First published online June 13, 2008
Journal of Experimental Biology 211, 2123-2133 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019125
Front leg movements and tibial motoneurons underlying auditory steering in the cricket (Gryllus bimaculatus deGeer)
T. Baden and
B. Hedwig*
Department of Zoology, University of Cambridge, Downing Street, Cambridge
CB2 3EJ, UK
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Fig. 1. Movements of the left front leg during phonotaxis. (A) Animals responded to
alternating six-chirp sequences from the left and right with steering towards
the active speaker. During steering to the contralateral (right) speaker the
left front leg performed large left–right movements towards the
stimulated side, but during steering to the ipsilateral (left) speaker only
small left–right movements occurred. The pattern of up–down leg
movements was constant. (B) Rapid change in leg movement; section from A as
indicated. The red trace is an exact copy of the first step shown, indicating
the leg movement without a turn. Within two syllables of ipsilateral sound
presentation (60 ms) the movement deviates from the predicted trace. (C)
Up–down and left–right recordings of left front leg movements
during steering were combined into 2D projections. The background photograph
was taken independently for illustrative purposes. During steering to the
contralateral (right) speaker the anterior extreme point (AEP, asterisk) of
the left front leg was shifted in front of the head during the swing phase.
This allowed animals to pull towards the active speaker during the following
stance phase. By contrast, during steering to the ipsilateral (left) speaker
the AEP was directly in front of the leg resting position.
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Fig. 2. Bilateral steering movements of the left front leg. (A) A third of animals
exhibited strong steering movements of the front leg towards both ipsilateral
and contralateral acoustic stimulation. In less than 10% of cases the step
rhythm was disrupted during a turn (asterisk). (B) Two-dimensional projections
of up–down and left–right movement components of the left front
leg. The AEP (asterisk) was shifted towards the respective active speaker
during both contralateral (right) and ipsilateral (left) sound presentation.
This allowed the animal to pull towards the active speaker during the
following stance phase for both ipsilateral and contralateral steering.
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Fig. 3. Phase relations between step and sound rhythms. (A) Interval histogram of
step cycle durations ranging between 250 and 600 ms, with a mean of 396 ms.
(B) Phase diagram of chirps within the step cycle. This revealed no indication
that the step cycle was coupled to the chirp pattern. (C) Double pulse
paradigm with the first and last two syllables of a chirp presented from
contralateral (right), but the middle two syllables presented from ipsilateral
(left) speakers (top traces). Stepping cycles were sorted into 20 bins
according to the phase values of acoustic stimulation; only four bins are
shown for clarity. Only when the ipsilateral two syllables occurred during
swing phase, were left–right front leg movements smaller in the
following stance phase (asterisk).
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Fig. 4. Tibial muscles and EMG recordings during walking. (A) A single tibia
extensor muscle (red, 135) extends dorsally throughout the entire length of
the femur. Four tibia flexor muscle bundles (green, 136a–d) were located
ventrally. A retractor unguis (pink, 139) runs anteriorly along the acoustic
trachea. (B) Simultaneous tibial extensor and tibial flexor EMG recordings
were taken at positions as indicated in A. Large amplitude muscle potentials
recorded in the extensor were directly related to small amplitude muscle
potentials measured in the flexor, and vice versa. (C) Amplitude histogram of
gliding length filtered tibial extensor EMG recording of a walking cricket.
Four different motor units were clearly identified. A muscle potential
attributed to FETi is shown only in the EMG recording because of its large
amplitude. FETi spikes occurred very rarely during walking (1 in 20 steps) and
are not visible in the histogram. (D) EMG recordings were obtained during
walking, with simultaneous recordings of forward-backward movements of the
femur as an indication of the step cycle. Peaks of the EMGs were sorted
according to amplitudes: FETi>SETi>FFTi>SFTi. The occurrence of motor
unit activity within each step was normalised to the mean duration of steps
(390 ms).
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Fig. 5. EMG recordings during phonotaxis. (A) Alternating six-chirp sequences from
the left and right were related to right front extensor tibiae EMG traces
while animals were acoustically orienting on a trackball. In single trace EMG
recordings the step pattern was the dominant modulation in motor unit
activity. (B) Averaging EMG activity with respect to the start of the
contralateral sound pattern revealed the auditory input to tibial motoneurons.
SETi spike rate increased in response to ipsilateral (right) sound, and FFTi
spike rate was modulated by contralateral (left) sound. SFTi activity was
unaffected. The spike rate of FETi was too low to reveal any auditory
activation and is not presented.
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Fig. 6. Timing of auditory inputs to SETi. (A,B) Animals acoustically orienting on
the trackball were presented with the double pulse paradigm. The trackball
recording revealed steering towards the stimulated side with a delay of
55–60 ms. Simultaneously recorded EMG traces reveal an increase in SETi
activity with a delay of 35–40 ms after ipsilateral (right) sound
presentation.
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Fig. 7. Morphology of tibial motoneurons. Motoneurons were located dorsally in the
prothoracic ganglion, with ventral somata. The amplitude of EMG potentials
elicited by spikes in each respective motoneuron is indicated. (A) Structure
of the FETi (N=12 stainings) and SETi (N=28). (B) Structure
of the FFTi1 (N=6) and the FFTi2–5 (N=12). (C) Example
of a SFTi1–3 (N=15). The projection patterns of the main
neurites varied between SFTi motoneurons, but the soma position and the
overall dendritic field was very similar.
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Fig. 8. Sensory and central inputs to tibial motoneurons. (A) Intracellular
recordings of SETi (left) and SFTi1–3 (right) at rest. No synaptic
activity was recorded in SETi, while SFTi1–3 received frequent synaptic
inputs. (B) Sensory stimulation during hyperpolarising current injection to
unmask any weak inputs. Motoneurons at rest did not respond to auditory or
visual inputs, but did respond to wind and tactile inputs. (C) Extracellular
electrical stimulation of descending pathways evoked EPSPs and spikes in all
motoneurons. Four examples are shown of recordings with increasing stimulation
amplitude. (D) Bath application of pilocarpine or picrotoxin elicited motor
bursts in all motoneurons.
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Fig. 9. Can auditory inputs be gated? Intracellular recordings of SETi during
stimulation of descending pathways (A) and during pharmacologically elicited
motor activity using pilocarpine (B) or picrotoxin (not shown). Chirps (4.8
kHz 90 dB) were presented at 2 Hz repetition rate. Neither stimulation of
descending pathways nor pharmacological manipulation gated any auditory inputs
to SETi. In both cases a hyperpolarising current (5 nA) was injected to reveal
even small inputs.
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© The Company of Biologists Ltd 2008
