First published online October 7, 2004
Journal of Experimental Biology 207, 3985-3997 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01228
The effects of head and tail stimulation on the withdrawal startle response of the rope fish (Erpetoichthys calabaricus)
Hilary S. Bierman1,
Julie E. Schriefer2,
Steven J. Zottoli4 and
Melina E. Hale1,2,3,*
1 Committee on Neurobiology, University of Chicago, Chicago, IL 60637,
USA
2 Department of Organismal Biology and Anatomy, University of Chicago,
Chicago, IL 60637, USA
3 Committee on Computational Neuroscience, University of Chicago, Chicago,
IL 60637, USA
4 Department of Biology, Williams College, Williamstown, MA 01267,
USA
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Fig. 1. Images and silhouettes of withdrawal behavior in Erpetoichthys
calabaricus. All images and silhouettes are oriented with the fish's head
to the right. (A) Time series of withdrawal to a head-directed stimulus. The
head initially rotates to one side (20 ms) in the pre-transition stage of
movement. After the transition point, the head is pulled back from the
stimulus and continues to rotate. (B) Silhouettes show examples of four
withdrawals to head-directed stimuli. One silhouette is shown for each of the
study animals. For an individual withdrawal, the silhouettes get darker
through the response. (C) Time series of withdrawal to a tail-directed
stimulus. (D) Silhouettes show examples of four withdrawals to tail-directed
stimuli. One silhouette is shown for each of the study animals. The response
to tail stimulation results in greater movement during withdrawal than the
response to head stimulation. In addition, unlike for responses to head
stimulation, responses to tail stimulation generally involve a post-withdrawal
propulsive stage of movement.
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Fig. 2. Head angle rotation during withdrawal responses. (A) Overlay of lines drawn
through the stiff rostral section of the fish at 4-ms intervals through the
course of a tail stimulus elicited withdrawal. Kinematic landmarks, located at
the head, are denoted by black (start of response), grey (transition point)
and white (end of withdrawal) circles. (B) Head angle measurements for the
same trial as in A, normalized to a start angle of zero and plotted as angle
over duration of response. A six-degree polynomial was used to fit the data to
a line. In this trial, the transition point (double-headed arrow) is reached
at 0.036 s, and the end of withdrawal (single-headed arrow) is at 0.06 s. (C)
Comparison of head angle during the periods from initiation of response to the
transition point and from the transition point to the end of withdrawal show
significantly greater angle movement during the former period
(P>0.0001) but no statistical difference between head and
tail-elicited responses.
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Fig. 3. Body extension ratio and movement during response to head- and
tail-directed stimuli. (A) Examples from three different fish showing the
change in body extension over the duration of response to head-directed
stimuli (dotted line) and tail-directed stimuli (solid line). Start of
response was set at 0 ms, and the extension ratio was measured as distance
between head and tail divided by total body length (BL). Kinematic
landmarks are denoted: transition point (1), end of withdrawal (2) and peak of
omega-like body shape (3). (B) The overall distance in body lengths moved by
the head and the tail during the withdrawal in response to head and tail
stimulation. Also shown is the overall distance moved by the center of mass
during the 48 ms following the withdrawal (post-withdrawal). There is
significantly more post-withdrawal movement of the center of mass in
tail-elicited responses than in head-elicited responses.
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Fig. 4. Duration and velocity of movement during withdrawal response. (A) Bar
graphs showing total mean withdrawal duration and mean withdrawal duration
before and after transition point (see text description of transition point)
for responses elicited by head- and tail-directed stimuli. (B) Mean velocity
of movement of the head and tail over the withdrawal response to head- and
tail-directed stimuli.
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Fig. 5. Example of a withdrawal trial in response to head stimulation. (A)
Silhouettes at three kinematic stages – initiation, transition and end
of withdrawal–are shown. (B) Six electrodes were implanted in pairs
along the length of the body. Asterisk indicates centre of mass. (C) EMG
activity for the electrodes shown in B. Broken lines represent kinematic
stages illustrated in A and are numbered accordingly: (1) initiation, (2)
transition point and (3) end of withdrawal. Compared with tail-stimulation
trials (Figs 6,
8) from the same fish, there is
relatively little muscle activity in response to head stimulation both in
terms of numbers of electrodes active and amplitude of activity. When
comparing figures, note that the scale bar for tail stimulation trials is four
times that of head stimulation trials, further emphasizing the difference in
strength. No muscle activity is present after the initial burst around the
onset of kinematic activity. Scale bar, 0.2 mV.
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Fig. 6. Example of a withdrawal trial in response to tail stimulation. (A)
Silhouettes at four kinematic stages – initiation, transition, end of
withdrawal and omega – are shown. (B) Six electrodes were implanted in
pairs along the length of the body. Asterisk indicates centre of mass. (C) EMG
activity for the electrodes shown in B. Broken lines represent kinematic
stages illustrated in A and are numbered accordingly: (1) initiation, (2)
transition point, (3) end of withdrawal and (4) omega. Compared with head
stimulation trials (Figs 5,
7) from the same fish, there is
strong activity of axial muscle in response to tail stimulation. In addition
to greater numbers of electrodes being active and those electrodes having
stronger activity, there is secondary activity after the initial burst
associated with movement after the initial withdrawal. Scale bar, 0.8 mV.
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Fig. 7. Additional trials of the fish illustrated in Figs
5,
6 are shown to illustrate the
diversity of response within an individual and for the same electrodes. Broken
lines and numbers correspond to the numbering in the previous corresponding
figures: (1) initiation, (2) transition point, (3) end of withdrawal and (4)
omega. Note that the differences in the strengths of activity across
electrodes may in part be due to variability in electrode construction and
placement. (A) Head stimulation trials comparable to the trial illustrated in
Fig. 5. (B) Tail stimulation
trials comparable to the trial illustrated in
Fig. 6. We show a total of six
trials from one fish (three head stimuli and three tail stimuli; Figs
5,
6, 7) so that the EMG activity
patterns can be compared for individual electrodes across trials. Scale bar:
0.2 mV (head stimulus trials) and 0.8 mV (tail stimulus trials).
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Fig. 8. Cross section (15 µm) through the right Mauthner cell of
Erpetoichthys calabaricus. The soma (S) of the Mauthner cell is
centered in this photomicrograph. The lateral dendrite extends towards the
right, where it bifurcates (arrows designate two branches) near the entry of
the VIIIth cranial nerve. The axon (A) projects to the left toward the
midline. Fibers that run parallel to the Mauthner axon project toward the soma
and form a network of fibers around the initial segment of the axon to form
the axon cap (delineated with a circle). Dorsal is up, and the open space
above the Mauthner axon is the IVth ventricle. Scale bar, 40 µm.
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© The Company of Biologists Ltd 2004
