Smelling, feeling, tasting and touching: behavioral and neural integration of antennular chemosensory and mechanosensory inputs in the crayfish

Abstract

SummaryCrustaceans possess two pairs of prominent, movable sense organs on the rostral aspect of their bodies termed antennae: (1) a relatively short, usually bifurcate pair, the 1st antennae, also referred to as antennules, and (2) a much longer, uniramous pair, the 2nd antennae, or just ʻantennaeʼ. The antennules are equipped with diverse arrays of six or more types of cuticular setae, most of which are believed to have a sensory function. Axons from these structures course within the antennular nerve to the deutocerebrum, a large middle brain region that is known to receive chemoreceptor and mechanoreceptor inputs. In crayfish, axons from two kinds of single sensory-function setae, the olfactory receptor aesthetasc sensilla and as yet unidentified hydrodynamic sensilla, on the lateral antennular flagellum terminate, respectively, within the ipsilateral olfactory lobe and the lateral antennular neuropil of the deutocerebrum, where their activity generates synaptic potentials in local interneurons having dendritic fields that span both of those regions. It has been suggested that the short-latency hydrodynamic input gates or otherwise supplements the olfactory input signals. Much less is known about the functional capabilities of the other sensillar types on the antennular flagella, including the bimodal sensilla: how their inputs are distributed to the various neuropils of the deutocerebrum, whether they target common or separate brain neurons, and the nature, if any, of their functional relationships to the aesthetasc and hydrodynamic sensilla. Integrated processing of chemical and hydrodynamic signals undoubtedly plays an important role in locating odorant sources, perhaps by detecting boundaries of odorant plumes (tropotactic discrimination); other less-plausible strategies include time averaging of turbulent odorant signals and determination of concentration slopes within turbulence-generated odorant patches. These gaps in our understanding present important, but surmountable, experimental challenges for the future.

Waptia revisited: Intimations of behaviors

“…1E, F), an arrangement that corresponds to the malacostracan organization of long haptic sensilla (guard sensilla) with mechanosensory functions (Mellon, 2012) flanking rows of chemosensory aesthetascs (Hallberg and Skog, 2011), as along the caudal edge of Nebalia antennules (Martin et al, 1996). In Waptia, pairs of long slender sensilla extend laterally and forward from the ventral side of the antennule (Fig.…”

“…Whether certain setae housed both contact chemosensory and mechanosensory receptors, as occurs in modern crustaceans, is unknown. There are no external markers that would differentiate these from exclusively tactile sensilla, but there is every reason to suppose that Waptia's antennae served multisensory functions comparable to those described for modern decapods (Mellon, 2012).…”

Simultaneous Sampling of Flow and Odorants by Crustaceans can Aid Searches within a Turbulent Plume

“…Odorants in the benthic flow are carried to the olfactory organs of the animal through turbulent water currents and diffuse toward the surface of the organs where chemoreceptors are located. These olfactory organs also contain mechano-receptors that provide information about the turbulent flow, and together with odorant concentration help the animal locate the source of the chemical plume [7]. Animals use a variety of sensing strategies to orient themselves in the direction of the plume source depending on the flow regimes they operate in [8].…”

“…Thus, concentration and flow cues simultaneously excite chemoreceptors and mechanoreceptors of the antennules during flicking. In addition, many invertebrate organisms, including the spiny lobster P. argus [36], and crayfish P. clarkii [7], contain bimodal chemo-mechanoreceptors on their antennules that respond to both odorants and flow. For P. clarkii , local deutocerebral interneurons integrate hydrodynamic and odorant inputs, and the response of these central elements is enhanced when both flow and odorant stimulation occurs together [31].…”

Adaptation of sensor morphology: an integrative view of perception from biologically inspired robotics perspective

“…It was observed that, along the antennule of the freshwater crayfish, there were four predominant mechanosensory sensilla, which were crucial for detecting their predators, mates and varying environmental substrates [88]. In this regard, a numerical model was proposed to confirm the relationship between the four sensilla morphologies and the sensitivity in sensing the flow perturbations within the crayfish's surrounding fluid [56] …”