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Combining dissimilar senses: central processing of hydrodynamic and chemosensory inputs in aquatic crustaceans.

Introduction

Aquatic crustaceans, along with other arthropods, display a rich and diverse battery of chemoreceptive and mechanoreceptive cuticular sensilla on the body and appendages. Excluding for the moment those that occur on the organs of smell--the first antennae or antennules--these include various setae on the 2nd antennae, head (including the mouth parts), thorax (including walking legs), and abdomen. Some of these respond primarily to touch, water movements, or both (Laverack, 1962, 1963, 1976; Mellon, 1963; Wiese, 1976; Vedel and Clarac, 1976; Tautz et al., 1981; Vedel, 1986); others respond to chemical stimuli (Bauer et al., 1981; Derby and Atema, 1982a, b; Hatt and Schmiedel-Jakob, 1984; Johnson et al., 1985; Derby and Harpaz, 1988; Voigt and Atema, 1992); and many are bimodal chemo-mechanoreceptors (Altner et al., 1983; Hatt, 1986; Cate and Derby, 2001; 2002a, b; Schmidt and Derby, 2005).

To a significant extent, the loci within the central nervous system in which information from the various sensilla is processed and the manner in which the information is processed depend upon the specific location of the receptors on an animal's body. Information from mechanoreceptors on the telson, uropods, and abdominal tergites, for example, is integrated within the abdominal ganglionic chain, but it may also be sent rostrad to higher centers in the central nervous system (Kennedy, 1963; Kennedy and Mellon, 1964a, b). Information about water movements from bi-directional mechanoreceptors on the branchiostegites of freshwater crayfishes enters the subesophageal ganglion (Mellon, 1963, and unpubl. obs.), whereas chemo- and mechanoreceptor information gleaned by the walking appendages enters at the appropriate thoracic segmental ganglion (Sandeman et al., 1992).

Central targeting and integration of mechanoreceptive input in crustaceans is most thoroughly understood from studies of the tailflip reflex in freshwater crayfish, a behavior that is driven by a relatively large population of bidirectional mechanoreceptor sensilla on the telson, uropods, and abdominal tergites (Kennedy et al., 1974, 1980; Wine et al., 1975; Wiese et al., 1976; Bryan and Krasne, 1977; Plummer et al., 1986; Tautz and Plummer, 1994; Herberholz et al., 2002). This review will, however, focus upon what is currently known about chemical and hydrodynamic sensitivity at the other, that is, rostral, end of the crustacean body and their conjoint integration within the brain.

High-Threshold Chemoreceptors Associated With Bimodal Sensilla

In all aquatic crustaceans, high-threshold chemoreceptors are found associated with a bewildering array of inter- and intraspecific morphological types of setae on the pereiopod dactyls, including those on the great claws, on the antennae, on both antennular flagella, and on the mouthparts (authoritatively reviewed by Derby, 1982). Fine-structural and electrophysiological studies show that many of these types of sensilla are bimodal chemo-mechanoreceptors, and the respective inputs from their associated sensory neurons are presumably used in the detection of food within the substrate by the walking leg dactyls and by contact of the antennae and antennular flagella with the substrate, and during mastication and ingestion of food. These types of bimodal sensilla probably have a functional role similar to those of insect tarsal and labellar contact chemoreceptors, in which substrate contact signaled by mechanoreceptor neurons associated with the sensilla may gate or reinforce the action of the chemoreceptive neurons (Grabowski and Dethier, 1954; Dethier, 1955; Wolbarsht and Dethier, 1958). In crustaceans, although the response spectra of dactyl chemoreceptor neurons has been examined in a number of species (Hatt and Bauer, 1980; Derby and Atema, 1982a, b; Altner et al., 1983; Hatt and Schmiedel-Jakob, 1984; Hatt, 1986), the central target (or targets) of these neurons has not been specifically identified, and the manner, if any, whereby their inputs are integrated with associated mechanoreceptive inputs during food-searching and ingestion behavior is not known. Afferents from mouthpart chemoreceptors must enter the subesophageal ganglion within the central nervous system, but whether they pass through to the brain or make synaptic connections within this complex ganglion is not now understood.

Bimodal chemo-mechanosensory sensilla also occur on both flagella of the 1st antennae (= antennules) of decapod crustaceans. These are best understood from ultrastructural and electrophysiological studies on the spiny lobster Panulirus argus that were carried out in the laboratory of Charles Derby (Cate and Derby, 2001, 2002a, b; Schmidt and Derby, 2005), although an earlier study (Laverack, 1964) presaged these more complete descriptions, as did an investigation of a hydrodynamic receptor (pinnate hair) on the antenna of the spiny lobster Panulirus japonicus (Tazaki and Ohnishi, 1974). Bimodal hooded sensilla on the antennular flagella of the spiny lobster are supplied by 12-13 primary sensory neurons, some of which are chemosensory and some of which are mechanosensory. The chemoreceptor cells were sensitive to a broad-spectrum search stimulus and to either ammonium ion or taurine, in some cases at concentrations down to [10.sup.-6] mol [1.sup.-1] (Cate and Derby, 2002a). Mechanosensory neurons associated with the hooded sensilla had a high threshold and did not respond to water currents introduced past the antennular flagellum at the flow velocity used. They did, however, respond with phasic spike bursts to tactile displacements toward the flagellum (Cate and Derby, 2002a), suggesting that they are contact mechanoreceptors. The previous study of antennular tactile receptors in P. argus by Laverack (1964) did not test whether those sensilla responded to water movements past the flagellum.

Schmidt and Derby recently (2005) examined another type of sensillum on the lateral antennular flagellum of P. argus, the asymmetric hair. On the basis of studies on grooming behavior, they concluded that these sensilla are sensitive to the amino acid L-glutamic acid. Scanning electron microscopical examination of the asymmetric hairs revealed a pore at the distal tip of the sensillum, and importantly, fluorescence-labeled probes to phalloidin disclosed scolopales at the sensillar base within the cuticle, providing strong presumptive evidence, respectively, for both a chemoreceptive and a mechanoreceptive function. In the freshwater crayfish Procambaus clarkii, electrical recordings from the antennular nerve within the base of the lateral antennular flagellum have revealed spiking responses to jets of water directed at the flagellar tip (Mellon, 1997). Recent preliminary unpublished evidence from the author's laboratory suggests that the sense organs in which this activity originates represent a small ([less than or equal to] 12) population of cuticular setae resembling in their morphology the branchiostegite pit receptor hairs previously studied (Mellon, 1963).

The preceding paragraphs indicate that, despite the prevalence of bimodal chemo-mechanoreceptor sensilla on the crustacean body, few studies have examined them in sufficient detail to provide anything like a comprehensive catalog of their physiological properties, and there is virtually no information concerning how these combined inputs are integrated, if they are, within the central nervous system. As will be presented below, the situation with respect to the olfactory system is somewhat more optimistic.

Why combine chemosensory and mechanosensory neurons within the same cuticular sensillum? The functional significance of grouping bimodal neurons in single sensilla, aside from anatomical parsimony, was recently addressed in a paper by Vermeulen and Rospars (2004). Their passive electrical model of insect olfactory sensilla suggests that the amplitude of the transmembrane receptor potential is increased in a sensory neuron whose sensitivity to a particular chemical stimulus is greater than that of its immediate neighbor. If this model includes mechanosensory neurons as well, the presence of non-excited chemosensory neurons adjacent to the excited mechanosensory neuron in a bimodal sensillum might actually enhance the firing capabilities of that neuron. The same model predicts, however, that combined firing of mechano- and chemosensitive neurons might slightly reduce the response capabilities of both.

Perhaps a more compelling argument can be made that housing the mechanoreceptor and chemoreceptor neurons within the same structure permits near-simultaneous activation of the two pathways when contacting an appropriate (= chemically attractive) substrate. Because central processing of these combined inputs is not currently understood, however, we can only speculate about possible mechanisms of cooperation between these two dissimilar sources of sensory activity. The presence of mechanoreceptor input, for example, could provide a "gate" for the central transmission of chemosensory information to higher centers, allowing purely fluid-borne chemical attractants to be ignored in the absence of mechanosensory input, or at least providing for a greatly (heterosynaptically) facilitated chemosensory input when it occurs in conjunction with foraging behavior that involves probing of the substrate itself. This type of central search strategy would thereby be more sharply focused upon potentially important environmental signals, much as concurrent auditory and visual inputs focus attention upon critically important signals in the brains of advanced vertebrates.

In contrast, another argument could be advanced that mechanoreceptor input actually inhibits the transmission of weak chemoreceptor signals and thus, by raising the threshold for chemical inputs, improves chances of uncovering the highly concentrated signal source within the substrate. Viewed as analogous to surround inhibition, such a mechanism would emphasize the contrast between the relatively weak, diffusible, or highly-chaotic fluid-borne chemical signals and those highly concentrated odors closely associated with the substrate-bound source.

Little also is understood concerning co-operativity--if any--between the contact-type chemoreceptors on the various appendages and the olfactory input from the lateral flagella. For example, do low concentrations of olfactory-mediated signals "alert" the appropriate flagellar- or pereiopod-associated contact chemoreceptor centers to the presence of a specific odorant cocktail in the water column? Do certain kinds of olfactory inputs implicitly generate substrate-searching behavior focused upon that odorant cocktail, whereas others trigger alternate search strategies? As discussed below, there are reasons to suspect central associations between the olfactory and non-olfactory chemoreceptor pathways.

Olfactory Chemoreceptor Sensilla: Morphology and Distribution

Olfactory setae in crustaceans are called aesthetasc sensilla; they are exclusively found on the lateral antennular flagella, where details of their position, spacing, and density are species-specific. In the Brachyura (true crabs) and hermit crabs, the aesthetases are found in a dense tuft on the ventral surface of the tip of the flagellum (Snow, 1973; Gleeson, 1980). In the spiny lobsters, this tuft is more spread out longitudinally, but its length is still only about 20% of that of the flagellum as a whole. In the spiny lobster Panulirus argus, the aesthetases are generally arranged in two rows of 8-10 each, diagonally across the ventral surface of an annulus. Each aesthetasc is roughly 1000 [micro]m long and 20 [micro]m at the base, tapering slightly toward the tip (Laverack, 1964, 1965; Grunert and Ache, 1988). Each annulus is about 500 [micro]m in diameter and roughly 300 [micro]m wide; since the aesthetasc array occupies only the central one-third of the ventral surface, the aesthetases are packed at a rather high density (ca. 1 per 140 [micro][m.sup.2]). In chelate lobsters such as Homarus americanus, aesthetasc packing has a similar high density, and the extent of the tuft region is larger than that of Panulirus. In the crab Paragrapsus gaimardii, there are 160-170 aesthetases on each lateral flagellum, each one being 11-12 [micro]m in diameter and 600 [micro]m long (Snow, 1973). In other marine decapods, such as the crab Cancer productus, the aesthetases are 15-20 [micro]m at their base and range to 1700 [micro]m in length, again with a high packing density (data from Ghiradella et al., 1970).

The distribution of aesthetasc sensilla on freshwater crayfishes is much sparser than in marine decapods, with the "tuft" region being spread out for at least half the length of the lateral flagellum; furthermore, there are only 2-6 aesthetases per annulus (Tierney et al., 1986; Mellon et al., 1989). Since the sensilla are again about 20 [micro]m in diameter at their base, the space between individual aesthetases is considerably larger than on their marine counterparts.

In all crustaceans, aesthetasc sensilla enclose the distal dendritic segments of olfactory receptor neurons (ORNs). It has been reported that about 350 ORNs are associated with each aesthetasc in P. argus (Grunert and Ache, 1988), 300 in the lobster Panulirus interruptus (Spencer and Linberg, 1986), about 130 in the crab Paragrapsus gaimardii (Snow, 1973), 100 in Cancer productus (Ghiradella et al., 1970), 400 in the marine hermit crab Pagurus hirsutiusculus (Ghiradella et al., 1968b), 100 in the terrestrial hermit crab Coenobita clypeatus (Ghiradella et al., 1968a), and 175 (Mellon et al., 1989) or between 40 and 110 (Tierney et al., 1986) in freshwater crayfish. Dye studies suggest that the cuticle on the distal regions of all decapod aesthetases is uniquely transparent to aqueous solutes (Ghiradella et al., 1968a, b; Snow, 1973; Tierney et al., 1986), providing the physical property necessary for diffusion of odorants into the lumen of the aesthetasc.

Numerical Relationships Between Olfactory Receptor Neurons, the Receptor Proteins Expressed on Their Dendrites, and Their Target Glomeruli in the Brain

Crustacean ORN axons course within the antennular nerve to a specific, ipsilateral region of the deutocerebrum, the olfactory lobe (OL), characterized in all decapods (as in the immediate central nervous targets of olfactory axons in all other arthropods as well as in vertebrates) by compartmentalized aggregations of neuropil referred to as glomeruli. In mammals, unique classes of ORNs have particular olfactory glomeruli as their targets, and it is thought that a single type of olfactory receptor protein is expressed in each (of about 1000) class (Buck and Axel, 1991; Mombaerts et al., 1996; Hildebrand and Shepherd, 1997; Couto et al., 2005). To an extent, a similar organizational principle applies in insects, although the number of different olfactory receptors expressed is far less (about 60 in Drosophila), and the parent ORNs project to 47 antennal lobe glomeruli (Clyne et al., 1999; Gao and Chess, 1999; Vosshall et al., 1999, 2000). However, the relationship of one receptor type per ORN does not necessarily hold in arthropods. In Drosophila, single ORNs expressing two types of receptors have recently been documented (Dobritsa et al., 2003; Jones et al., 2007), and in single ORNs of the spiny lobster Panulirus, two types of olfactory ligand-gated signal transduction pathways have been identified through their action on separate ion channels (Hatt and Ache, 1994). The latter finding is presumptive evidence that more than one receptor type resides on the same ORN.

Although different families of heterogeneous ORNs have been found to occupy distinct, identifiable zones in the mammalian olfactory mucosa (Astic and Saucier, 1988), this is not the case in crayfish, where the distribution of ORN/aesthetasc associations is nontopographic inasmuch as ORN axons from aesthetases on the tip or the middle of the antennule project to all glomeruli of the OL. From studies using transport of radioactive leucine, every aesthetasc appears to contain identical, heterogeneous classes of ORNs, each of which probably targets a uniquely different glomerulus (Mellon and Munger, 1990; Mellon and Alones, 1993). The conclusion is that all aesthetases contain an identical combination of different types of ORNs, based upon the diversity of their odorant receptor proteins. Since, as stated above, it is thought that each glomerulus is targeted by ORNs expressing the same odorant receptor or receptors, it follows that the number of glomeruli should bear some consistent numerical relationship with the number of classes of ORNs. Because the odorant receptors of no crustacean species have yet been cloned, we still have no correlation between the number of odorant receptors expressed and the number of glomeruli in the OL; however, if the organizational principles are similar to those found in other metazoans to date, the number of glomeruli in the OL should provide a numerical value close to, if not identical with, the actual number of expressed odorant receptors across the ORN array.

Not all crustaceans share the same number of glomeruli in their OLs; thus there are apparently species differences in the number of expressed odorant receptors. Beltz et al. (2003) have examined and compared the numerical relationships between the number of aesthetases, the number of OL glomeruli, the convergence ratio, and the natural habitat of several different decapods in the Achelata, Homarida, Astacida, Anomala, and Brachyura. There are very large differences across taxa and species in absolute number of glomeruli (which in all crustaceans is apparently determined at the final developmental instar), in the density and number of aesthetases (the latter, however, increasing during growth), and in the convergence ratio of aesthetases to glomeruli. These differences cross taxonomic boundaries, but they are also present within specific groups. Variability in the number of ORNs per aesthetasc, on the other hand, is smaller, in all probability being no greater than a factor of 3 (Beltz et al., 2003).

Physiology of Olfactory Receptor Neurons

Electrophysiological recordings of action potentials from individual ORNs have to date been confined to the homarid Homarus americanus and the spiny lobster Panulirus argus. Early studies by Ache (1972) on responses of presumptive Homarus ORNs indicated that they are sensitive to some amino acids (taurine) at concentrations as low as 5 X [10.sup.-7] mol [l.sup.-1]. More recent and more extensive analysis of Homarus ORNs by Atema and his colleagues (Johnson and Atema, 1983; Borroni and Atema, 1988; Gomez and Atema, 1996a, b) showed that presumptive ORNs of Homarus are narrowly tuned to certain amino acids and to ammonium ion ([NH.sub.4.sup.+]). Their responses are a function of odorant concentration, application rate, and exposure time. The dynamics of individual lobster ORN responses to odorant presentations have been examined in detail by Gomez and Atema (1996a, b). Increased concentrations of odorant decreased the latency to first spike by about 25% over 2 log units of change. Maximal responses to odorant at a fixed concentration, in terms of initial spike frequency, were obtained to rectangular odor pulses of about 220 ms in duration; longer pulses generated more spikes but did not increase the initial spike frequency. Adaptation to odor exposure was rapid, occurring in less than 1 s. The time constant for disadaptation in individual lobster ORNs averaged 14 s, regardless of the adapting concentrations used (Gomez and Atema, 1996b). These results suggest that ORN receptor dynamics are tuned to odorant concentration changes occurring at 4-5 Hz, which not only corresponds to the Homarus flicking frequency but also represents the time window of changes in odor concentration observed in natural odor plumes (Gomez and Atema, 1996a). Importantly, at least in the case of some narrowly tuned Homarus ORNs, the response-intensity functions were shifted to the right, without a change in slope, in the presence of adapting, background concentrations of the preferred odorant species. These findings indicate that, as with arthropod and vertebrate visual receptors, the ORNs are sensitive to changes in the ratio of stimulus concentration to background concentration, allowing the receptors to function with equal sensitivity to rapid changes in stimulus concentration over at least 3 log units of background (Borroni and Atema, 1988). The findings with Homarus ORNs emphasize the important, perhaps critical, role of temporal factors in odor reception by this large crustacean.

Additional, extensive data concerning response characteristics of crustacean ORNs come from a long series of investigations with the achelate decapod Panulirus argus. Beginning in the mid 1970s, Ache and his co-workers have tabulated response properties, antennular flicking effects, and odorant mixture interactions in spiny lobster presumptive ORNs. Among these studies were early measurements of the very low thresholds for amino acids that could be detected by Panulirus ORNs (Thompson and Ache, 1980), the complexities of interactions between different amino acid odorants in stimulating individual ORNs (Derby and Ache, 1984; Gleeson and Ache, 1985; Fine-Levy et al., 1988; Girardot and Derby, 1990a, b; Daniel and Derby, 1991a, b; Derby et al., 1991a, b; Michel and Ache, 1995), and the enhancement of ORN responses to amino acid odorants by antennular flicking (Price and Ache, 1977; Schmitt and Ache, 1979). These studies showed that the ORNs of spiny lobsters are sensitive at very low concentration levels ([10.sup.-13]-[10.sup.-12] mol [l.sup.-1]) to dissolved amino acids and other biological compounds such as amines, ammonium ion, and some nucleotides. In general, tuning of individual ORNs is narrow but not absolute, its breadth varying as a direct function of concentration. This situation is consistent with the odor determinants, that is, the ligands for specific ORN odor receptors, occurring in various combinations on many different complex molecules encountered by the ORNs. Adaptation to odorant stimuli in individual ORNs apparently occurs over a longer time frame than in Homarus. How the presence of more than one molecular species of an odorant changes the ORN sensitivity to one or the other of the individual components of the mixture cannot be readily predicted. This uncertainty can be viewed as a reflection of our current ignorance of the specific nature of olfactory determinants that are recognized by receptors on individual ORNs.

A potentially crucial caveat must be sounded concerning these early electrophysiological studies of the presumed ORNs in both Homarus and Panulirus. Until the advent of patch clamp recordings from individual ORN somata in Panulirus (Schmiedel-Jakob et al., 1989; McClintock and Ache, 1989; Fadool et al., 1993), all the relevant data were obtained from extracellular suction electrodes attached to small aggregations of tiny axons mechanically stripped from the antennular nerve branches. Along with our recent understanding of the presence of non-aesthetasc-associated chemoreceptor neurons on the lateral antennular flagellum has arisen uncertainty regarding the sensillar associations of the early data. Were they obtained from ORNs or from neurons associated with non-aesthetasc sensilla? This confusion underscores the tenuous state of our current understanding about the diversity, respective properties, and central effects of antennular chemoreceptor inputs.

Central Targets of Olfactory Receptor Neuron Axons

Figure 1 is a simplified diagram of the crayfish deutocerebrum and some of its input and output connections. In all decapods, ORN axons run within the antennular nerve and terminate within a glomerulus of the ipsilateral olfactory lobe (Sandeman and Denberg, 1976; Sandeman and Luff, 1973; Mellon et al., 1989; Mellon and Munger, 1990; Mellon and Alones, 1993; Schmidt and Ache, 1992; Schmidt et al., 1992). Within a glomerulus, individual afferents make synaptic contact with local interneurons and, probably, with multiglomerular projection neurons whose somata reside in cell cluster 10 (Sandeman et al., 1992) and that send their axons to targets in the lateral protocerebrum (Mellon and Alones, 1995; Schmidt and Ache, 1996b; Wachowiak et al., 1996; Sullivan and Beltz, 2001, 2005; Sandeman and Mellon, 2002; McKinzie et al., 2003). It is thought that the local interneurons may provide interglomerular linkages vital for processing and identifying complex odorants (Stopher et al, 1997). Immunocytochemical studies have identified at least six types of local interneuron in the spiny lobster deutocerebrum (Schmidt and Ache, 1997).

In many decapods, a large, paired deutocerebral structure called the accessory lobe (AL) is intimately conjoined with the OL. This region of glomerular neuropil has proved to be enigmatic in both its functional significance and its capricious appearance across taxa (Sandeman and Sandeman, 1994; Sandeman et al., 1995; Sullivan and Beltz, 2004, 2005). Extensive neural connections occur between the OL and AL (Wachowiak et al., 1996) as well as between the AL and the lateral protocerebrum (Mellon and Alones, 1993; Wachowiak et al., 1996; Sullivan and Beltz, 2001, 2004, 2005). The AL receives no direct sensory inputs, but it is the target of higher order inputs from tactile and visual centers of the brain (Sandeman and Sandeman, 1994; Sandeman et al., 1995) as well as from the OL (Wachowiak et al., 1996). The AL appears to have evolved in association with the brains of more recent decapods (Sullivan and Beltz, 2005). Its large size in astacids, homarids, and achelatids suggests an important, perhaps critical, role in integrating visual, tactile, and olfactory inputs. In the crayfish Procambarus clarkii, multimodal sensory information is transmitted to parasol cells in the hemiellipsoid body, within the lateral protocerebrum (Mellon, 2000), presumably by projection neurons originating in the accessory lobes (Sullivan and Beltz, 2001, 2005; McKinzie et al., 2003).

[FIGURE 1 OMITTED]

In the crayfish Procambarus clarkii and the spiny lobster Panulirus argus, local interneurons in cell clusters 9/11 of the deutocerebrum invest extensive dendritic arbors not only within the OL but also in another antennular input center, the lateral antennular neuropil, or LAN (Mellon and Alones, 1995; Mellon, 1996; Schmidt et al., 1992; Schmidt and Ache, 1996a). Electron microscopical examination has shown that at least some of these local interneurons possess input synapses within both the LAN and the OL (Mellon and Alones, 1995). Because the LAN is a major target of both mechanosensory and non-aesthetasc chemosensory inputs (Schmidt et al., 1992; Schmidt and Ache, 1996a), these local interneurons are prime candidates as integrators of olfactory and hydrodynamic inputs. Physiological studies of the multisensory local interneurons are limited to Procambarus and Panulirus. Mellon and Alones (1995) examined three classes of local interneurons having somata in cell cluster 9/11 of Procambarus. Of these, Type I and Type II have dendrites within both the OL and the LAN. The presumed output pathway for these cells consists of terminal branches within a small bilateral neuropil called the olfactory globular tract neuropil, through which pass the axons of cluster 10 projection neurons that course between the OL, AL, and lateral protocerebrum. Whereas Type I neurons respond in a dose-dependent, excitatory manner to broad-spectrum odorants, amino acids, and glucose injected into a freshwater stream flowing past the antennule, Type II neurons are driven by fluid flow but are inhibited by the same odorant compounds, with the strength of their response again directly dependent upon stimulus concentration (Mellon and Alones, 1995; Mellon, 1996). It is conceivable that networks within the brain in which both Types I and II local neurons converge upon common postsynaptic targets could amplify those hydrodynamic inputs that are flavored by odorants. Hypothetical targets that are inhibited by Type II cell activity but excited by Type I activity would be silent or only weakly excited during pure hydrodynamic stimulation, but they would be strongly excited by fluid movements containing odors, during which Type II activity would be suppressed. While conjectural, such considerations are supported in principle by known network properties in other arthropod and vertebrate sensory systems.

Similar patterns of dendritic arborization and electrical activity were observed in cell cluster 9/11 in Panulirus by Schmidt and Ache (1996b). In these studies, the flagella of an antennule were sealed within separate tubes through which either seawater or a combination of odors dissolved in seawater could be separately flushed. Several of the interneuron types identified by their physiology and dye-filled morphology--including in one instance a multiglomerular projection neuron--generated action potentials in response to the passage of seawater past the lateral flagellum as well as (at longer latency) to the pulse of test odorant. A number of the neurons observed by these authors also had dendrites with LAN as well as in OL; thus these local interneurons clearly were integrating both hydrodynamic and olfactory inputs.

Recently a more thorough study was made of the responses to odorant and hydrodynamic stimuli in Procambarus Type I local deutocerebral interneurons (Mellon, 2005). As with the earlier study by Schmidt and Ache (1996b), the lateral and medial antennular flagella were sealed within individual olfactometers, through which either plain fresh water or dissolved odorant could be injected. By itself, a rectangular pulse of water alone flushed past the lateral flagellum generated short-latency ([less than or equal to] 450 ms), phasic bursts of spikes in the Type I cells. These responses were short (generally lasting 1 s or less) and rapidly adapted to repeated stimuli. By seamlessly incorporating an odorant pulse within the longer pulse of water, dose-dependent, prolonged responses to a broad-spectrum test stimulus (tetramin) were obtained at long latency ([greater than or equal to] 700 ms) from these neurons. Over the range of tetramin concentrations tested (0.000001%-0.01 %), the Type I neurons responded linearly (in terms of numbers of spikes during the period of stimulation) to log increases in stimulus strength, presumably reflecting the response-intensity function of the population of ORNs. Importantly, when initial onset of fluid past the antennule was odorant solution instead of plain water, a summed response occurred that in some cells was twice the response magnitude of that to odorant alone (Mellon, 2005). Because odorants are imbedded in advective and eddy-turbulent fluid movements within the aquatic environment, it is apparent that these two sources of sensory input can act co-operatively to assess ambient conditions (Atema, 1996).

During antennular flicking behavior, the lateral antennular flagellum is rapidly depressed from its normal resting posture and then returned at a slower speed. This behavior undoubtedly stimulates mechanoreceptors on the lateral flagellum (Mellon and Humphrey, 2007; Humphrey and Mellon, 2007), which in turn would be expected to excite Type I and, perhaps, other classes of interneurons in the deutocerebrum. Flicking temporally enhances the responses of spiny lobster ORNs to odorants (Price and Ache, 1977; Schmitt and Ache, 1979), possibly by disrupting the boundary layer of water around individual aesthetases (Koehl et al., 2001; Koehl, 2006). If a similar argument applies for crayfish aesthetases, then the response of Type I interneurons to both ORNs and antennular hydrodynamic receptors will certainly be enhanced during a downward flick of the lateral flagellum. This possibility seems more than likely in light of recent experimental observations that fluid movement past the lateral flagellum in a caudal-to-rostral direction, which mimics (but with less velocity) the fluid movement experienced by the flagellum during a downward flick, optimally enhances the hydrodynamic component of Type I interneuron responses (Humphrey and Mellon, 2007). These observations suggest, then, that maximum excitation of local interneurons in the crayfish brain will occur in response to flicking, as well as to odor-flavored eddy fronts.

Conclusions

There are large gaps in our understanding of the central processing of information conveyed to the central nervous system via bimodal chemo-mechanoreceptor sensilla on crustacean appendages. Although different types of these bimodal structures are still being described, the potential interactions of their dissimilar inputs with each other as well as with other classes of chemo- and mechanosensory inputs on the antennular flagella are virtually unexplored. On the other hand, some of the principles that have emerged from several decades of work on chemoreception in freshwater and marine decapods suggest that peripheral sensors and central integrating pathways emphasize temporal changes in the conditions of background chemical and hydrodynamic stimuli. Chemoreceptors in homarid lobsters respond maximally to brief, rapid odorant exposures. In the face of adapting background odor concentrations, absolute sensitivity is depressed, but the response-intensity functions maintain their original slope while being shifted to the right along the axis of increasing concentration. Spiny lobsters provide evidence that transient enhancement of slowly adapting ORN responses occurs during brief downward flicks of the antennule. In both spiny lobsters and freshwater crayfish, local deutocerebral interneurons integrate hydrodynamic and odorant inputs; in the case of the crayfish, the response of these central elements is enhanced when the two sources of stimulation occur in concert (Mellon, 2005). In other crustaceans, however, chemical and hydrodynamic cues can be used in a sequential manner to bring critical behaviors to fruition. Male copepods can track the lingering pheromone trail left in the aquatic realm by conspecific females, and they do so until they encounter the strong wake vortices close to their target, at which point hydrodynamic inputs from the female become critical (Yen et al., 1998). Recent measurements by Catton et al. (2007) suggest that the hydrodynamic signature of free-swimming copepods can be quite large; males up-swimming females' trails should thus have ample warning that their approach to target is imminent. These findings underscore our growing appreciation for the temporal filtering of chemical cues and the contribution of hydrodynamic input to this process for chemical guidance within the aquatic environment.

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DEFOREST MELLON, JR.

Department of Biology, University of Virginia, Charlottesville, Virginia 22903

Received 19 January 2007; accepted 22 March 2007.

* To whom correspondence should be addressed. E-mail: dm6d@virginia.edu

Abbreviations: AL, accessory lobe; OL, olfactory lobe; ORN, olfactory receptor neuron; LAN, lateral antennular neuropil.
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