode dependencies of antennal movement. When only the HS joint was free, the horizontal angular range during walking significantly narrowed, as with normal antennae (Fig. 8C), suggesting that the HS joint is concerned in the mode-dependency. On the other hand, in the SP joint-free condition, the central position of the vertical component lowered significantly by about 25° during walking (Fig. 7C). Similarly, the lowering of vertical position (about 15° in amplitude) was observed in the HS joint-free condition (Fig. 8C). These results imply that both the SP and HS joints participated in the searching-mode dependency of the vertical central position.
An observation that the cockroach antennae tend to point forward at a low
angle was described in an earlier unpublished thesis study (McCoy,
1985,
1986
). Insects when walking
generally point their antennae to the front in order to detect forthcoming
gaps or obstacles (Pelletier and McLeod,
1994
; Horseman et al.,
1997
; Camhi and Johnson,
1999
; Dürr et al.,
2001
). In the cockroach, antennal oscillation seemed to be
suppressed according to the animal's locomotion. Actually, cockroaches almost
fixed their antennae anteriorly during running or flight (J.O. and Y.T.,
personal observation). However, Yagodin and Kovbasa
(1984
) reported in P.
americana that a vibration-like activity of the antenna with small
amplitude (around 1 mm) and fast frequency (310 Hz) is still observable
even in the flight. They also described from joint-fixation experiments that
self-stimulation of unidentified pedicellar mechanoreceptors by the active
vibration of antennae may be essential for maintenance of prolonged flight. It
is therefore possible that feedback from mechanoreceptors located at the
pedicel or its adjacent segments, such as the campaniform sensilla,
chordotonal organ and Johnston's organ, affects the locomotion center and
consequently or simultaneously the antennal motor center as well. Horseman et
al. (1997
) showed in the
cricket that the transection of the ipsilateral circumesophargeal connective
abolishes antennal oscillation in walking and the prolonged forward
positioning of antennae during flight. The authors concluded that the brain
may be insufficient to generate antennal movements, and that ascending inputs
from the subesophageal and/or thoracic ganglia are important for the
behavior-specific antennal movement and posture. Though we have not applied
such treatment to cockroaches, it might give some clues for
locomotion-dependent control of antennal movements and gross localization of
its center in the CNS.
Regularity in antennal trajectory patterns
In most cases analyzed here, antennal trajectories showed no patterned
regularity in either pausing or walking; however, in a few cases, the
loop-like pattern occurred (Fig.
6). It is still unclear whether the loop-like pattern was induced
by some unpredictable external stimuli or by unknown endogenous factors. We
found recently in independent experiments that the loop-like pattern is
related to tactile orientation behavior (J. Okada and Y. Toh, unpublished).
When a blinded animal encounters a stable object with its antennae while
searching, it may touch the object repeatedly with its antennae and try to
approach it (Okada and Toh,
2000). This positive thigmotaxis may be useful for finding
appropriate habitats such as narrow crevices. Our recent finding in the
tethered-walking condition was that once animals have released tactile
orientation behavior, many of them exhibit the loop-like pattern in their
antennal trajectory, which continues for more than a few minutes even in the
absence of tactile objects. It is thus likely that the antennal trajectory
pattern may reflect motivation of cockroaches.
The loop-like pattern could be subdivided into three basic pattern units,
the loop, arch and vertical line (see insets in
Fig. 6B2 for examples). The
loop and arch patterns are presumably attributable to coordination between the
horizontal and vertical deflections at the antennal joints. We surmise that
the pattern generation arises from coordinated activities between the vertical
motor system in the SP joint and the horizontal one in the HS
joint. To determine the extent of the coupling between these motor systems,
cross-correlation analysis is useful, but we hesitated to use this analysis
because the rotation axes of the joints were not precisely horizontal or
vertical. If cross-correlation analyses were applied to the ipsilateral
horizontal and vertical components using the present measuring system, the
results would contain many artefacts, indicating excessively large
correlations. An alternative method for avoiding such errors would be to
record activities of antennal muscles or motor nerves and to perform
cross-correlations. This should be a more reliable procedure for understanding
the central mechanism for the pattern generation directly, and is currently
under investigation using muscarinic agonists as the antennal rhythm generator
(for preliminary results, see Okada and
Toh, 2003).
Couplings between the right and left antennal motor systems
Cross-correlation analyses on searching cockroaches showed coupling
strengths between the right and left antennal motor systems in different
behavioral modes. The horizontal motor system comprises a pair of abductor and
adductor muscles for the scape. The vertical motor system involves two
elements: a levator muscle for the scape and a pair of levator and depressor
muscles for the pedicel. The center controlling these antennal motor systems
is located at the dorsal deutocerebrum (dorsal lobe) in many insects
(Rospars, 1988;
Homberg et al., 1989
). This
area also receives primary afferents of the antennal mechanoreceptors, so is
called alternatively the antennal mechanosensory and motor center (AMMC).
Moreover, in cockroaches, descending interneurons related to the antennal
mechanoreception send their dendrites to the dorsal lobe
(Burdohan and Comer, 1996
) and
crickets (Gebhardt and Honegger,
2001
). It may thus be a general feature in insects that the dorsal
lobe is regarded as the center for both integrating antennal mechanosensory
information and generating outputs for appropriate antennal motor
patterns.
Anti-phase couplings between the right and left horizontal systems were
consistently observed regardless of the searching mode (pausing/walking). The
coupling strength was significantly larger during walking than in pausing.
Couplings between the antennal horizontal component and the head yaw could not
be examined quantitatively in the present study because large yaw deflections
were rare in the data sampled. However, whenever sufficiently large yaw
deflections occurred, both antennae pointed in the same direction as the head.
In addition, large deflections in the antennae and head often accompanied
intended turns of the body. These suggest that the antennal horizontal motor
systems in both sides, which are probably composed of antagonistic pairs of
the abductor and adductor muscles for the scape, couple to the head yaw system
as well as to the steering system for walking. The anti-phase relationship in
the horizontal components of both antennae has been described in cockroaches
(McCoy, 1985,
1986
;
Okada et al., 2002
), crickets
(Honegger, 1981
;
Horseman et al., 1997
) and
stick insects (Dürr et al.,
2001
) as well as in crustaceans
(Zeil et al., 1985
). Thus,
this might be common to arthropods for active sensing of the physical
environment by antennation.
Coupling between the right and left vertical motor systems changed
dynamically depending on the animal's behavioral state. When an animal paused,
the coupling was relatively loose, but became coherent during walking. The
mode of coupling was orthophase: dorsoventral movements were synchronized
between the right and left antennae. The frequency of synchronization was
relatively fast at more than 2 Hz. Spectral analyses about the
joint-manipulated animals revealed that vertical deflections of the HS
joint contained few fast components at >2 Hz in its FFT spectra
(Fig. 8B). Thus, the
synchronized movement may originate mainly from the SP joints. As far
as we observed in the video images, it is unlikely that the antennal vertical
rhythmicity is always caused by contact with the ground, which is consistent
with observations in the stick insect
(Dürr et al., 2001).
Although some proprioceptors in the antenna may actually be involved
more-or-less in its oscillatory movements (e.g.
Okada et al., 2002
), the
synchronization of the vertical systems may derive essentially from the
antennal motor center in the dorsal deutocerebrum, independent of the
proprioceptive influence.
Temporal relationships were examined between antennae and legs. Coupling
analyses detected significant correlations only in one walk out of 14 (tested
in 14 animals). We therefore conclude that there is little evidence for
coupling between the antennae and the legs, as suggested earlier by McCoy
(1985,
1986
). Coordination between
the antenna and leg has been described in crickets
(Horseman et al., 1997
), stick
insects (Dürr et al.,
2001
) and crayfish (Sandeman
and Wilkens, 1983
), but is absent in locusts
(Saager and Gewecke, 1989
).
This inconsistency, including the present results, may simply reflect species
differences. Another interpretation is that the inconsistency is attributable
to methodological differences: some studies used quantitative analyses, but
others were based just on visual observation. It is possible that application
of reliable statistical analyses might yield different results.
How is the coordination or synchronization of antennal movements generated? Our survey is largely behavioral, so there is no physiological evidence bearing upon the question. A simple speculation for the phenomenon is that the antennal motor systems receive bilateral oscillatory inputs in common from an unknown locomotion-related center, and coordination or synchronization may be generated as the result. Another hypothesis is that the antennal motor systems in both sides themselves interact directly with each other, and entrainment arises between both antennae. This problem remains to be examined physiologically, and should be addressed initially with neural mechanisms in the dorsal deutocerebrum.
What is the purpose of coordination or synchronization in both antennae? The phenomenon was pronounced in the walking state. Because both antennae are aligned more in parallel during walking, antennation in this situation probably increases the opportunity to detect objects in front with both antennae simultaneously. This is more effective for gaining information about objects than using only a single antenna; simultaneous activation of both antennae could be concerned in identification of an object, and consequently in perception of its size.
We proposed in a previous study that cockroaches recognize the orientation
of stable objects by antennation (Okada
and Toh, 2000). A cluster of mechanosensitive hairs at the scape
(the scapal hair plate) is one potential candidate to perceive the orientation
of the antenna itself, and in turn the direction of objects. In addition, it
was recently reported that cockroaches can presumably discriminate texture or
shape of tactile objects by antennation
(Comer et al., 2003
), and these
behavioral studies suggest that mechanoreception by the active antenna
involves a variety of tactile modalities. We surmise that searching by
antennal scanning is an alternative strategy to vision for constructing a map
of the physical world in the brain, which is especially important for
nocturnal insects.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Altner, H. and Prillinger, L. (1980). Ultrastructure of invertebrate chemo-, thermo, and hygroreceptors and its functional significance. Int. Rev. Cytol. 67, 69-139.
Bell, W. J. (1991). Searching Behaviour: The Behavioural Ecology of Finding Resources. London: Chapman and Hall.
Burdohan, J. A. and Comer, C. M. (1996).
Cellular organization of an antennal mechanosensory pathway in the cockroach,
Periplaneta americana. J. Neurosci.
16,5830
-5843.
Camhi, J. M. and Johnson, E. N. (1999).
High-frequency steering maneuvers mediated by tactile cues: antennal
wall-following in the cockroach. J. Exp. Biol.
202,631
-643.
Chapman, R. F. (1982). Chemoreception: The significance of receptor numbers. Adv. Insect Physiol. 16,247 -356.
Comer, C. M., Parks, L., Halvorsen, M. B. and Breese-Terteling, A. (2003). The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions. J. Comp. Physiol. A 189,97 -103.
Dürr, V., König, Y. and Kittmann, R. (2001). The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern during walking. J. Comp. Physiol. A 187,131 -144.
Ehmer, B. and Gronenberg, W. (1997a). Antennal muscles and fast antennal movements in ants. J. Comp. Physiol. B 167,287 -296.
Ehmer, B. and Gronenberg, W. (1997b). Proprioceptors and fast antennal reflexes in the ant Odontomachus (Formicidae, Ponerinae). Cell Tissue Res. 290,153 -165.[CrossRef][Medline]
Erber, J., Pribbenow, B., Bauer, A. and Kloppenburg, P. (1993). Antennal reflexes in the honeybee: Tools for studying the nervous system. Apidologie 24,283 -296.
Erber, J., Pribbenow, B., Grandy, K. and Kierzek, S. (1997). Tactile motor learning in the antennal system of the honeybee (Apis mellifera L.). J. Comp. Physiol. A 181,355 -365.[CrossRef]
Gebhardt, M. and Honegger, H.-W. (2001).
Physiological characterisation of antennal mechanosensory descending
interneurons in an insect (Gryllus bimaculatus, Gryllus campestris)
brain. J. Exp. Biol.
204,2265
-2275.
Homberg, U., Christensen, T. A. and Hildebrand, J. G. (1989). Structure and function of the deutocerebrum in insects. Ann. Rev. Entomol. 34,477 -501.[CrossRef][Medline]
Honegger, H.-W. (1981). A preliminary note on a new optomotor response in crickets: Antennal tracking of moving targets. J. Comp. Physiol. 142,419 -421.
Horseman, B. G., Gebhardt, M. J. and Honegger, H.-W. (1997). Involvement of the suboesophargeal and thoracic ganglia in the control of antennal movements in crickets. J. Comp. Physiol. A 181,195 -204.
Keil, T. A. and Steinbrecht, R. A. (1984). Mechanosensitive and olfactory sensilla of insects. In Insect Ultrastructure, vol. 2 (ed. R. C. King and H. Akai), pp. 477-516. New York: Plenum Press.
Lee, J.-K. and Strausfeld, N. J. (1990). Structure, distribution and number of surface sensilla and their receptor cells on the olfactory appendages of the male moth Manduca sexta.J. Neurocytol. 19,519 -538.[Medline]
Lent, D. D. and Kwon, H.-W. (2004). Antennal
movements reveal associative learning in the American cockroach
Periplaneta americana. J. Exp. Biol.
207,369
-375.
McCoy, M. M. (1985). Antennal movements of the American cockroach Periplaneta americana. PhD thesis, University of Kansas.
McCoy, M. M. (1986). Antennal movements of the American cockroach Periplaneta americana. Diss. Abst. Int. 46,3327-B .
Norris, D. and Chu, H.-M. (1974). Morphology and ultrastructure of the antenna of male Periplaneta americana as related to chemoreception. Cell Tissue Res. 150, 1-9.[Medline]
Okada, J., Hinoue, K. and Toh, Y. (2001). 3-D analysis of spontaneous antennal movements in the cockroach Periplaneta americana. Zool. Sci. 18 Suppl, 92 (Abstr).
Okada, J., Kanamaru, Y. and Toh, Y. (2002). Mechanosensory control of antennal movement by scapal hair plates in the American cockroach. Zool. Sci. 19,1201 -1210.[Medline]
Okada, J. and Toh, Y. (2000). The role of antennal hair plates in object-guided tactile orientation of the cockroach (Periplaneta americana). J. Comp. Physiol. A 186,849 -857.[Medline]
Okada, J. and Toh, Y. (2002). A three dimensional analysis of antennal movement in the tactile orientation behavior of American cockroaches. Zool. Sci. 19, 1463 (Abstr).
Okada, J. and Toh, Y. (2003). Antennal movements in cockroaches: A comparison between the spontaneous and drug-induced patterns. Zool. Sci. 20, 1572 (Abstr).
Pelletier, Y. and McLeod, C. D. (1994). Obstacle perception by insect antennae during terrestrial locomotion. Physiol. Entomol. 19,360 -362.
Rospars, J. P. (1988). Structure and development of the insect antennodeutocerebral system. Int. J. Insect. Morphol. Embryol. 17,243 -294.[CrossRef]
Rust, M. K., Burk, T. and Bell, W. J. (1976). Pheromone-stimulated locomotory and orientation responses in the American cockroach. Anim. Behav. 24, 52-67.
Saager, F. and Gewecke, M. (1989). Antennal reflexes in the desert locust Schistocerca gregaria. J. Exp. Biol. 147,519 -532.
Sandeman, D. C. and Wilkens, L. A. (1983). Motor control of movements of the antennal flagellum in the Australian crayfish, Euastacus armatus. J. Exp. Biol. 105,253 -273.
Schafer, R. and Sanchez, T. V. (1973). Antennal sensory system of the cockroach, Periplaneta americana: Postembryonic development and morphology of the sense organs. J. Comp. Neurol. 149,335 -354.[Medline]
Schaller, D. (1978). Antennal sensory system of Periplaneta americana L: Distribution and frequency of morphologic types of sensilla and their sex-specific changes during postembryonic development. Cell Tissue Res. 191,121 -139.[Medline]
Schneider, D. (1964). Insect antennae. Ann. Rev. Entomol. 8,103 -122.[CrossRef]
Seelinger, G. and Tobin, T. R. (1981). Sense organs. In The American Cockroach (ed. W. J. Bell and K. G. Adiyodi), pp. 217-245. London: Chapman and Hall.
Steinbrecht, R. A. (1984). Chemo-, hygro, and thermoreceptors. In Biology of the Integument, vol.1 (ed. J. Bereiter-Hahn, A. G. Matoltsy and K. S. Richards), pp. 523-553. Berlin: Springer-Verlag.
Suzuki, H. (1975). Antennal movements induced by odour and central projection of the antennal neurones in the honey-bee. J. Insect Physiol. 21,831 -847.[CrossRef]
Toh, Y. (1977). Fine structure of antennal sense organs of the male cockroach, Periplaneta americana. J. Ultrastruct. Res. 60,373 -394.[Medline]
Yagodin, S. V. and Kovbasa, S. I. (1984). The flight maintenance mechanisms in the cockroach Periplaneta americana L. J. Comp. Physiol. A 155,697 -712.
Ye, S., Leung, V., Khan, A., Baba, Y. and Comer, C. M. (2003). The antennal system and cockroach evasive behavior. I. Roles for visual and mechanosensory cues in the response. J. Comp. Physiol. A 189,89 -96.
Zacharuk, R. Y. (1985). Antennae and sensilla. In Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 6 (ed. G. A. Kerkut and L. I. Gilbert), pp. 1-69. Oxford: Pergamon Press.
Zeil, J., Sandeman, R. and Sandeman, D. C. (1985). Tactile localization: The function of active antennal movements in the crayfish Cherax destructor. J. Comp. Physiol. A 157,607 -617.[Medline]