Integration of hydrodynamic and odorant inputs by local interneurons of the crayfish deutocerebrum
Department of Biology, 286 Gilmer Hall, University of Virginia, Charlottesville, VA 22903, USA
e-mail: dm6d{at}virginia.edu
Accepted 8 August 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: olfaction, glomerulus, olfactory lobe, antennule, crustacean, sensilla, Procambarus clarkii
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Little is understood concerning the details of interactions between neural
inputs from sensory receptors mediating coincident mechanical and chemical
sources of peripheral excitation within the central nervous systems of aquatic
animals. In crustacean chemoreception models, competing hypotheses have been
advanced to account for the putative integration of chemical and hydrodynamic
information in odorant-source tracking, variously implicating advection,
eddies or edge effects in navigation of an animal toward odor sources (Moore
et al., 1991; Basil and Atema,
1994; Weissburg and
Zimmer-Faust, 1994
; Atema,
1996
; Guenther et al.,
1996
; Webster and Weissburg,
2001
).
Crabs, lobsters and crayfishes all detect odorants using their antennules,
which exhibit batteries of chemoreceptive sensilla. The lateral antennular
flagella, in particular, possess aesthetascs and associated olfactory sensory
neurons (ORNs) that are sensitive to amino acids and other dissolved organic
molecules (Ache, 1972;
Ache and Derby, 1985
;
Schmiedel-Jakob et al., 1989
;
Mellon and Alones, 1995
;
Mellon, 1996
,
1997
; Schmidt and Ache,
1996a
,b
),
but they also possess mechanoreceptive setae
(Schmidt et al., 1992
;
Schmidt and Ache, 1996a
;
Mellon, 1997
; Cate and Derby,
2001
,
2002
). The extent to which
hydrodynamic factors participate in or influence odorant detection, however,
has remained poorly understood (reviewed in
Atema, 1996
;
Grasso and Basil, 2002
).
Moreover, crustaceans routinely flick the lateral antennular flagella in the
presence of odors and water movements
(Reeder and Ache, 1980
;
Daniel and Derby, 1991
;
Mellon, 1997
). Flicking
transiently enhances the response of ORNs to odors, although the mechanism
responsible remains unclear (Schmitt and
Ache, 1979
; Koehl et al.,
2002
). There can be little doubt, however, that the act of
flicking should itself generate hydrodynamic stimulation of the antennular
sensilla.
Previous electrophysiological studies of olfactory interneurons in the
crayfish brain from my laboratory did not consider effects of hydrodynamic
stimulation of the antennules during responses to odorants, since a
continuous, regulated flow of freshwater bathed the immobilized antennular
flagella during the course of an experiment
(Mellon and Alones, 1995;
Mellon, 1996
). Similar
electrophysiological studies of neurons in the olfactory midbrain of the spiny
lobster Panulirus argus, using a different stimulus regimen, did
provide evidence for transient effects of rapidly introducing seawater past
the antennule but they were not followed up in any detail
(Schmidt and Ache, 1996b
).
The present study was undertaken to re-evaluate the responses of local deutocerebral neurons to olfactory and hydrodynamic stimulation of the lateral antennular flagellum and to determine the interactive effects of these dual sources of sensory input. I used multiple stimulus routines in which different schedules of freshwater and odorant were flushed past the lateral antennular flagellum. The results indicate that at least two major classes of the local interneurons that have dendritic arborizations within the olfactory lobe (OL) receive input from mechanoreceptors as well as chemoreceptors on the lateral flagellum of the antennule and that interactions between chemosensory and mechanosensory inputs together determine the output dynamics of these neurons. Mechanosensory input potentiates the responses to odorants in some neurons and thus may serve to amplify weak chemical signals. Furthermore, the integration of olfactory and hydrodynamic information at this early stage in the central olfactory pathways supports theoretical views that cooperation between these two major sensory inputs is critical for accurate determination of odor sources by aquatic animals.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
For electrical recordings, crayfish were quickly decapitated using sharp scissors to cut through the cuticle just posterior to the cervical groove on the cephalothorax, transecting the stomach and circumesophageal neural connectives. The rostrum was removed, and the head capsule was rinsed in chilled crayfish saline (see below) and mounted dorsal side up in a recording chamber that separately accommodated the medial and lateral flagella of the right-hand antennule within an olfactometer, as described below. The median artery, which supplies the brain, and the right lateral cephalic artery, supplying both the brain and ipsilateral antennular sense organs, were then quickly cannulated with small glass pipettes and flushed continuously at 2 ml min-1 with chilled (15°C), oxygenated saline having the following composition (in mmol l-1): NaCl, 205; KCl, 5.4; CaCl2.2H2O, 13.6; MgCl2.7H2O, 2.7; NaHCO3, 2.4. The pH of the saline was adjusted to 7.4 with HCl.
The loose membrane lying over the dorsal aspect of the brain was removed
with microscissors, and the perineural sheath applied to the accessory lobe
and OL on the right side of the brain was torn using sharpened watchmaker's
forceps. Loose glial cells and hemolymph were gently washed away using a
saline-filled tuberculin syringe. This procedure exposed both the dorsal
surface of the OL and cell cluster 11 to approach with microelectrodes. Sharp
microelectrodes were pulled on a Brown-Flaming puller and were filled with 2
mol l-1 KCl or, when staining with neurobiotin, 1 mol
l-1 KCl. The resistance of the electrodes measured in crayfish
saline was consistently in the range of 50-200 M.
The isolated crayfish head preparation and details of the fluid supply to the olfactometers are shown in Fig. 1. Fig. 1A shows a simplified diagram of the recording and stimulating situation using the isolated head preparation. Antennular flagella were inserted within the parallel tubes of an olfactometer, through which either water or odorant flowed in a controlled regimen. The olfactometers were two parallel polyethylene T-connectors, the cross-members of which penetrated one wall of the lucite recording chamber, with the stems of the Ts, through which both freshwater and odorant were introduced, pointing upwards. The antennular flagella were inserted into the cross-members of the Ts, with their distal ends extending well beyond the intersection with the influx stems. The bases of cross-members around the flagella were then sealed with Vaseline to prevent odorant and water from entering the recording chamber or saline from flowing past the flagella. The other end of the cross-member tubes constituted an exhaust for the water and odorant once they had flowed past the antennule. Fig. 1B shows the switching arrangement controlling the flow of water and odorants through the olfactometer. Water and odorant could be flushed through either of the olfactometers separately or in concert by means of the electrically controlled switches. The data in the present paper are confined to responses from OL interneurons following stimulation of the lateral flagellum alone. The standard stimulus paradigm was to switch on a 10-s water flow, which triggered the computer acquisition file, followed after a variable delay by interruption of the water by a 1-2 s odor pulse. Water and odorant flowed through the olfactometers under gravitational acceleration at 18 ml min-1. The common feed from the switch to the antennule in the olfactometer constituted a `dead space' volume of 0.016 ml, which was cleared in approximately 50 ms at the initiation of each stimulus. Normally, water onset constituted a much more vigorous hydrodynamic stimulus than the injection of odorant, which was nearly seamless when the respective flow rates were appropriately adjusted. A broad spectrum odorant was made up fresh for each experiment from 5 ml frozen aliquots of a 1% (w/v) tetramin solution, which were each dissolved in 95 ml of dechlorinated tap water. In some, but not most, preparations, morphological identification of interneuron types was pursued by injecting neurons with a 2% neurobiotin solution in 1 mol l-1 KCl. Crayfish heads were fixed overnight at 4°C in 4% paraformaldehyde made up in 0.15 mol l-1 Hepes buffered saline, pH adjusted to 8.2. Fixed, desheathed brains were then incubated at 4°C for 2 days with slow agitation in a solution of Hepes buffered saline, 0.5% Triton X-100 and 25 µg ml-1 Texas Red avidin D (Vector Laboratories, Burlingame, CA, USA). Brains were dehydrated, cleared in methyl salicylate and examined with an epiflourescence binocular dissecting microscope or, in some cases, with a laser scanning confocal microscope.
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Dual response properties of Type I neurons
Cells resembling Type I cells (Mellon
and Alones, 1995; Mellon,
1996
) in their excitatory physiological responses to odorant
stimulation and, in four cases, in their morphology, were most frequently
encountered by recording electrodes, especially when penetrations were made at
a depth of 300-400 µm within the central region of the OL. Tests were
started following stabilization of the resting potential, which was usually
between -55 and -65 mV. The current paper is based upon observations of 21
Type I-like neurons, obtained over a six month period. Although at least five
additional types of neurons extend dendrites or axon terminals within the OL,
Type I cells have the largest processes (up to 15 µm in diameter) and
presumably are the largest targets within this neuropil. As shown in Figs
2,
3,
4,
5, which are typical, these
cells were excited by tetramin in a dose-dependent manner when it was injected
seamlessly into the olfactometer during a long pulse of freshwater. Moreover,
in both these and other Type I-like cells, the neurons responded not only to
the odorant pulses but to the onset of water flow past the antennules as well.
Fig. 2 shows responses of a
Type I cell to both the leading edge of the water pulse and to different pulse
durations of standard (0.05%) tetramin odorant embedded in a 10-s pulse of
water. Very short odor pulses experienced more dilution by the ensuing tail of
the interrupted water pulse and were thus less effective at stimulating the
ORNs (Mellon and Alones,
1995
). Fig. 3 shows
responses of a different Type I neuron to 2-s pulses of standard tetramin and
of three successive 10-fold dilutions of the standard. The responses of the
cell, in terms of number of spikes, were a linear function of the
log10 of different tetramin concentrations over the range tested.
This cell was more typical than the one shown in
Fig. 2 in that the response to
the onset of water consisted of a sequence of
depolarization-hyperpolarization-depolarization (E-I-E), with the initial
depolarization usually generating one or two spikes.
Fig. 4 records responses from
another Type I neuron to illustrate the non-stimulatory nature of the injected
fluid pulse from the odorant reservoir.
Fig. 4A shows combined
responses to water and standard odorant, whereas
Fig. 4B shows the lack of
response one minute later when the odorant reservoir was switched to
freshwater. The responses to hydrodynamic stimuli in Type I-like neurons were
more temporally labile than those to odorants in Type I neurons. A sequence of
standard stimulus paradigms was presented to the cell shown in
Fig. 3, alternately separated
by 60 s and 120 s rest intervals. As shown in
Table 1, the spike responses to
water onset were absent on subsequent stimulus presentations that were
separated by only 60 s, but they were present in most cases after a 120 s rest
period. By contrast, the responses to a standard odorant stimulus were as
robust following a 60 s interstimulus interval as they were after one lasting
120 s. A more dramatic illustration of this lability is shown in
Fig. 5, in which records from a
Type I neuron to successive standard stimulus paradigms are shown. A second
stimulus set was initiated within 1.5 s following termination of a previous
water pulse, at which point the input from hydrodynamic receptors was severely
reduced while that to the odorant stimulus was undiminished.
|
|
|
|
|
The response latencies to water onset were also very different from the latencies to odorant presentation in Type I neurons (Fig. 6). The mean latencies of the excitatory postsynaptic potentials (EPSPs) generated by the neuron of Fig. 3 in response to water onset ranged from 408 to 448 ms in this cell; those in response to tetramin injection ranged from 854 ms for the most dilute stimulus to 598 ms for the highest concentration. Latency measurements for responses to water and standard (0.05%) odorant onset in seven other Type I neurons are summarized by the bar graphs in Fig. 7. The majority of these data suggests that the input pathways for odors and hydrodynamic stimuli exhibit very different conduction times and must, therefore, be separate.
|
|
In two preparations, while recording from neurons exhibiting Type I response characteristics, the medial antennular flagellum as well as the lateral was stimulated with both water and odorant pulses to determine whether sensilla on this branch of the antennule are capable of driving OL interneurons. This was not the case in either instance, an example of which is shown in the records of Fig. 8; while not definitive because of the small number of cells examined, these tests suggest that chemosensory input arrives at Type I neurons only via lateral flagellar pathways. Other classes of OL interneurons were not tested this way, however, and possibly do respond to medial flagellar stimulation.
|
|
Experimental data for combined hydrodynamic-odorant stimuli were then obtained from six additional Type I-like cells. Of these, two provided evidence of enhanced spike responses to a combination of odorant onset and fluid movement (Fig. 10) compared with responses to the odorant-imbedded paradigm, although the increase in the responses was not as robust as that for the cell in Fig. 9. These data support the hypothesis that, in a proportion of the Type I cells, a combination of hydrodynamic and odorant stimuli potentiates the response to either stimulus modality by itself. As noted previously, the initiation of fluid movement past the antennule normally generates a three-phase response, E-I-E, and, with this paradigm, the third, excitatory phase will occur during the peak of the long-latency response to odors, as indicated from the data of Fig. 11. Summation of these response components would be expected to occur, possibly accounting for the potentiation when odorant and hydrodynamic inputs occur simultaneously. In addition, as shown in Fig. 12, the consistently more rapid rate of rise of the EPSP following an initial odor pulse, as opposed to an odor pulse imbedded within a long water pulse, may also influence the spike frequency response of these cells. The mechanism for this increased slope is not yet understood, but it may reflect differences in the rise times of EPSPs generated by hydrodynamic and odorant inputs, respectively.
|
|
|
In other Type I-like neurons, the sequence in which odor was presented to the antennular flagellum made little difference to the response magnitude. An example is shown in the records of Fig. 13. Here, it should be noted that the prominent depolarizing peak that normally follows the hyperpolarization evoked by fluid onset is missing from this cell's response profile; furthermore, the hyperpolarization is especially strong. Cell-by-cell variations in the strength of these segments of the response sequence would be expected to affect the magnitude of the delayed EPSP in response to odor.
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In the spiny lobster Panulirus argus, at least nine distinct types
of setae in addition to aesthetasc sensilla are found on the antennular
flagella, and all of them show evidence of being innervated by both
chemosensory and mechanosensory neurons (Cate and Derby,
2001,
2002
). Furthermore, previous
studies have provided evidence for neurons in the spiny lobster deutocerebrum
that are responsive to mechanical as well as odorant stimuli applied to both
antennular flagella (Schmidt and Ache,
1996b
). These cells have dendritic inputs within not only the
olfactory lobes but also the lateral antennular neuropil (LAN), an integration
center for mechanical and non-olfactory chemosensory inputs
(Schmidt et al., 1992
; Schmidt
and Ache, 1992
,
1996a
,b
).
Studies of Type I and II broad-spectrum chemosensory interneurons within the
OL of Procambarus have also provided anatomical evidence for
dendritic arborizations within both the LAN and the OL
(Mellon and Alones, 1995
;
Mellon, 1996
). Since
mechanoreceptive neurons on the antennules project axons to the LAN in
lobsters (Schmidt et al.,
1992
), and because mechanical stimulation drives antennular
flicking in Procambarus, it is assumed that mechanoreceptor axons
terminate in the LAN; thus, both olfactory and mechanosensory afferents may
provide inputs, via OL and LAN pathways, respectively, to Types I and
II deutocerebral interneurons in crayfish.
Electrophysiological recordings from OL neurons in the present study
document multimodal responses to both hydrodynamic and chemical stimulation of
the lateral antennular flagellum in Procambarus clarkii. It is
presumed, but not yet established experimentally, that the hydrodynamic
stimuli are mediated by one or more of the setae types present on the lateral
antennular flagellum. It is assumed that responses of OL neurons to chemical
stimulation of the lateral antennular flagellum are primarily mediated by ORNs
associated with aesthetascs on the ventral aspect of the distal half of the
lateral flagellum, as these are the only classes of lateral flagellum
receptors that innervate the OL directly. However, other classes of
chemoreceptor axons may terminate within the LAN
(Schmidt et al., 1992), and it
is therefore possible that they could contribute to responses evoked in Type I
and II deutocerebral interneurons.
Electrophysiological studies of Type I-like interneurons
Most of the electrophysiological responses from Type I-like neurons
analyzed in the present paper were not verified by morphological examination
of the cells involved, although they strongly resembled the responses to
chemical stimulation from neurons that were analyzed morphologically in
previous studies (Mellon and Alones,
1995; Mellon,
1996
). In our earlier studies, responses of Type I cells did not
include evoked activity to hydrodynamic input, undoubtedly due to the
different mode of stimulation used, where freshwater continuously flowed over
the antennular flagella, probably causing adaptation of the mechanoreceptors
comprising the afferent source of the responses. Furthermore, injection of
odorants into the freshwater stream was effected seamlessly, further
compromising any lingering hydrodynamic sensitivity.
Neurons judged to be Type I in our current study responded to the onset of water flow past the lateral antennular flagellum by a three-phase response profile that consisted of an initial depolarization, usually generating spikes, following the hyperpolarization lasting a second or more, and a second `rebound' depolarization that sometimes generated a spike or two. Above a threshold water pulse duration, the length of the pulse had little influence on the form or the amplitude of the three-phase response, unlike the response to odorant input, which increased with longer stimulus pulses. The functional significance of the E-I-E sequence is not intuitively obvious, and, at this stage of investigation, one can only speculate about its role in the integration of mechanical and chemical inputs. In response to a purely hydrodynamic input, the initial, short-latency spike response is curtailed by an ensuing hyperpolarizing shift in the membrane voltage level, although this is usually terminated by a brief, third-phase depolarization. Consequently, the response to fluid shear alone will be phasic and brief. If the hydrodynamic input is accompanied by a simultaneous exposure to odorant, however, the third phase of the hydrodynamic response may summate with the long-latency response to chemical input and may potentiate it. Therefore, if response dynamics of local deutocerebral interneurons play a role in the interpretation of antennular inputs by the crayfish brain, the triphasic response generated by fluid movements could be important in behavioral choices. As suggested above, differences in the respective response-phase amplitudes, either because of adaptation to previous stimulation or due to intrinsic neuronal properties, could be expected to modulate the extent to which such interactions between stimulus categories can happen. Moreover, in those cells where potentiation of responses to odorants does occur in the presence of simultaneous hydrodynamic stimulation, there would be an obvious benefit to the organism in the form of increased sensitivity to dilute or weak odorants.
The cellular mechanisms involved in the enhanced rate of rise of the primary EPSP in some Type I-like neurons during simultaneous hydrodynamic/chemical stimulation (e.g. Fig. 12) are not immediately obvious; possibly, the steeper slope is simply a reflection of different synaptic dynamics of the short-latency, hydrodynamic-evoked response, but other explanations may be valid. For example, an enhanced membrane conductance during the inhibitory postsynaptic potential (IPSP) response phase, coupled with a raised membrane potential, could favor an increased excitatory synaptic current density due to the afference from the odor receptors, because of a reduced membrane time constant. Insights into the processes involved, however, must await computer modeling studies coupled with biophysical experimentation.
Observations on Type II-like interneurons
Type II-like neurons were recorded from on three occasions during the
present study. Again, due to the revised stimulation paradigm, the responses
of these cells were somewhat different from those originally described by
Mellon and Alones (1995). As
shown in Fig. 14, these
neurons generated tonic impulse activity during water flow past the antennular
flagellum, and this activity was inhibited in a dose-dependent manner by a
seamless injection of odorant into the water pulse. Type II responses are
essentially the inverse of those exhibited by Type I cells, and interactions
between each of them and other, target neurons could also amplify weak odorant
signals imbedded in eddies within the aquatic environment.
The crucial value of the present findings is the extent to which both hydrodynamic and odorant inputs interact to generate responses in large multiglomerular interneurons in the crayfish deutocerebrum. Even though the immediate role of any of these interneuron classes in detecting odor sources by the organism is not yet understood, the data presented suggest that such interactions may take advantage of the simultaneity of fluid movements and changes in odorant concentration, leading to the potentiation of chemical signals by large multiglomerular OL interneurons.
It has been suggested previously that flavored eddies, such as those in the
wake of moving prey, may provide critical cues used in food-finding behavior
for aquatic animals. Such eddy rheo-chemotaxis, as it has been called, would
depend upon cooperativity between chemical and hydrodynamic inputs to locate
the source of moving - or possibly, stationary - food odors
(Basil and Atema, 1994;
Atema, 1996
;
Guenther et al., 1996
).
Another hypothesis predicts that odor-gated rheotaxis, in which animals
actively track upstream during smooth turbulent advection when prompted by the
presence of odors, is critical to locating sources of chemical stimuli
(Weissburg and Zimmer-Faust,
1994
; Weissburg,
2000
; Weissburg and Dusenbury, 2002). Both of these proposed
behavioral mechanisms, as well as others, would depend upon higher-level
central integration of conjoint activity of chemosensory and hydrodynamic
inputs. Although converging mechanical and chemical inputs to the accessory
lobes and lateral protocerebrum of the brain in crayfishes and lobsters have
been reported previously (Sandeman et al.,
1995
; Wachowiak et al.,
1996
; Mellon,
2000
), the present data illustrate that this integration can occur
much earlier, in the central olfactory pathway at the level of presumed
first-order interneurons within the deutocerebrum.
Finally, crayfish and other crustaceans flick their antennules during
food-searching activities, a behavior that must certainly activate antennular
hydrodynamic receptors. Thus, it is expected that mechanoreceptive inputs
during antennular flicking would supplement activity from the aesthetascs, the
spiking activity of which in response to odors, in spiny lobsters at least, is
enhanced by flicking (Schmitt and Ache,
1979). Observations in the current paper suggest that this
enhanced input from the ORNs may be amplified at the level of some local
interneurons by integration of concurrent input from hydrodynamic
mechanoreceptors. It is quite possible, therefore, that interactions between
olfactory and hydrodynamic inputs are most pronounced during flicking
behavior, a time when the animal is actively searching for food-related odors
and would be most attuned to positive interactions between these two critical
sources of sensory input. Experiments are currently underway to specifically
address this possibility.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ache, B. W. (1972). Amino acid receptors in the antennules of Homarus americanus. Comp. Biochem. Physiol. 42A,807 -811.[CrossRef]
Ache, B. W. and Derby, C. (1985). Functional organization of olfaction in crustaceans. Trends Neurosci. 8,356 -360.[CrossRef]
Atema, J. (1996). Eddy chemotaxis and odor
landscapes: exploration of nature with animals sensors. Biol.
Bull. 191,129
-138.
Basil, J. A. and Atema, J. (1994). Lobster
orientation in turbulent odor plumes: simultaneous measurement of tracking
behavior and temporal odor patterns. Biol. Bull.
187,272
-273.
Bender, M., Gnatzy, W. and Tautz, J. (1984). The antennal feathered hairs in the crayfish: a non-innervated stimulus transmitting system. J. Comp. Physiol. A 154, 45-47.[CrossRef]
Cate, H. S. and Derby, C. D. (2001). Morphology and distribution of setae on the antennules of the Caribbean spiny lobster Panulirus argus reveal new types of bimodal chemo-mechanosensilla. Cell Tissue Res. 304,439 -454.[CrossRef][Medline]
Cate, H. S. and Derby, C. D. (2002). Ultrastructure and physiology of the hooded sensillum, a bimodal chemo-mechanosensillum of lobsters. J. Comp. Neurol. 442,293 -307.[CrossRef][Medline]
Daniel, P. C. and Derby, C. D. (1991). Mixture suppression in behavior: The antennular flick response in the spiny lobster towards binary odorant mixtures. Physiol. Behav. 49,591 -601.[CrossRef][Medline]
Dusenbury, D. B. (1992). Sensory Ecology. New York: W. H. Freeman.
Grasso, F. W. and Basil, J. A. (2002). How lobsters, crayfishes, and crabs locate sources of odor: current perspectives and future directions. Curr. Opin. Neurobiol. 12,721 -727.[CrossRef][Medline]
Guenther, C. M., Miller, H. A., Basil, J. A. and Atema, J.
(1996). Orientation behavior of the lobster: responses to
directional chemical and hydrodynamic stimulation of the antennules.
Biol. Bull. 191,310
-311.
Koehl, M. A. R., Koseff, J. R., Crimaldi, J. P., McCay, M. G., Cooper, T., Wiley, M. B. and Moore, P. A. (2002). Lobster sniffing: antennule design and hydrodynamic filtering of information in the odor plume. Science 294,1948 -1951.[CrossRef]
Mellon, DeF. (1996). Dynamic response properties of broad spectrum olfactory interneurons in the crayfish midbrain. Mar. Fresh. Behav. Physiol. 27,111 -126.
Mellon, DeF. (1997). Physiological characterization of antennular flicking reflexes in the crayfish. J. Comp. Physiol. A 180,553 -565.[CrossRef]
Mellon, DeF. (2000). Convergence of multimodal
sensory input onto higher-level neurons of the crayfish olfactory pathway.
J. Neurophysiol. 84,3043
-3055.
Mellon, DeF. and Alones, V. E. (1995). Identification of three classes of multiglomerular, broad-spectrum neurons in the crayfish olfactory midbrain by correlated patterns of electrical activity and dendritic arborization. J. Comp. Physiol. A 177, 55-71.
Moore, P. A. and Grills, J. L. (1999). Chemical orientation to food by the crayfish Orconectes rusticus: influence of hydrodynamics. Anim. Behav. 58,953 -963.[CrossRef][Medline]
Reeder, P. B. and Ache, B. W. (1980). Chemotaxis in the Florida spiny lobster, Panulirus argus. Anim. Behav. 28,831 -839.
Sandeman, D. C. (1989). Physical properties, sensory receptors and tactile reflexes of the antenna of the Australian freshwater crayfish Cherax destructor. J. Exp. Biol. 141,197 -217.
Sandeman, D. C. and Denburg, J. L. (1976). The central projections of chemoreceptor axons in the crayfish revealed by axoplasmic transport. Brain Res. 115,492 -496.[CrossRef][Medline]
Sandeman, D. C. and Luff, S. E. (1974). Regeneration of the antennules in the Australian freshwater crayfish, Cherax destructor. J. Neurobiol. 5, 475-488.[CrossRef][Medline]
Sandeman, D. C., Sandeman, R. E., Derby, C. and Schmidt, M.
(1992). Morphology of the brain of crayfish, crabs, and spiny
lobsters: a common nomenclature for homologous structures. Biol.
Bull. 183,304
-326.
Sandeman, D. C., Beltz, B. and Sandeman, R. (1995). Crayfish brain interneurons that converge with serotonin giant cells in accessory lobe glomeruli. J. Comp. Neurol. 352,263 -279.[CrossRef][Medline]
Schmidt, M. and Ache, B. W. (1992). Antennular projections to the midbrain of the spiny lobster. II. Sensory innervations of the olfactory lobe. J. Comp. Physiol. 318,291 -303.
Schmidt, M. and Ache, B. W. (1996a). Processing of antennular inputs in the brain of the spiny lobster, Panulirus argus. I. Non-olfactory chemosensory and mechanosensory pathway of the lateral and median antennular neuropils. J. Comp. Physiol. A 178,579 -604.
Schmidt, M. and Ache, B. W. (1996b). Processing of antennular input in the brain of the spiny lobster, Panulirus argus. II. The olfactory pathway. J. Comp. Physiol. A 178,605 -628.
Schmidt, M. and Derby, C. D. (2005).
Non-olfactory chemoreceptors in asymmetric setae activate antennular grooming
behavior in the Caribbean spiny lobster Panulirus argus. J. Exp.
Biol. 208,233
-248.
Schmidt, M., Van Eckeris, L. and Ache, B. W. (1992). Antennular projections to the midbrain of the spiny lobster. I. Sensory innervation of the lateral and medial antennular neuropils. J. Comp. Neurol. 318,277 -290.[CrossRef][Medline]
Schmiedel-Jakob, I., Anderson, P. A. V. and Ache, B. W.
(1989). Whole cell recordings from lobster olfactory receptor
cells: Responses to current and odor stimulation. J.
Neurophysiol. 61,994
-1000.
Schmitt, B. and Ache, B. W. (1979). Olfaction: responses of a decapod crustacean are enhanced by flicking. Science 205,204 -206.
Wachowiak, M., Diebel, C. E. and Ache, B. W. (1996). Functional organization of olfactory processing in the accessory lobe of the spiny lobster. J. Comp. Physiol. A 178,211 -226.
Webster, D. R. and Weissburg, M. J. (2001). Chemosensory guidance cues in a turbulent chemical odor plume. Limnol. Oceanogr. 46,1034 -1047.
Weissburg, M. J. (2000). The fluid dynamical
context of chemosensory behavior. Biol. Bull.
198,188
-202.
Weissburg, M. J. and Zimmer-Faust, R. K.
(1994). Odor plumes and how blue crabs use them in finding prey.
J. Exp. Biol. 197,349
-375.