Perisympathetic Organ

A perisympathetic organ (PSO) is one of a metameric series of segmentally reiterated neurohemal organs associated with the thoracic and abdominal ganglia of the ventral nerve cord and the unpaired median or paired transverse nerves of the sympathetic (visceral) nervous system across insects (Entomology; Raabe, 1965; Predel et al., 2004). Discovered and named by the French neuroendocrinologist Marie Raabe in 1965 in walking sticks (Phasmatodea) and subsequently mapped across every major hexapod order by Raabe, Baudry-Partiaoglou, Grillot, and Predel, the perisympathetic organs form the metameric ventral counterpart to the cephalic corpora cardiaca (Raabe, 1989; Predel, 2006). Whereas the retrocerebral corpora cardiaca store and release cerebral neuropeptides from the brain and subesophageal ganglion into the cephalic aorta, the thoracic and abdominal perisympathetic organs serve as specialized neurohemal release sites for neurosecretory axons originating within the segmental ganglia of the ventral nerve cord—most notably the median Va (ventral abdominal) neurosecretory neurons that synthesize CAPA peptides (periviscerokinins and pyrokinins), crustacean cardioactive peptide (CCAP), bursicon, myoinhibitory peptides, and FMRFamide-related peptides. By exocytosing these hormones directly through fenestrated neural lamellae into the perivisceral hemolymph, perisympathetic organs regulate Malpighian tubule fluid secretion, dorsal vessel cardiac output, visceral gut peristalsis, and the stereotypic motor sequences of cuticular ecdysis (Predel & Wegener, 2006; Halberg et al., 2015).

Median, Transverse, and Ganglionic Neurohemal Architectures

In the generalized insect nervous system, each thoracic and abdominal segment contains not only paired segmental somatic nerves innervating body-wall muscles and cuticular sensilla, but also an unpaired median nerve (derived from midline neuroectodermal cells and glial midline precursors) that emerges posteriorly from the dorsal surface of each segmental ganglion and bifurcates into two lateral transverse nerves running along the intersegmental boundary near the spiracles (Snodgrass, 1935; Raabe, 1989).

Depending on the degree of ventral nerve cord condensation across insect orders, perisympathetic organs differentiate at three anatomical positions along this median–transverse nerve tract (Raabe, 1989; Predel et al., 2004):

1. Median Perisympathetic Organs (mPSOs): Fusiform or bulb-like neurohemal swellings located directly along the unpaired median nerve between two successive ventral ganglia (or protruding dorsally as a median club from fused ganglionic neuromeres, as in cyclorrhaphous Diptera and Hymenoptera).
2. Transverse Perisympathetic Organs (tPSOs): Elongated or plexiform neurohemal thickenings situated along the paired transverse nerves after the bifurcation of the median nerve, positioned in direct contact with the lateral perivisceral sinus and the alary muscles of the dorsal vessel (characteristic of Orthoptera, Blattodea, Mantodea, and Lepidoptera).
3. Internal (Ganglionic) or Subcapsular Perisympathetic Organs: In lineages with extreme fusion of abdominal neuromeres into a single thoraco-abdominal synganglion—such as heteropteran true bugs (Hemiptera, including the Chagas disease vector Rhodnius prolixus) and scarab beetles—the neurohemal terminals coalesce inside dorsal superficial grooves beneath the perineurial sheath of the compound ganglion itself or along the proximal roots of the abdominal nerves.

Comparative Topology of Perisympathetic Organs Across Insect Orders

Sinusoidal Glial Fenestrations and Dense-Core Granule Exocytosis

Transmission electron microscopy reveals that a perisympathetic organ lacks intrinsic neuronal cell bodies; unlike the corpora cardiaca (which possess an intrinsic glandular lobe of AKH-synthesizing cells), the PSO is a purely extrinsic neurohemal organ composed of hundreds of tortuous, varicose axon terminals enveloped by attenuated glial processes and a heavily folded, sinusoidal neural lamella (extracellular matrix basal lamina; Raabe, 1989).

Within the PSO stroma, the blood–brain barrier (perineurium) that normally insulates the central nervous system from high-K⁺ hemolymph is absent or perforated by wide extracellular channels (0.5–2.0 μm diameter). Axon varicosities packed with 120- to 250-nm electron-dense neurosecretory granules sit directly against the inner face of the thin neural lamella. When action potentials propagate down the median nerve from the somata of the ventral ganglionic neurosecretory cells, voltage-gated Ca²⁺ channels trigger omega-figure exocytosis of peptide cargoes directly into the bathing hemolymph.

MALDI-TOF Mass Spectrometric Discovery of the capability (CAPA) Gene Products

In 1995, Reinhard Predel and colleagues isolated single abdominal perisympathetic organs from the American cockroach Periplaneta americana and identified the first periviscerokinin (Pea-PVK-1)—a myotropic and diuretic/antidiuretic neuropeptide characterized by the conserved C-terminal motif -PRV-NH₂ or -LIPVMRN-NH₂ (Predel et al., 1995). Subsequent direct-tissue matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass spectrometry on single dissected PSOs (~10–30 μm in diameter) across insects demonstrated a striking metameric neurochemical division of labor (Predel et al., 2004; Predel, 2006):

• Thoracic Perisympathetic Organs are innervated by posterolateral thoracic neurosecretory neurons that synthesize extended FMRFamides (-RFamide peptides), which modulate neuromuscular junction synaptic transmission in thoracic flight and walking muscles and regulate heart contractility.
• Abdominal Perisympathetic Organs are innervated almost exclusively by paired ventral median neurosecretory neurons (Va neurons, typically one pair per abdominal neuromere A1–A6, reduced to three pairs in A2–A4 in Drosophila and mosquitoes) that express the capability (capa) gene. Proteolytic cleavage of the CAPA prepropeptide generates two CAPA-periviscerokinins (CAPA-PVK-1 and -2) and one CAPA-pyrokinin (CAPA-PK, ending in -FXPRL-NH₂), packaged equimolarly inside the same neurosecretory granules of the abdominal PSOs.

Dual Control of Malpighian Tubule Secretion and Cold/Desiccation Tolerance

The CAPA-periviscerokinins released from abdominal perisympathetic organs act on a high-affinity G-protein-coupled receptor (CAPAR) expressed intensely on the principal cells of the Malpighian tubules (Halberg et al., 2015):

1. Nitric Oxide / cGMP Signaling in Diptera (Drosophila and Mosquitoes): In Drosophila melanogaster and some hematophagous dipterans, nanomolar titers of CAPA-1 and CAPA-2 bind CAPAR on Malpighian tubule principal cells, elevating intracellular Ca²⁺, activating mitochondrial and cytosolic nitric oxide synthase (NOS), and stimulating soluble guanylyl cyclase to raise cGMP, which modulates apical V-type H⁺-ATPase proton pumping and coordinates post-prandial diuresis alongside cold-chill coma recovery and desiccation survival (Terhzaz et al., 2012; Halberg et al., 2015).
2. Antidiuretic Action in Hemiptera (Rhodnius prolixus) and Orthoptera: Conversely, in the blood-feeding kissing bug Rhodnius prolixus (vector of Trypanosoma cruzi) and in locusts, CAPA-periviscerokinins released from the abdominal PSOs act as potent antidiuretic hormones. After Rhodnius completes rapid post-blood-meal diuresis driven by serotonin and corticotropin-releasing-factor-like diuretic hormone, abdominal PSO release of Rhopr-CAPA-α2 inhibits serotonin-stimulated fluid secretion by the Malpighian tubules via a cGMP-dependent phosphodiesterase cascade, preventing fatal hemolymph dehydration (Paluzzi & Orchard, 2006).

Coordination of the Ecdysis Motor Cascade and Cuticular Tanning

In Lepidoptera (Manduca sexta), Coleoptera (Tribolium castaneum), and Orthoptera, the transverse perisympathetic organs also house neurohemal terminals of the segmentally reiterated Cell 27 / 704 neurosecretory group (Davis et al., 1993). At the conclusion of each molt, rising ecdysis-triggering hormone (ETH) from tracheal Inka cells and eclosion hormone (EH) from the brain activate this segmental network to release Crustacean Cardioactive Peptide (CCAP) and the heterodimeric cystine-knot hormone Bursicon from the transverse PSOs into the hemolymph. CCAP initiates the rhythmic peristaltic abdominal contractions that shed the old exuviae and accelerates dorsal vessel pumping to expand the newly emerged wings, after which Bursicon activates its leucine-rich repeat receptor Rickets (DLGR2) to phosphorylate tyrosine hydroxylase and drive quinone tanning (sclerotization) of the new insect cuticle.

1. Raabe, M. (1965). Étude des phénomènes de neurosécrétion au niveau de la chaîne nerveuse ventrale des Phasmides. Bulletin de la Société Zoologique de France, 90, 631–654. https://doi.org/10.1007/978-1-4684-7905-8_1
2. Predel, R., Linde, D., Rapus, J., Vettermann, S., & Penzlin, H. (1995). Periviscerokinin (Pea-PVK): A novel myotropic neuropeptide from the perisympathetic organs of the American cockroach. Peptides, 16(1), 61–66. https://doi.org/10.1016/0196-9781(94)00144-U00144-U)
3. Predel, R., Neupert, S., Wicher, D., Gundel, M., Roth, S., & Derst, C. (2004). Unique accumulation of neuropeptides in an insect: FMRFamide-related peptides in the cockroach, Periplaneta americana. European Journal of Neuroscience, 20(6), 1499–1513. https://doi.org/10.1111/j.1460-9568.2004.03598.x
4. Halberg, K. A., Terhzaz, S., Cabrero, P., Davies, S. A., & Dow, J. A. T. (2015). Tracing the evolutionary origins of insect renal function. Nature Communications, 6, 6800. https://doi.org/10.1038/ncomms7800