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First published online January 31, 2007
Journal of Experimental Biology 210, 561-569 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02697
Orienting and avoidance turning are precisely computed by the predatory sea-slug Pleurobranchaea californica McFarland
1 Program in Biophysics and Computational Biology, University of Illinois at
Urbana-Champaign, University of Illinois, Urbana, IL 61801, USA
2 Department of Molecular and Integrative Physiology, University of Illinois
at Urbana-Champaign, University of Illinois, Urbana, IL 61801, USA
3 The Neuroscience Program, University of Illinois at Urbana-Champaign,
University of Illinois, Urbana, IL 61801, USA
* Author for correspondence (e-mail: rhanor{at}uiuc.edu)
Accepted 13 December 2006
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Summary |
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Key words: trailing, orienting, odor tracking, decision
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Introduction |
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;
Mpitsos and Collins, 1975;
Gillette et al., 2000). Diverse
studies have elucidated the computations for directional behavior in
arthropods and fish (Murphey,
1971; Levi and Camhi,
2000; Zeil et al.,
1985; Eaton and Emberly,
1991), but few have similarly examined elements of foraging
behavior in molluscs (but see Teyke et
al., 1990). Further, to our knowledge none have quantitatively
studied the interactions of sensation and internal state for which these model
systems are most useful.
We used the predatory sea-slug Pleurobranchaea californica to
study the relationships between stimulus location, stimulus amplitude and
modality, and internal state on orienting and avoidance turns.
Pleurobranchaea is an opportunistic predator on numerous
invertebrates, including conspecifics
(Davis and Mpitsos, 1971),
whose abilities to track appetitive chemotactile stimuli and to recognize and
avoid potentially dangerous stimuli must be most critical to the animal's
eventual reproductive success. This species generally inhabits deeper waters
(20 to >1000 m) characterized by constant and changing currents. Without
external eyes and imaging vision, the animals depend largely on chemotactile
cues in their environmental interactions.
Foraging gastropods are well-documented for their abilities to orient to
and follow odor trails of potential prey and mates
(Hall, 1973;
Tyndale et al., 1994;
Townsend, 1974;
Clifford et al., 2003;
Wyeth and Willows, 2006) or to
avoid those of potential predators (Wyeth
and Willows, 2006). However, to date few studies have elucidated
the behavioral elements of orienting or avoidance or of their neural bases.
For Pleurobranchaea, previous work outlined a neural network of
identified neurons that mediates avoidance turning stimulated by unilateral
electrical shocks to the oral veil (Jing
and Gillette, 2003). This neural network, composed of bilaterally
homologous pairs of neurons, was hypothesized also to mediate orienting turns
if active in an inverted configuration. We have extended behavioral
observations on turning to further define the constraints that must attend the
neural network structure and function, through assessing the causative factors
that determine the turn response in terms of direction and angle.
Escape turns induced by strongly noxious electric shocks to
Pleurobranchaea's oral veil have been studied
(Jing and Gillette, 2003). Such
turns were characterized by their vigor, large and unpredictable amplitudes,
and similarity to classic fixed action patterns. However, our informal
observations suggested that most turns in the actively exploring animal are of
smaller amplitudes and might serve either in locating appetitive stimuli or in
avoidance of non-appetitive stimuli
(http://www.life.uiuc.edu/slugcity/movies.html).
Thus, in the present study, we tested the effects of appetitive and only
moderately aversive chemotactile stimuli. We adapted procedures for
quantitatively relating stimulus site to turn response in other species
(Murphey, 1971;
Zeil et al., 1985;
Teyke et al., 1990;
Levi and Camhi, 2000) for use
with Pleurobranchaea. Our findings indicate that the angle of the
turn response to a punctate chemotactile stimulus applied to the animal's oral
veil is precisely computed on the basis of stimulus site and strength, while
the turn direction is a function of both stimulus modality and satiation
state. These results seem to speak to chemotaxic tracking and avoidance
strategies, and they suggest neural circuit hypotheses for future
investigation.
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Materials and methods |
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;
Gillette et al., 2000).
Ascending tenfold dilutions of betaine (trimethylglycine) from
10–6 to 10–1 mol l–1 were
applied to the oral veil with a pasteur pipette in 1.5 ml volumes over a
period of 10 s. Those dilutions at which proboscis extension and biting
responses occurred were recorded as feeding thresholds. Betaine is the single
most potent feeding stimulant, and an abundant osmolyte of
Pleurobranchaea's invertebrate prey
(Gillette et al., 2000). Animal
sizes, determined by seawater displacement, ranged from 8 to 400 ml. An animal
was considered quite ready-to-feed if its betaine threshold for biting was
less than or equal to 10–3 mol l–1, values
at which animals tend to ignore mildly noxious stimuli to attack food stimuli
(Gillette et al., 2000). Gelatin cubes of 3–5 mm on a side were used for chemotactile stimulation. The cubes were cut from a shallow tray of unflavored gelatin powder (Knox; Kraft Foods, Northfield, IL, USA) dissolved as 1 g per 30 ml of artificial seawater with a few drops of red food color (Red #40; Supplier, Meijer Inc., Grand Rapids, MI, USA) added to improve visibility for video data analysis. In the gelatin we also dissolved appetitive (betaine) or noxious (taurine) chemical stimuli in varying concentrations. The cubes were impaled on the tips of Pasteur pipettes, leaving no sharp glass edges exposed, for application to the chemosensory oral veil (Fig. 1).
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). The seawater arenas used were large enough to permit several complete unrestrained turns and had no active water flow. Animals were positioned at one end of the arena at the beginning of trials. When an animal began to locomote straight forward, a gelatin pellet was brought in front into the water parallel with the locomotion path, taking care not to introduce ripples and currents. The stimulus was moved toward the animal, positioned within a body length in the animal's path so as to contact a desired locus on the oral veil, and held there, stationary, until contact. Only responses of animals that locomoted straight forward to touch the pellet were included in the analysis. Stimulus application to quiescent animals rarely elicited a response. In those few cases where quiescent animals actively responded, responses were not robust and those trials were not included, nor were rare occasions when an animal turned toward the stimulus before touching it. Stimulus application to actively turning animals was avoided.
When animals touched the pellet with their oral veil, it was held there for 1–2 s and then removed. The pellet was moved slowly with the animal as it locomoted forward so as not to cause appreciable distortion of the oral veil. This light, transient contact allowed clear estimation of the stimulus position on the oral veil and also prevented animals from biting the pellet. At times animals with marked readiness to feed (10–7 mol l–1–10–5 mol l–1 betaine biting threshold) oriented to the gelatin pellet as it was brought near, thus performing an orienting turn to a stimulus not yet defined by our criteria. In other cases animals succeeded in biting the gelatin pellet and such trials were excluded from the data analysis. After stimulus removal the animal was allowed to locomote until it encountered a wall or made more than three sequential turns, and was then repositioned for the next application several minutes later. Animals on average yielded 10–12 raw data points before they ceased to respond.
For stimulation and data analysis, the oral veil was divided into nine regions of roughly equal width, which denoted the position of the stimulus (Fig. 1). Thus, for the nine regions the left tentacle at the extreme edge of the oral veil corresponded to stimulus position x=–4, the midline x=0, and the right tentacle x=+4. Those regions could be estimated fairly well during stimulus application, and exact stimulus positions were determined during the video analysis. Responses were recorded on a Sony camcorder. Videos were digitized with a Dazzle multimedia adapter for PC and stored on computer in mpeg format (examples can be seen at http://www.life.uiuc.edu/slugcity/movies.html). Using those mpeg files for stop-frame video analysis, we traced the locomotion paths of animals by marking the position of both tentacles approximately every 2–5 s on a transparency overlain on a computer monitor. As animals locomoted at 5–10 mm s–1 and turns could take more than 1 min to complete for larger animals, 12–30 data points were adequate to measure the turns, varying with animal size. Responses for oral veil regions were averaged within and across animals for the turn response plots of Fig. 2.
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The locomotion traces described above were used to measure the angles of turn responses induced by stimuli. Turns were measured using a protractor with a precision of 0.5°. Completion of turns was marked either by initiation of an oppositely directed turn or by straight and forward locomotion. The angle of turn was defined as the angle between the midline of the animal at the moment of stimulus application and the midline at the end of the turn. If an animal performed only one turn in response to the stimulus, the final orientation of the midline was measured when it became clear that the animal was locomoting straight forward. If a series of turns was performed, the end of each turn was marked clearly by the change of the oral veil orientation, facilitating measurements (Fig. 4).
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Statistical analyses employed unpaired two-tailed Student t-tests for statistical comparisons of slopes computed by means of linear regression. Linear regression was performed with least-squares algorithm, using an acceptable level of significance of P<0.05. Fisher's exact test was used to determine relationship between readiness-to-feed and prevailing nature of turn responses (orienting or avoidance).
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(Fig. 2A; correlation
coefficient r=0.99, N=9, P<0.001):
 |
To determine the possible effect of chemical stimulus strength, we used a range of betaine concentrations, from 10–7 mol l–1 to 10–1 mol l–1. A linear relationship between the angle of turn and the site of stimulus application existed at all concentrations (Table 1). In addition, there was a linear correlation between the slope a and the concentration of the feeding stimulant (correlation coefficient r=0.91, N=5, P=0.0326). As concentration of the stimulus increased, the slope a also increased (Fig. 2B), reflecting that animals performed turns of greater amplitude at higher stimulus strengths. The average value of the relation's intercept b was very close to zero (b=–0.36±0.82, significance level 95%), indicating that animals tended to continue locomoting straight when the stimulus was applied to the midline.
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Pleurobranchaea overshoot during orienting turn
In these experiments chemotactile stimuli were applied to the oral veil to
simulate direct contact with prey. We initially expected
Pleurobranchaea to perform an orienting turn that would approximately
center the stimulus on the oral veil, such that the connection between
stimulus locus and subsequent turn angle would follow a simple relationship
where angle=arctan (xk/4), where k is the ratio of
the oral veil width to the body length L as shown in
Fig. 3A. However, the results
unexpectedly revealed that animals overshot by approximately fourfold
(Fig. 3B).
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Two appetitive stimuli applied simultaneously at different loci constitute a distributed stimulus, which from the animal's perspective is a minimum estimate of the size of the object causing the stimulus. This posed a question: do Pleurobranchaea average their response to the two sites of stimulation, as if they were turning toward the center of the object? If so, then the slope of the relationship for 2-point applications should be one-half of the value for single point applications, a2=a/2. Indeed, we found the difference between a2 and a/2 was not significant (Table 3) for both unilateral (P=0.1723, N=17, unpaired two-tailed t-test) and bilateral applications (P=0.6056, N=16, unpaired two-tailed t-test).
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Sequential turn angles are correlated
In unilateral 2-point applications, we observed that 8 of 18 animals
performed 2–5 sequential turns before their paths straightened or they
ceased locomoting (Fig. 4). A
sequence of three turns was most frequently observed, on average in 2 of 10
stimulus applications for each animal that performed multiple turns.
Fig. 5 summarizes our analysis
of those cases, in which data from all animals are combined into a single
dataset. Correlation analysis of 17 cases showed that the angle of the third
turn was highly correlated with and was not significantly different from the
angle of the first turn (correlation coefficient r=0.84), whereas the
second angle and first angle were not correlated (correlation coefficient
r=0.08).
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Appetitive state affects turn direction
We found that a fraction of animals avoided the feeding stimulant betaine,
instead of orienting to it. This suggested that the animals' readiness to feed
was affecting the direction of the turn. We combined data from multiple trials
on all tested animals and related feeding thresholds to turn direction. We
found that animals with biting thresholds for betaine lower than
10–3 mol l–1 were indeed significantly more
likely to orient to betaine than the animals with higher thresholds
(Table 2). The frequencies of
orienting and avoidance turns strongly correlated with readiness to feed
(Fisher's exact test; P<0.001).
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Avoidance turns
Avoidance turns were reliably elicited by applying gelatin pellets infused
with taurine, a stimulus noxious to Pleurobranchaea
(Gillette et al., 1991). The
transient and focal nature of the stimuli used here, unlike for previous
observations where taurine solutions were pipetted onto the oral veil, did not
result in full escape turns where animals stopped locomoting to make a large
turn, but simply caused a smooth change in movement similar, but oppositely
directed, to orienting. In addition, we analyzed those incidents where
avoidance, instead of orienting, turns were caused by betaine pellet
applications.
Avoidance turns showed a relationship to the stimulus locus similar to orienting turns. The slope was linear (Fig. 2A, Table 1), and the differences between the slopes for orienting and avoidance in case of single- and double-point applications were not statistically significant in either treatment, except for sign relationship. From the data in Table 3, it may be seen that the slopes of the relations for 10–2 mol l–1 taurine avoidance were not significantly different from those for avoidance of 10–2 mol l–1 betaine (P=0.3716, two-tailed t-test), nor was the difference between slopes for orienting and avoidance of 2-point unilateral betaine application (P=0.2569; two-tailed t-test). Moreover, for unilateral 2-point applications, animals averaged their avoidance responses to 10–2 mol l–1 taurine much as they did in orienting to 10–2 mol l–1 betaine. The difference between a2 and a/2 was not significant (P=0.6600, two-tailed t-test).
A consequence of the similar, but oppositely signed, turn angle/stimulus
locus relation for both orienting and avoidance was that the transient, mildly
noxious stimulus to the very midline of the oral veil caused no turn. Adaptive
significance of this non-response in the absence of directional stimulus
information is suggested from observations where such stimuli were maintained:
either the animal stopped and initiated an escape avoidance turn
(Gillette et al., 1991) or the
animal initiated a normal closed-loop turn.
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Search strategies
The four initial findings of this study seem to illuminate the foraging
animal's search strategy and provide clues to the possible structure of the
underlying computational neural circuitry. First, Pleurobranchaea
calculated the angles of its orienting as linear functions of the site of
application of transient appetitive stimuli across the oral veil. However, we
next found that orienting turns tended to markedly overshoot the target
stimulus site, and that overshoot increased with stimulus strength. Finally,
the angle of the turn was averaged when two stimuli at different loci were
presented to the oral veil simultaneously.
These first three findings resemble those of an earlier study on
Aplysia (Teyke et al.,
1990). The commonalities emerge despite the marked differences in
the foraging strategies of the two animals, in the anatomy of the head
chemosensory region, and in the ways in which the experiments were conducted.
Pleurobranchaea is a predatory opportunist whose oral veil presents a
fairly horizontal shelf overlying the mouth. Stimuli were applied to active
animals locomoting on the substrate; non-locomoting animals did not perform
well in turns. In contrast, Aplysia is an herbivore whose mouth lies
between the frond-like tentacles, the oral veil homo/analogs, and which
commonly feeds on leafy red and green algae. Stimuli were presented to
Aplysia while non-locomoting, attached by the posterior foot to a
vertical aquarium glass with the ventral surface of the anterior head region
at the water surface. The strong similarities suggest that orienting turn
mechanisms could be conserved broadly across molluscan species, and that in
both cases the similar computations optimize search strategies of animals
distinctly differing in form and habit.
Linear relationships for directional turn angles versus stimulus
location have resulted from investigations in a variety of arthropods,
including the water strider Gerris remegis
(Murphey, 1971), water boatman
Notonecta sp. (Murphey,
1973), cockroach Periplaneta americana
(Levi and Camhi, 2000) and
crayfish Cherax destructor (Zeil
et al., 1985). For terrestrial arthropods in particular, turns are
mediated by combinations of leg movements, the joint angles of which determine
the direction and amplitude of the turn movement
(Levi and Camhi, 2000;
Mu and Ritzmann, 2005). A
similar linear relation is also found for the earliest movement component of
the fish escape response (Eaton and Emberley, 1991). In each of these cases
the anatomy underlying the turns is very much more complex than for the
soft-bodied sea-slug Pleurobranchaea, in which turns are simply
mediated by musculature that shortens one side of the body relative to the
other (Jing and Gillette,
2003). However, Murphey pointed out
(Murphey, 1973) that a quite
simple neural computation based on lateral inhibition among the sensory
pathways could produce the linear relation; the simplicity would lend it
useful for the core computations observed in both simple and complex animals.
The commonality across species of the linearity of the turn/stimulus relation
is notable. It suggests that the relation is particularly advantageous to both
the goals of directional orienting and avoidance, and/or that its simplicity
lends itself to use in more complex computations; for instance in the
integration of other sensory information like vision into the movement
(Ye et al., 2003), or adding a
third movement dimension, or incorporating temporal modifications to
directional movement.
The further finding, that Pleurobranchaea precisely computes the average of two stimuli presented to separate loci and then swings to the intermediate angle, could supply the animal with the ability to strike at the center of an appetitive stimulus. However, the tendency to overshoot the appetitive turn past the stimulus site might appear to reduce the utility of the computational precision. Is this really the case?
In view of the precision of the turn response, the inaccuracy introduced by
the overshoot, itself also precise, must confer some advantage. The nature of
that advantage may be sought in consideration of the conditions when the
open-loop search most often occurs. Our informal observations in our marine
system indicate that Pleurobranchaea resembles many other aquatic
molluscan foragers in its abilities to accurately navigate upstream to the
source of appetitive odor plumes in currents as well as to follow slime trails
of potential prey (often smaller Pleurobranchaea specimens) (cf.
Hall, 1973;
Townsend, 1974).
Pleurobranchaea resembles Tritonia diomedia in general body
form, habitat choice and odor tracking abilities, for which odor tracking has
been documented most elegantly in the wild
(Wyeth and Willows, 2006). The
oral veil, sited closer to the less-stirred aqueous layer next the substrate,
is used during locomotion to repeatedly sample the substrate (an example for
Pleurobranchaea may be seen at
www.life.uiuc.edu/slugcity/movies.html).
In slime trail following, the overshooting turn can bring larger portions of
the oral veil into the trail stimulus area and thereby enhance the computation
of a subsequent turn toward the source. The overshoot caused by lateral
stimulation of the oral veil should bring in corrective turn action by
involving more medial or opposite side stimulation. Moreover, if the trail
should abruptly turn laterally then the overshooting turn to the same side
would enhance tracking.
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The positive effect of stimulus intensity, where stronger appetitive stimuli cause larger overshooting turns, may be interpreted in a similar fashion by taking into account the animal's ability to average stimuli along the oral veil. Of multiple simultaneous stimuli, such as might be provided by substrate trail or odor plume, those sites with stronger stimulation would bias the turn amplitude to bring a larger surface of the oral veil into contact with stimuli for the next turn computation.
It remains to deal with one of the most interesting observations of this study: apparent working memory in tracking. Following single-point appetitive stimulation, animals often made sequential turns. The first turn, when unrewarded with a new stimulus, was succeeded by a second turn in the opposite direction whose own angle was random with respect to the first. However, the third turn was back to the original direction and repeated the angle of the first. This observation leads to inference of a persistent memory of the first turn angle calculation, its retrieval, and the associated problem of how this could be encoded in the neural circuitry.
The significance of the sequential turn computations seems most immediately
accessible in terms of efficient search strategy. In the process of following
an odor trail, if a lateral stimulus suggests a lateral movement of the trail
but further stimulation is not encountered upon a turn in that direction, it
would most reasonably imply that the stimulus source itself moved again to
either right or left. A choice to continue the original turn path would
diminish the opportunity to sample the other direction. The second brief turn
in the other direction would accomplish a quick check and, if negative, the
original direction could be pursued with the increased likelihood that it was
appropriate. These maneuvers resemble the `casting flight' of moths following
a pheromone odor plume, in which, after losing an odor during flight, they may
fly in broad swings back and forth across the wind
(Willis and Arbas, 1991).
Thus, this form of working memory in odor tracking could markedly enhance
tracking efficiency.
Behavioral choice of orienting and avoidance
Pleurobranchaea switches behaviorally from orienting to avoidance
responses to appetitive stimuli when trained in a food-avoidance paradigm
using paired food and shock (Mpitsos and
Collins, 1975), or when satiated
(Gillette et al., 2000). We did
not distinguish between learning and satiated state here, but simply observed
that orienting and avoidance were associated with readiness-to-feed, as
assessed by measures of the animals' feeding thresholds. The findings that the
choice to express orienting or avoidance turns correlated with low or high
feeding thresholds, respectively, resembles previous observations on hungry
and satiated animals (Gillette et al.,
2000). However, in the present context the results seem to speak
directly to the nature and control of a neural switch that may regulate the
asymmetry of activity in the premotor turning network.
Avoidance turns induced either by normally appetitive or by noxious stimuli applied to the oral veil followed the same computational rule for turn angle vs stimulus site as did orienting turns, save that the direction was opposite. These observations are consistent with a marked economy of neural circuitry in an animal with a small nervous system, where degree of turning for opposite actions is probably calculated in the same neural network, and the direction of the turn is then based on an estimation of the stimulus value – positive or negative, as decided through the animal's integration of stimulus nature, its internal state and learning experience. The savings in network maintenance by use of a simple circuit for both orienting and avoidance might be justified by a low average cost of potential behavioral errors.
A framework for chemotactile sensory integration and decision
The observations presented above suggest the outline of an integrated
neural model for odor tracking/avoidance in Pleurobranchaea. The
schematic of Fig. 6 portrays
the initial integration of afferent inputs from the oral veil in an
interneuronal layer, whose function would be to encode and average amplitude
and laterality of chemotactile input. The turn motor network in
Pleurobranchaea is a bilaterally symmetrical circuit whose
lateralized activity determines turn direction
(Jing and Gillette, 2003).
Thus, translation of the output of the interneuronal layer into an orienting
or avoidance turn requires an intervening switch mechanism regulated by the
animal's appetitive state. The switch would act to invert the laterality of
the output to the turn motor network.
Conclusion
We documented seven simple parameters of turning behavior in
Pleurobranchaea: (1) linearity of the relation of turn angle to
stimulus site on the oral veil; (2) increase of turn amplitude with stimulus
strength; (3) overshoot of turn angle past target; (4) averaging of stimulus
loci in the response; (5) memory and retrieval in sequential turns; (6)
influence of appetitive state on turn direction; and (7) similarity between
avoidance and orienting turn computations, differing only in direction.
Collectively these seem to compose a behavioral strategy for efficiently
tracking an odor trail. Tracking is regulated by a decision-making process
capable of integrating sensation, internal state and experience in toggling
between orienting and avoidance turns. Future work should be aimed at
computational testing of a general model incorporating the above seven
parameters, and at elucidating their bases in biological neural networks.
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Acknowledgments |
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