Neuroanatomy of a crayfish thoracic ganglion: Sensory and motor roots of the walking-leg nerves and possible homologies with insects

Abstract

The internal organization of the third and fourth thoracic ganglia of the crayfish, Pacifastacus leniusculus, was studied in serial sections stained with osmium ethyl gallate. The aims were 1) to provide an anatomical framework for studies of sensorimotor integration in the walking system and 2) to explore possible homologies with abdominal ganglia in crayfish and with the thoracic ganglia of insects. Crayfish thoracic ganglia show several intersegmental homologies with the unfused ganglia of the abdominal nervous system: 1) Longitudinal tracts and dorsal commissures are arranged similarly, allowing use of the same nomenclature. 2) Paired lateral neuropils are located dorsolaterally and contain many large neurites including those of leg motor neurons and of nonspiking, proprioceptive afferents from the basal limb joints. They resemble the lateral neuropils of abdominal ganglia. 3) Neuropil lying more ventrally is fine textured and receives projections from other leg afferents. This ventral neuropil resembles the "horseshoe neuropil" of abdominal ganglia. The functional implications of this organization are discussed. Compared to the abdominal ganglia, however, thoracic ganglia also show specific intersegmental differences: 1) They have more ventral commissures; 2) the ventral neuropil undergoes a large bilateral extension; 3) distinct anteromedial regions of the ventral neuropil receive specific afferent projections; and 4) recognizable dorsoventral "T-tracts" occur. Moreover, these "thoracic" features show a striking resemblance to structures found in thoracic ganglia of orthopteran insects. These correspondences provide further indications that the neuropil of segmental ganglia may be organized in homologous ways in crustaceans and in insects.

Changes in the nitric oxide system in the shore crab Hemigrapsus sanguineus (Crustacea, decapoda) CNS induced by a nociceptive stimulus

“…Their physiology is similar to mammalian low-threshold mechanoreceptors (Byrne et al, 1974) or typical nociceptors (Illich and Walters, 1997) and their noxious-induced responses has been characterized in some invertebrate species (Shen et al, 2002), including crustaceans Barr et al, 2007;Elwood and Appel, 2009;Puri and Faulkes, 2010). In the sensory neuropils, fibers from cheliped receptors make synaptic contacts with dendrites of interneurons and motoneurons (Elson, 1996;Mulloney et al, 2003). In our study, these appeared to be the neurons that display maximum NADPH-d activity shortly after injury, and iNOS immunoreactivity thereafter.…”

Nitric oxide synthase in crayfish walking leg ganglia: Segmental differences in chemo‐tactile centers argue against a generic role in sensory integration

“…1A, asterisk). Cold‐preincubation in the NADPH/NBT solution overnight improved the penetration of the reagents, and the four main soma clusters (anterolateral, lateral, posterolateral, and medial cluster; Elson, 1996) showed as dark regions in the cortex (Fig. 1B).…”

“…We were therefore interested to explore the extent to which NOS is associated with sensory centers in arthropods other than insects, such as crustaceans. A close kinship between insects and crustaceans (“pancrustacea”) is supported by molecular phylogenies (Wilson et al, 2000; Cook et al, 2001; Nardi et al, 2003; Negrisolo et al, 2004) and by a highly conserved organization of the brain and ventral nerve cord (Osorio et al, 1995; Elson, 1996; Strausfeld, 1998; Mulloney et al, 2003). Several neural functions for NO in decapod crustaceans have been identified, including network partitioning and motor pattern selection in the stomatogastric nervous system (Scholz et al, 2001; Christie, 2003; Stein et al, 2005) and retrograde signaling in the heart (Scholz et al, 2002; Goy, 2006).…”

Recruitment in a heterogeneous population of motor neurons that innervates the depressor muscle of the crayfish walking leg muscle

“…This neuron has an extracellular spike of intermediate size and innervates all of the different muscle groups of the leg (Cattaert et al, 1993;Wiens and Wolf, 1993). The main neurite of the common inhibitor lies anteriorly to the primary neurites of all the depressor motor neurons, and its soma lies on the midline of the ganglion, which is in sharp contrast to the somata of depressor motor neurons, which are all located posterior and medial to the neuropil (Chrachri and Clarac, 1989;Elson, 1996). The common inhibitor changes the membrane properties of the muscle fibers to favor rapid relaxation and, thus, promotes more phasic contraction of leg muscles during locomotion (Ballantyne and Rathmayer, 1981).…”