Journal
of Comparative
Physiology. A
J Comp Physiol(i981) 142:339-346
9 Springer-Verlag 1981
Properties of the Escape System of Cockroaches During Walking
Jeffrey M. Camhi and Thomas G. Nolen
Section of Neurobiologyand Behavior, Divisionof Biological Sciences, LangmuirLaboratory, Cornell University,
Ithaca, New York 14850, USA
Accepted December 30, 1980
Summary. 1. Adult male cockroaches (Periplaneta
americana) which were fixed in place but could move
their legs normally were presented with wind puffs
of different amplitudes. The puffs were given while
the cockroaches were walking at different speeds,
standing or grooming their antennae. In different experiments we recorded either the movement responses
of one metathoracic leg or the action potentials from
impaled, individually identified giant interneurons.
2. Cockroaches were most responsive behaviorally
to wind puffs presented during slow walking (1-4
steps/s). At such times the latency was shortest (1118 ms for large puffs) and the threshold lowest
(Fig. 2). The threshold wind puff, having a peak velocity of 3 ram/s, evoked a pause in walking. Puffs of
12 mm/s or larger evoked running.
3. The ventral giant interneurons (GI's) though
known to be inhibited slightly during slow walking
(Daley and Delcomyn 1980a) are still activated by
wind puffs of 3 or 12 mm/s (Fig. 3) and thus can
contribute to the behaviors that these small wind stimuli evoke. Pronounced inhibition of the ventral GI's
occurred only during fast walking (Fig. 4). The dorsal
GI's appear to be insufficiently activated by these
small winds to contribute to the havior.
4. In response to large wind puffs presented during
slow walking, the behavioral latency is so short that
only a few action potentials of the largest ventral
GI's appear to be capable of mediating the onset
of the behavior. The dorsal GI's appear to be activated too late to contribute to initiating the behavior.
5. The information suggesting that the ventral,
and not the dorsal GI's initiate the escape behavior
has permitted us to develop a coherent model of the
escape system in which all the known synaptic interactions involving both the ventral and the dorsal GI's
have a meaningful role (Fig. 5). The model includes
negative feedback onto the ventral GI's and positive
Abbreviation." G[ giant interneuron
feedback onto the dorsal GI's from the motor system.
According to this model, the ventral GI's initiate and
steer the early part of the escape behavior, and the
dorsal GI's maintain and steer the subsequent phases
of the behavior.
Introduction
Cockroaches (Periplaneta americana) are known to
respond to gentle wind puffs by turning away from
the source of wind and running. This behavior is
mediated by wind-receptive hairs on the cerci (Camhi
and Tom 1978). The wind-mediated evasive behavior
appears to be this insect's major or only means of
escaping from the strike of a natural predator of cockroaches, the toad Bufo marinus (Camhi et al. 1978).
The cockroach is extremely sensitive to wind, permitting early detection of the air disturbance made by
the toad's lunge (Camhi et al. 1978).
Cockroaches are active walkers. In fact, it is during walking that they are most likely to encounter
predators. Moreover, since many nocturnal predators
are visually most sensitive to moving prey (e.g. Ewert
1976), a walking cockroach probably is especially vulnerable to attack. Paradoxically, however, one group
of giant interneurons (GI's) that appears to contribute
in mediating the escape behavior, the ventral GI's,
are inhibited while the cockroach walks (Ritzmann
and Camhi 1978; Ritzmann 1979; Daley and Delcomyn 1980a, b). The ventral GI's comprise 4 neurons
on each side of the nerve cord, designated as GI's
1 through 4 (Camhi 1976). GI's 1 through 3 are in
fact the GI's with the greatest axonal diameter and
thus the fastest conduction, and are also the first
to initiate action potentials in response to wind puffs
(Westin et al. 1977). The remaining, dorsal group
of GI's (numbers 5, 6, and 7 on each side) are not
0340-7594/81/0142/0339/$01.60
340
i n h i b i t e d d u r i n g w a l k i n g , a n d so p r e s e n t n o p r o b l e m .
(In fact, these dorsal GI's are mildly excited during
w a l k i n g ; D a l e y a n d D e l c o m y n 1 9 8 0 a , b).
T h e s e c o n s i d e r a t i o n s h a v e led u s t o c o m p a r e in
standing versus walking cockroaches both the escape
behavior and the responses of ventral GI's. We find
t h a t t h e e s c a p e b e h a v i o r is m u c h m o r e r e a d i l y e v o k e d
b y w i n d p u f f s d e l i v e r e d w h i l e t h e c o c k r o a c h is w a l k i n g slowly. D u r i n g s u c h s l o w w a l k i n g t h e i n h i b i t i o n
o f t h e v e n t r a l G I ' s is o n l y v e r y slight. I n fact, f o r
large wind puffs presented during slow walking, the
b e h a v i o r a l l a t e n c y is so s h o r t t h a t o n l y t h e s e v e n t r a l
G I ' s a p p e a r to b e c a p a b l e o f i n i t i a t i n g t h e m o t o r
output. Also, even wind puffs that are just suprathreshold for the behavior in slowly walking cockroaches evoke some action potentials in the ventral
G I ' s , a n d little o r n o r e s p o n s e i n t h e d o r s a l G I ' s .
T h i s i n f o r m a t i o n is u s e d t o c o n s t r u c t a m o d e l o f t h e
known synaptic relations involving the ventral and
dorsal GI's which suggests different roles for these
two groups of interneurons.
Materials and Methods
Adult male Periplaneta americana were used in these, as in our
earlier studies. The animals were purchased as adults from commercial suppliers. They were kept in 30 gallon barrels with screen
tops and were fed dog chow and water ad lib. Some animals
were kept in constant light at 27 ~ with variable humidity, and
others were kept in our laboratory without any special lights or
other controls. No consistent differences were noted among these
groups of insects.
In all experiments, an unanesthetized cockroach whose wings
had been cut off was placed on a lucite substrate lubricated with
light machine oil, and four vertical pins were placed through the
lateral margins of its abdomen. The pins were inserted into a
drop of wax adhering to the lucite platform. Care was taken to
prevent the cerci from touching the lubricated surface. Also, if
the cerci were groomed by a leg at any time, thereby possibly
covering the cercal hairs with lubricant, the experiment was terminated. More than half of the cockroaches prepared in this way
made walking movements with all six legs in which the inter-leg
coordination appeared normal. Also, these walking movements
were indistinguishable from those of unrestrained cockroaches as
studied through EMG recordings from single hind legs or recordings of the movements of both hind legs (D. Daley, personal communication).
The open end of a copper tube through which wind puffs
were delivered was positioned 20 mm behind the tips of the cerci.
Upstream from the open end of this tube was the active wire
of a hot wire anemometer (Datametrics 800 VPT), used to record
instantaneous puff amplitude. The anemometer had a flat frequency response to wind signals of roughly 0-100 Hz. Before and
after a set of experiments, the puff amplitude recorded inside the
delivery tube was calibrated with respect to that at the cerci by
placing the probe of a second, identical anemometer at the cercal
position. Both anemometers were periodically calibrated by methods already described (Camhi et al. 1978) and were stable to within
_+ 10% over periods of several months.
The wind puff generator, which consisted of a solenoid whose
moving arm pushed a rubber membrane, was described in detail
J.M. Camhi and T.G. Noien: Escape System of Walking Cockroaches
by Westin et al. (1977). By pushing downward on the membrane,
wind was directed out through the delivery tube and over the
cerci from behind the animal. By lifting up on the membrane,
the opposite direction of wind was created. It was possible, by
mechanically limiting the excursion of the solenoid's arm, to vary
the peak amplitudes of the puffs between 0.001 and 2.6 m/s, as
recorded at the cerci.
The movements of the right metathoracic leg were monitored
during ongoing walking and during responses to wind puffs by
means of two photocells, each 4 mm wide, located beneath the
lucite substrate. In a darkened room, the photocells detected the
leg's movement by the shadow cast from a light guide above the
cockroach. The photocells had a rise time of less than 1 ms, as
determined by shining light through a camera's shutter which
opened for 1 ms. They recorded leg movements of less than 15 ~tm
as determined by moving an ablated leg over them with a micromanipulator. If the response to a puff began while the shadow
was partially over one of the photocells, as determined from the
records, the behavioral latency could be measured to the nearest
IIIS.
To record from the giant internenrons of a walking eockroach~
the animal was prepared in the manner just described. Then, after
being pinned in place, its ventral nerve cord was exposed by dissection. No anesthesia was used. The medial region of the dorsal
cuticle was dissected away between the second and fifth abdominal
tergites. The digestive tract was severed at the anterior and posterior limits of the exposed area and the freed section of gut was
removed. The abdominal cavity was flushed with saline (Callec
and Satelle 1973) taking care not to wet the cerci or the lucite
platform. After cutting the peripheral roots of ganglia A3 and
A,, a wax covered supporting platform was placed under the A~ s
connective. Saline was perfused over the cord and aspirated away.
Glass microelectrodes filled with 4% Procion yellow M4RS in
0.2 mol/1 KCI or whose tips were filled with 3% Lucifer yellow
and then backfilled with 0.1 mol/1 LiC1 were used for all recordings,
which were amplified by a WPI M701 DC amplifier. After recordings a neuron's responses to wind, the dye was introduced into
the cell for 5 to 30 rain by passing current pulses of 5x 10 -s A.
The pulses lasted 0.5 s and were repeated every second. Subsequently, the nerve cord was dissected free, fixed in 10% formalin in
saline, embedded in paraffin, cross sectioned at 10 gm and viewed
by fluorescence microscopy. The filled giant axon was identified
by its position relative to other giant axons within the nearest
abdominal ganglion (Camhi 1976).
In all experiments, the outputs of the photocells, anemometer
and DC amplifier were led to an instrumentation tape recorder
(Hewlett Packard 3968) having a frequency response of 0-2.5 kHz.
All signals were led to a Tektronix 565 oscilloscope for filming
with a Grass C4 kymograph camera.
Results
Behavioral Responses to Wind Puff~
Cockroaches were presented with wind puffs having
a p e a k a m p l i t u d e o f 2.6 m / s w h i l e t h e y w e r e e n g a g e d
i n t h e f o l l o w i n g b e h a v i o r s : w a l k i n g in p l a c e a t differe n t s t e p p i n g r a t e s , s t a n d i n g still f o r d i f f e r e n t d u r a tions after a bout of walking, standing quiescently
(i.e. w i t h t h e b o d y l o w t o t h e g r o u n d a n d t o t a l l y
motionless) and grooming an antenna. Stepping rates
u p t o 4/s o c c u r r e d s p o n t a n e o u s l y . F a s t e r s t e p p i n g
rates were evoked by lightly touching the head or
J.M. Camhi and T.G. Nolen: Escape System of Walking Cockroaches
341
Fig. 1A-C. Responses of the right
metathoracic leg of a slowly walking
A
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antennae. Stereotyped grooming, in which an antenna
is drawn through the mouth parts, was evoked by
placing a dropled of oil on the antenna. Quiescent
standing occurred spontaneously, most often late in
an experiment.
The latency of the behavioral response was shortest and least variable when puffs were presented during slow walking - that is, up to 4 steps/s (Figs. 1A ;
2 'high wind'). The mean latency during this slow
walking was 14 ms for these 2.6 m/s puffs, the largest
that we used (Fig. 2 - 'high wind'). This was much
shorter than previously reported latency measurements (54 ms, Roeder 1967; 58 ms, Camhi and Tom
1978) carried out on standing cockroaches, and is
similar to latencies of escape behaviors in crayfish
(approximately 12-22 ms; Krasne and Wine 1977)
and teleost fish ( < 10 ms; Kimmel and Powell 1978).
The responses studied here were active movements,
rather than a passive pushing of the leg by the wind,
since the response of a leg during the retraction phase
of a step was typically an accelerated retraction
(Fig. 1 A). This moved the leg into the wind. The
response was mediated by receptors on the cerci, since
covering the cerci with petroleum jelly obliterated all
responses to wind puffs, whereas covering other parts
of the body did not.
When puffs of only 25 mm/s were used (Fig. 2
- 'low wind'), the response to wind was even more
sharply ' t u n e d ' to slow walking. In fact, there were
few responses to wind puffs other than those delivered
,,
cockroach to wind puffs of different
velocities.
A Wind puff 2.6 m/s. Top trace, wind
recorded inside puff tube. Bottom two
traces, two photocells monitoring leg
movements. Approximately 300 ms of slow
walking is shown (top panel) before a wind
stimulus is delivered (bottom panel) which
elicits a run. Response latency was
determined as follows: At first arrow, wind
stimulus begins (downward deflection) and
goes off scale. Wind arrives at the cerci
within less than 1/2 ms of its arrival at the
point of measurement inside the tube
(Camhi, unpublished observation). At
second arrow, 12 ms after the first arrow,
the leg's ongoing stepping movement
accelerates, p protraction; r retraction.
B Wind puff of 3 ram/s, delivered during a
long series of steps, 4 of which are shown.
The puff is followed by a pause.
C Wind puff of 12 mm/s during a long
series of steps, three of which are shown.
The puff is followed by high frequency
stepping. In B and C only one photocell
trace is shown
during slow walking. The mean latency during siow
walking was still fairly short, 17 ms.
We next examined the threshold wind velocity for
slowly walking cockroaches. The smallest wind puff
which evoked any detectable change in ongoing walking movements on 50% of the trials had a mean
peak amplitude of 3 mm/s (n = 130, 11 animals). The
most c o m m o n response to these stimuli (90%) was
a pause in walking (Fig. 1 B); the rest were running
responses. Wind puffs having a peak amplitude of
12 mm/s were the smallest stimuli which consistently
(75%) evoked several cycles of rapid stepping, that
is, stepping faster than 10 cycles/s (n=130, 11 animals ; Fig. 1 C). These values confirm those from earlier preliminary measurements (Camhi et al. 1978).
Recordings from Giant Interneurons During Walking
In view of the enhanced behavioral responsiveness
to wind during slow walking, we next measured the
responses during walking of the ventral GI's since,
as mentioned in the Introduction, these cells are inhibited during walking (Daley and Delcomyn 1980a).
Three GI's l, four GI's 2, and one GI 3, were each
recorded during both slow walking and, for comparison, during standing 1 There were fewer action poten1 Unfortunately, it was not usually possible to record from the
GI's while observing behavioral responses to wind, since the
latter response waned quickly when we dissected the animal,
apparently as a result of influences at the GI-to-motor level
(Ritzmann and Carnhi 1978)
342
J.M. Camhi and T.G. Nolen: Escape System of Walking Cockroaches
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BEHAVIOR
Fig. 2. Behavioral latency of cockroach's response to wind, tested during different ongoing behaviors. Latency was measured as in
Fig. 1A. The running response to wind which was evoked while the animal was already stepping at high frequencies usually consisted
of an acceleration of the first few steps following the stimulus. Responses to high wind (puffs of 2.6 m/s): open circles. Responses
to low wind (puffs of 25 ram/s): filled circles. See text for definition of ongoing behaviors. N R no response. The two curves are
only approximations, drawn to show the trends. For both wind velocities, latencies during slow walking (1-4 steps/s) were less than
during either fast walking (4-20 steps/s) or during pauses (P < 0.01, Student's t-Test)
C/9
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Fig. 3. Number of action potentials evoked in identified GI's 1, 2 and 3 by wind puffs of different amplitudes. The puffs were delivered
either while the cockroach was standing (St) or while it was walking slowly, that is up to 4 steps/s (SW). Points represent means;
bars represent+ 1 standard deviation. Data from three GI's 1, four GI's 2, and one GI 3. Number beside each point number of trials
for that point
tials d u r i n g s l o w w a l k i n g (Fig. 3), as h a d p r e v i o u s l y
b e e n s h o w n ( D a l e y a n d D e l c o m y n 1980a). N e v e r t h e less, puffs o f a b o u t 12 m m / s (the b e h a v i o r a l t h r e s h o l d
for running) delivered from behind a slowly walking
c o c k r o a c h still e v o k e d a m e a n o f 0.33 a c t i o n p o t e n -
rials p e r trial for G I 1 a n d 1.65 a c t i o n p o t e n t i a l s per
trial for G I 2. T h e s a m e p u f f size d e l i v e r e d f r o m the
f r o n t e v o k e d a m e a n o f 0.33 a c t i o n p o t e n t i a l s for
G I 3, w h i c h d o e s n o t r e s p o n d to w i n d f r o m b e h i n d
( W e s t i n et al. 1977). G i v e n t h a t b o t h left a n d r i g h t
J.M. Camhi and T.G. Nolen: Escape System of Walking Cockroaches
343
14
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Fig. 4. Numbers of action potentials evoked
in ventral GI's by large wind puffs
presented while the cockroach was engaged
in different ongoing behaviors. Each
symbol represents the data from a different
cell. 9 and o, two different Gl's 1; ~,
GI 3; &, GI 4. The data shown for GI 4
are represented as one-half the actual
number of action potentials of this highly
responsive cell. Responses were severly
reduced during fast walking. For instance,
the difference between the number of
action potentials evoked while stepping
faster than 6 steps/s vs the number of
action potentials while stepping at 0-6
steps/s was highly significant (P< 0.001,
Student's t-test)
Ouiescent
BEHAVIOR
G I ' s 1 and 2 (but not G I 3) are excited by wind puffs
from behind the animal, there would be a mean of
approximately 4 action potentials in the two bilateral
sets of G I ' s l , 2 and 3 in response to a 1 2 m m / s
puff from behind the animal. The total mean number
of action potentials was reduced to about 1.5 for
puffs of 3 mm/s (the behavioral threshold for a pause
response). It is expected that at least these numbers
of action potentials would be evoked by these stimuli
in the G I ' s of intact, undissected animals. Thus the
ventral G I ' s can apparently at least contribute to the
just-threshold pause and running behavior evoked
during slow walking.
The dorsal G I ' s appear no more able than the
ventrals, and perhaps less so, to evoke these just
threshold behavioral responses. We made one recording each from a G I 5 and a G I 7 during slow walking,
and found that puffs of about 12 mm/s evoked means
of only 0.8 and 0.0 spikes respectively ( n = 5 and n = 4 ,
respectively). Thus these dorsal G I ' s appear to be
no more strongly activated than are the ventrals.
Moreover, the dorsal G I ' s are known to be activated
during walking, partly by corollary discharge from
the thoracic m o t o r centers (Daley and Delcomyn
1980a, b). Thus these dorsals have considerable ongoing activity against which very small wind-evoked
stimuli may be difficult to detect 2. By contrast, there
is almost no ongoing activity in the ventral G I ' s during slow walking since these G I ' s are slightly inhibited
at such times (Daley and Delcomyn 1980a).
In addition, recordings were made from two
2 In spite of the activity in the dorsal GI's during walking, the
interspike intervals are sufficiently long to have permitted the
counting of action potentials in response to puffs in the two
GI's from which we recorded. Only action potentials occurring
during the recorded wind stimulus were counted
G I ' s 1, one G I 3 and one GI 4 during stepping at
rates up to 12/s as well as during standing, quiescence,
and antennal grooming. The puffs were large - 2.6 m/s
for G I ' s 1 and 4 and 75 mm/s, posteriorly directed,
for G I 3. These large puffs evoked roughly the same
numbers of action potentials during all behaviors except fast walking when the responses were severely
reduced (Fig. 4). The reduction of the ventral G I responses during fast walking may contribute to the
elevation of threshold and the lengthening of the latency observed during fast walking (Fig. 2). However,
since there is little or no difference in the responses
of the ventral G I ' s to these large wind puffs during
slow walking, standing, quiescence, and antennal
grooming (Fig. 4), other factors must be responsible
for the decreased responsiveness during these behaviors as compared with slow walking.
Discussion
Selective Responsiveness During Slow Walking
One main finding of this paper is that the cockroach's
escape system is especially responsive to wind stimuli
that are presented while the insect is walking slowly.
We emphasize that this seems a suitable strategy, since
cockroaches would seem most likely to encounter predators while they are walking about slowly, and
would also be more visible to them than while standing still.
During locomotion, in several species of animal,
sensory inputs that mediate escape behavior are inhibited. For instance, the escape behavior of the crayfish
is evoked by mechanical stimulation of the body surface (Wine and Krasne 1972). During this escape behavior, corollary discharge from the giant interneu-
344
rons, which themselves mediate the behavior, gives
rise to presynaptic inhibition of the primary afferent
terminals of the mechanoreceptors. This is thought
to prevent re-excitation of the escape behavior which
might otherwise occur as a consequence of self-stimulation of mechanoreceptors (Kennedy et al. 1974).
In the cockroach, the responses of G I ' s 1-4 are
also reduced during locomotion (Fig. 3, 4; Daley and
Delcomyn 1980a). These are among the neurons that
appear to mediate the escape behavior (Westin et
al. 1977; Ritzmann and Camhi 1978; Ritzmann 1979,
and in preparation). However, in this paper we show
that this inhibition is strong only during rapid locomotion such as occurs during the escape behavior
itself. During slow walking, there is only slight inhibition and at least some of these G I ' s are still excited
by even the smallest wind puffs that evoke any detectable behavior. These outputs of the G I ' s may somehow be amplified more during slow walking than
during standing, quiescence, or grooming, thus accounting for the greater responsiveness during slow
walking than during these other behaviors.
Implications for Processing
of InJormation Encoded in the GI's
Although there is substantial evidence suggesting that
at least some of the 14 G I ' s participate in mediating
the cockroach's escape behavior (Westin et al. 1977;
Ritzmann and Camhi 1978; Ritzmann 1979, and in
preparation), it has been difficult to assign specific
functions to particular GI's. There are two groups
of GI's, the ventrals (left and right G I ' s 1-4) and
the dorsals (left and right G I ' s 5-7) which differ from
each other in numerous anatomical and physiological
properties (Daley and Delcomyn 1980a, b; Daley et
al., in press; Ritzmann 1977, and in preparation).
Many of the G I ' s of each group are selectively responsive to particular wind directions. In fact, each of
the two groups by itself encodes all the directional
information that would be required to specifiy the
direction of the cockroach's turn away from the
source of wind (Westin et al. 1977 ; Camhi and T o m
1978). Why, then does the cockroach need both
groups? The results of the present paper offer some
hints. As we shall now explain, these results suggest
that the ventral G I ' s 1, 2 and 3 (those G I ' s having
the greatest axonal diameter) may initiate the escape
response, at least during slow walking, and dorsal
G I ' s may mediate later phases of the escape behavior.
In crayfish it is well established that the largest diameter interneurons mediate the initial movements and
smaller interneurons the later phases of the escape
behavior, at least in response to sudden stimuli (Wine
and Krasne 1972; Schrameck 1970).
J.M. Camhi and T.G. Nolen: Escape System of Walking Cockroaches
Table 1. Time budget for the flow of neural information through
the escape circuit. Minimal values are presented, resulting in the
shortest reasonable total estimate of 8 ms
ms
Event
From:
Source
Onset of wind at cerci
2.5
Camhi (unpublished)
Arrival of 1st spike of
To:
GI 1, 2 or 3 at A5-6
From : connective
1.5
Spira et al. (1969)
To: ~ Arrival of 1st spike at
From: ~ Ta ganglion
1.0
(Minimal reasonable
estimate)
To: f Initiation of 1st motor
From: ~ neuronal spike at Ta
(Minimal reasonable
estimate)
1.5
To ;
From:
Arrival of 1st motor
neuronal spike at presynapatic neuromuscular
terminals
1.5
(Minimal reasonable
estimate)
To :
8.0
Onset of detectable leg
movement
Total
The suggestion that the ventral G I ' s may initiate
the escape behavior emerges partly from a consideration of the short behavioral latency in response to
large wind puffs presented during slow walking. The
minimal behavioral latency was 11 ms, and the mean
was 14 ms (Fig. 2). It is known that ventral G I ' s 1,
2 and 3 are the first to respond to such wind puffs,
and dorsal G I ' s 5, 6 and 7 are not activated until
approximately 5 ms later in both standing and walking cockroaches (Westin et al. 1977; Camhi, unpublished). As Table 1 shows, at least 8 ms are needed
for neural information to travel completely through
the escape circuit. This leaves only 1 1 - 8 = 3 ms for
a train of G I spikes prior to the first running movements in those trials that showed the shortest latency,
or 6 ms for the average trials. Thus owing to the
5 ms delay in activating the dorsal GI's, these cells
are all but ruled out of contributing to the initiation
of escape especially since several of their action potentials would probably be required to evoke running.
The responses of the G I ' s to very small wind puffs
are also consistent with the suggestion that the ventral
G I ' s initiate the escape behavior. For very small
puffs, below about 12 mm/s, GI 2 is several times
more responsive than either G I ' s 1 or 3 (Fig. 3). G I 2
is the only omnidirectional cell of this triad (Westin
et al. 1977). (GI 4, not tested, is also omnidirectional;
Westin et al. 1977). Therefore, there should be some
J.M. Camhi and T.G. Nolen: Escape System of Walking Cockroaches
F
J VENTRALL ~ ~ ~ J
3
5 MSEC DELAY
6
345
INITIAL TURNINGI
MOV'MNTi
5
~~7
,,JSUBSEQUENT TURNING
"1
AND RUNNING
low wind speed for which a puff can excite the cockroach by stimulating a left and right GI 2, but cannot
provide information about wind direction, since it
does not excite left or right GI's 1 and 3. Correspondingly, we have shown in this paper that the smallest
effective wind puffs evoke a non-directional response,
namely a pause in walking. Only larger puffs evoke
running. Running responses to puffs roughly in the
range of 12 mm/s delivered to freely-ranging cockroaches are appropriately directed away from the
stimulus (Camhi, unpublished). This correspondence
between the responses of the ventral GI's and the
behavior lends support to the initiating role of the
ventral GI's, especially since we record little or no
response in dorsal GI's for puffs of 12 mm/s.
The suggestion that the ventral GI's may initiate
the escape behavior appears at first inconsistent with
an earlier observation, namely, that motor outputs
to the legs were more readily evoked by stimulation
of individual dorsal than individual ventral GI's
(Ritzmann and Camhi 1978). However, more recently, simultaneous stimulation of pairs of the ventral
GI's has revealed summation in their effect on leg
motor outputs (Ritzmann 1979). Moreover, stimulation of ventral GI's inhibits the motor output of all
the dorsal GI's (Ritzmann 1979, and in preparation).
Since the ventrals are activated by wind 5 ms before
the dorsals, the inhibition of the dorsals may prevent
these cells from expressing their output during the
early phase of the behavior.
Based upon the suggested sequential action of the
ventral and then the dorsal GI's, We present the flow
diagram of Fig. 5. This diagram, we feel, makes sense
out of a large number of excitatory and inhibitory
interactions involving the GI's that have been demonstrated but for which there previously was no clear
function. In this flow diagram, activity is initiated
by wind which results in action potentials first in
the ventral GI's (path 1 on the diagram). It is suggested, in accordance with the arguments presented
above, that these ventral GI's initiate the turn away
from the wind source (path 2). The ventral GI's also
inhibit the outputs of the dorsal GI's (path 3; Ritz-
Fig. 5. Tentative flow diagram of the
activation of escape behavior by the dorsal
and ventral GI's. The two circles, one
following the ventral GI's (on path 2) and
the other following the dorsal GI's (on
path 7) represent thoracic GI-to-motor
centers. All interactions shown have been
demonstrated. The model reveals that the
two sets of GI's may work sequentially;
first the ventrals would initiate the oriented
escape response, then the dorsals would
continue to drive the turn during running
mann 1979). When the rapid escape movements begin,
negative feedback inhibits the ventral GI's (path 4;
Daley and Delcomyn 1980a). This would result in
disinhibition of the dorsal GI outputs (path 3). Since
the outputs of the dorsal GI's are now disinhibited,
and are also being activated by positive feedback from
the escape movement itself (path 5 ; Daley and Delcomyn 1980a), and are now being activated by wind
(path 6), these dorsal GI's would begin to dominate
the control of the behavior (path 7). Since the turning
component of escape behavior can last for up to
180 ms (Camhi and Tom 1978), this subsequent phase
of the behavior, controlled largely by the dorsal GI's,
would include turning as well as running.
The suggested sequence of activation of ventral
and then dorsal GI's may be an adaptation for effectively encoding the wind stimulus under the changing
sensory conditions that occur during an escape behavior. A special property of the ventral GI's is their
ability to detect very rapidly the onset of tiny wind
puffs. The moment substantial noise enters the system
as a result of the cockroach's rapid escape movements, this ventral GI system would be inappropriately excited and thus is apparently turned off. Consequently, the sample time of this ventral system is
very brief, as little as a few ms in some instances.
Thus additional information might be needed in order
to permit a reasonably accurate final direction of running. This information would be provided by the second, dorsal GI system which, rather than being inhibited, is excited during rapid running (Daley and Delcomyn 1980a, b). It is possible that a particular advantage of the early inhibition of the ventral GI's
during the escape behavior is the protection from
habituation of the ventral GI-to-motor pathway,
thereby retaining the sensitivity of this pathway for
subsequent stimuli. Such protection from habituation
has been found in the crayfish escape system, where
the primary afferent terminals are subjected to presynaptic inhibition during the escape behavior (Kennedy
et al. 1974; Wine et al. 1975). The dorsal GI-to-motor
pathway of the cockroach appears to habituate less
quickly than the ventral (Ritzmann and Camhi 1978).
346
We thank R. Ritzmann, C. Comer, D. Daley, N. Vardi and S.
Volman for reading the manuscript and S. Volman for technical
assistance. This work was supported by NIH grant No. NS09083.
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