Morphology and innervation of the teleost physostome swim bladders and their functional evolution in non-teleostean lineages.

Swim bladders and lungs are homologous structures. Phylogenetically ancient actinopterygian fish such as Cladistians (Polypteriformes), Ginglymods (Lepisosteids) and lungfish have primitive lungs that have evolved in the Paleozoic freshwater earliest gnathostomes as an adaptation to hypoxic stress. Here we investigated the structure and the role of autonomic nerves in the physostome swim bladder of the cyprinid goldfish (Carassius auratus) and the respiratory bladder of lepisosteids: the longnose gar and the spotted gar (Lepisosteus osseus and L. oculatus) to demonstrate that these organs have different innervation patterns that are responsible for controlling different functional aspects. The goldfish swim bladder is a richly innervated organ mainly controlled by cholinergic and adrenergic innervation also involving the presence of non-adrenergic non-cholinergic (NANC) neurotransmitters (nNOS, VIP, 5-HT and SP), suggesting a simple model for the regulation of the swim bladder system. The pattern of the autonomic innervation of the trabecular muscle of the Lepisosteus respiratory bladder is basically similar to that of the tetrapod lung with overlapping of both muscle architecture and control nerve patterns. These autonomic control elements do not exist in the bladders of the two species studied since they have very different physiological roles. The ontogenetic origin of the pulmonoid swim bladder (PSB) of garfishes may help understand how the expression of these autonomic control substances in the trabecular muscle is regulated including their interaction with the corpuscular cells in the respiratory epithelium of this bimodal air-breathing fish.

Immunolocalization of neurotransmitter-synthesizing enzymes and neuropeptides with associated receptors in the photophores of the hatchetfish, Argyropelecus hemigymnus Cocco, 1829.

Anatomical and functional studies of the autonomic innervation of the photophores of luminescent fishes are scarce. The present immunohistochemical study demonstrated the presence of nerve fibers in the luminous epithelium and lens epithelium of the photophores of the hatchet fish, Argyropelecus hemigymnus and identified the immunoreactive elements of this innervation. Phenylethanolanine N-methyltransferase (PNMT) and catecholamine (CA)-synthesizing enzymes were detected in nerve varicosities inside the two epithelia. Neuropeptides were localized in neuropeptide Y (NPY) and substance P (SP)- and its NK11 receptor-immunopositive nerves in the lens epithelium. Neuropeptides were also localized in non-neural cell types such as the lens cells, which displayed immunoreactivities for pituitary adenylate cyclase activating peptide (PACAP) and their receptors R-12 and 93093-3. This reflects the ability of the neuropeptide-containing nerves and lens cells to turn on and off the expression of selected messengers. It appears that the neuropeptide-containing nerves demonstrated in this study may be sensory. Furthermore, neuronal nitric oxide synthase-immunopositive axons associated with photocytes in the luminous epithelium have previously been described in this species. Whereas it is clear that the photophores receive efferent (motor) fibers of spinal sympathetic origin, the origin of the neuropeptide sensory innervation remains to be determined. The functional roles of the above neuropeptides or their effects on the bioluminescence or the chemical nature of the terminals, either sensory or postganglionic neurons innervating the photophores, are still not known.

Nervous control of photophores in luminescent fishes.

Functional studies of the autonomic innervation in the photophores of luminescent fishes are scarce. The majority of studies have involved either the stimulation of isolated photophores or the modulatory effects of adrenaline-induced light emission. The fish skin is a highly complex organ that performs a wide variety of physiological processes and receives extensive nervous innervations. The latter includes autonomic nerve fibers of spinal sympathetic origin having a secretomotor function. More recent evidence indicates that neuropeptide-containing nerve fibers, such as those that express tachykinin and its NK1 receptor, neuropeptide Y, or nitric oxide, may also play an important role in the nervous control of photophores. There is no anatomical evidence that shows that nNOS positive (nitrergic) neurons form a population distinct from the secretomotor neurons with perikarya in the sympathetic ganglia. The distribution and function of the nitrergic nerves in the luminous cells, however, is less clear. It is likely that the chemical properties of the sympathetic postganglionic neurons in the ganglia of luminescent fishes are target-specific, such as observed in mammals.

Nitric oxide in control of luminescence from hatchetfish (Argyropelecus hemigymnus) photophores.

Nitric oxide synthase-like immunoreactivity (NOS-LI IR) was detected by immunohistochemistry in ventral light organs of the mesopelagic fish, Argyropelecus hemigymnus. Strong NOS-LI IR was present in nerve fibres and in other cells central for production or modulation of light: immunoreactive fibres surrounded the photophores, and were also present in the filter area. Filter cells, particularly in the outer layers, showed strong IR throughout the cytoplasm. Pharmacological studies suggested that nitric oxide (NO) modulates adrenaline-stimulated light emission, and that the modulation is correlated to the ability of the light organ to respond to adrenaline. Adrenaline is known to produce two different types of light response in isolated photophores from Argyropelecus: a slow, long-lasting, high intensity response, or a fast and weak response of short duration. Incubation of photophores in the NO donors sodium nitroprusside or S-nitroso-N-acetylpenicillamine prior to adrenaline stimulation reduced the intensity of the strong and long-lasting type of response, but had little or even a potentiating effect on the weakly responding photophores. Hydroxylamine, which is converted to NO if catalase activity is present in the tissue, reduced the duration and the intensity of the adrenaline response in all tested organs. The NOS-inhibitor L-thiocitrulline potentiated the adrenaline response in the weakly responding organs; the weaker the adrenaline effect, the stronger the potentiation caused by L-thiocitrulline. The strongly responding organs were instead inhibited by L-thiocitrulline. The results suggest that NO has an important role in the control of light emission from Argyropelecus hemigymnus photophores. The cGMP analogue dibutyryl cGMP, the guanylate cyclase inhibitor ODQ and the phosphodiesterase inhibitor pentoxiphylline had no effect, indicating that the NO effect does not involve cGMP.