Paraneurons in the gills and airways of fishes

2015

Severe hypoxia elicits aquatic surface respiration (ASR) behaviour in many species of fish, where ventilation of the gills at the air-water interface improves O 2 uptake and survival. ASR is an important adaptation that may have given rise to air breathing in vertebrates. The neural substrate of this behaviour, however, is not defined. We characterized ASR in developing and adult zebrafish (Danio rerio) to ascertain a potential role for peripheral chemoreceptors in initiation or modulation of this response. Adult zebrafish exposed to acute, progressive hypoxia (P O2 from 158 to 15 mmHg) performed ASR with a threshold of 30 mmHg, and spent more time at the surface as P O2 decreased. Acclimation to hypoxia attenuated ASR responses. In larvae, ASR behaviour was observed between 5 and 21 days postfertilization with a threshold of 16 mmHg. Zebrafish decreased swimming behaviour (i.e. distance, velocity and acceleration) as P O2 was decreased, with a secondary increase in behaviour near or below threshold P O2 . In adults that underwent a 10-day intraperitoneal injection regime of 10 μg g −1 serotonin (5-HT) or 20 μg g −1 acetylcholine (ACh), an acute bout of hypoxia (15 mmHg) increased the time engaged in ASR by 5.5 and 4.9 times, respectively, compared with controls. Larvae previously immersed in 10 μmol l −1 5-HT or ACh also displayed an increased ASR response. Our results support the notion that ASR is a behavioural response that is reliant upon input from peripheral O 2 chemoreceptors. We discuss implications for the role of chemoreceptors in the evolution of air breathing.

Section: Evolutionary Implicationsmentioning

confidence: 99%

Aquatic surface respiration and swimming behaviour in adult and developing zebrafish exposed to hypoxia

Abdallah

Thomas

2015

“…Future studies may reveal whether VAChT cells are innervated, as are NECs, and whether they have a neural or paracrine role in the gill. Closer examination of these cells may also determine whether they should be considered 'paraneurons', which share structural and functional properties of neurons (Fujita, 1989;Zaccone et al, 1997), as do O 2 -sensitive NECs.…”

Section: Vacht-positive Cells Are a Separate Population Of Neurosecrementioning

confidence: 99%

Serotonergic and cholinergic elements of the hypoxic ventilatory response in developing zebrafish

Shakarchi

Zachar

2012

SUMMARYThe chemosensory roles of gill neuroepithelial cells (NECs) in mediating the hyperventilatory response to hypoxia are not clearly defined in fish. While serotonin (5-HT) is the predominant neurotransmitter in O 2 -sensitive gill NECs, acetylcholine (ACh) plays a more prominent role in O 2 sensing in terrestrial vertebrates. The present study characterized the developmental chronology of potential serotonergic and cholinergic chemosensory pathways of the gill in the model vertebrate, the zebrafish (Danio rerio). In immunolabelled whole gills from larvae, serotonergic NECs were observed in epithelia of the gill filaments and gill arches, while non-serotonergic NECs were found primarily in the gill arches. Acclimation of developing zebrafish to hypoxia (P O2 =75mmHg) reduced the number of serotonergic NECs observed at 7days post-fertilization (d.p.f.), and this effect was absent at 10d.p.f. In vivo administration of 5-HT mimicked hypoxia by increasing ventilation frequency (f V ) in early stage (7-10d.p.f.) and late stage larvae (14-21d.p.f.), while ACh increased f V only in late stage larvae. In time course experiments, application of ketanserin inhibited the hyperventilatory response to acute hypoxia (P O2 =25mmHg) at 10d.p.f., while hexamethonium did not have this effect until 12d.p.f. Cells immunoreactive for the vesicular acetylcholine transporter (VAChT) began to appear in the gill filaments by 14d.p.f. Characterization in adult gills revealed that VAChT-positive cells were a separate population of neurosecretory cells of the gill filaments. These studies suggest that serotonergic and cholinergic pathways in the zebrafish gill develop at different times and contribute to the hyperventilatory response to hypoxia. Supplementary material available online at

“…NECs store 5-HT in cytoplasmic synaptic vesicles near the plasma membrane (Fig. 5) and have a morphology and distribution that is highly conserved among fish (Dunel-Erb et al, 1982;Zaccone et al, 1994;Zaccone et al, 1997;Sundin et al, 1998a;Jonz and Nurse, 2003;Saltys et al, 2006;Coolidge et al, 2008). Experiments have demonstrated that gill NECs isolated from zebrafish respond to hypoxia with K + channel inhibition and membrane depolarization, thus confirming their O 2 sensitivity, and a cellular model for O 2 sensing in fish has been proposed where Ca 2+ -dependent release of neurotransmitter results in activation of postsynaptic sensory nerve fibres (Jonz et al, 2004).…”

Section: Role Of Innervation In O 2 Sensingmentioning

confidence: 99%

“…Several studies have indicated that other neurochemical candidates may include nitric oxide or catecholamines (Zaccone et al, 2006;Burleson et al, 2006;Milsom and Burleson, 2007), and a variety of neuropeptides may also be involved (for reviews, see Zaccone et al, 1994;Zaccone et al, 1997). It is conceivable that the neurochemical basis of O 2 sensing in the gill may involve multiple neurotransmitters or neuropeptides and, perhaps, a diversity of excitatory, inhibitory and modulatory mechanisms, as has been described in the mammalian O 2 -sensing organ, the carotid body (González et al, 1994;Nurse, 2005;Prabhakar, 2006;Lahiri et al, 2006).…”

Section: Role Of Innervation In O 2 Sensingmentioning

confidence: 99%

New developments on gill innervation: insights from a model vertebrate

Nurse

2008

SummaryThe fish gill is a highly specialized and complex organ that performs a variety of important physiological functions. In this article, we briefly review the innervation of important structures of the branchial region, such as the gill filaments, respiratory lamellae and pseudobranch, and discuss the physiological significance of this innervation within the context of homeostatic functions of the gill, such as oxygen sensing and ion regulation. Studies in zebrafish utilizing techniques of confocal microscopy and immunolabelling, with specific antibodies against neuronal markers, have recently led to the characterization of innervation patterns in the gills not attained with traditional techniques of histochemistry and electron microscopy. We will discuss the association of putative sensory nerve fibres with O 2 -chemoreceptive neuroepithelial cells and the implications of dual sensory pathways for cardiorespiratory and vascular control. In addition, the idea of the neural control of ion regulation in the gill based on the apparent innervation of mitochondria-rich cells, and the role of innervation in the pseudobranch, will be presented.