Autonomic control of the swimbladder

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Autonomic control of the swimbladder

Frank M. Smith a, Roger P. Croll b,⁎a Department of Anatomy & Neurobiology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 1X5b Department of Physiology & Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada B3H 1X5

a b s t r a c ta r t i c l e i n f o

Article history:Received 17 November 2009Received in revised form 24 June 2010Accepted 2 August 2010

Keywords:ZebrafishTeleostAdrenergicCholinergicPeptidesSwimbladderSmooth muscleVasculatureRete mirabileGas glandBuoyancy

The swimbladder of teleost fishes is the primary organ for controlling whole-body density, and thusbuoyancy. The volume of gas in the swimbladder is adjusted to bring the organism to near neutral buoyancyat a particular depth. Swimbladder morphology varies widely among teleosts, but all species are capable ofinflating and deflating this organ under reflex control by the autonomic nervous system, to achieve neutralbuoyancy. Here we review the control of effectors within the swimbladder, including acid-secreting cells,vasculature and musculature, that are involved in determining gas volume. This control system is complex. Itincorporates the “classical” efferent elements of the autonomic nervous system, the spinal autonomic andcranial autonomic limbs and their neurotransmitters (typically noradrenaline (NA)/adrenaline (ADR), andacetylcholine, respectively), but also non-adrenergic, non-cholinergic neurotransmitters such as peptides,purines and nitric oxide. The detailed patterns of autonomic innervation of swimbladder effectors are notwell understood, nor are the relationships of terminals releasing non-adrenergic, non-cholinergicneurotransmitters onto these effectors. Furthermore, in most cases the complement of postjunctionalreceptor subtypes activated by adrenergic, cholinergic and other neurotransmitters, and the biological effectsof these neurochemicals, have not been completely established. In order to clarify some of these issues and toprovide insight into basic principles underlying autonomic control of swimbladder function, we propose thezebrafish as a potentially useful model teleost.

© 2010 Elsevier B.V. All rights reserved.

1. Introduction

The seeming effortlessness of a fish hovering motionlessly over apatch of coral reef belies themetabolic costs and the complexity of thecontrol mechanisms needed to attain neutral buoyancy in an aquaticenvironment. The majority of body tissues, but particularly skeletaltissues, are denser than the surrounding water (Pelster, 2009).Without buoyancy compensation, fish would sink to the bottom oftheir watery environment and these animals must therefore haveevolved a variety of methods to decrease whole-body density in orderto attain neutral buoyancy. Such mechanisms include the develop-ment of watery muscle, the synthesis of low density lipids, and areduction in bone mass. However, the most energy-efficient mech-anism for approximately half of extant teleosts is the gas-filledswimbladder which adds a relatively large and adjustable internalvolumewith negligible mass. Such swimbladders work well for all butthe most deeply dwelling fish (Alexander, 1966; Pelster, 2009), butthe use of a gas-filled organ presents its own problems. According tothe Combined Gas Law, the volume of a gas changes with bothtemperature and pressure. Temperature-related changes in volumevary proportionally over the Kelvin temperature scale and are

therefore likely negligible over the temperature range of the aquaticenvironment inhabited by most swimbladder-bearing teleosts. Amore significant factor influencing swimbladder volume, however, isdepth-related pressure. A fish may experience many-fold changes inpressure during large vertical migrations through the water columnwhich, if not compensated, cause large changes in the buoyancy of thefish. However, because of the non-linearity of the Combined Gas Lawdue to proportionally increasing pressure changes in shallowerwaters, even variations of a few meters in depth can result insignificant changes in swimbladder volume, causing marked shifts inbuoyancy away from neutral. Thus fish require effective mechanismsfor re-adjusting swimbladder volume as they vary their depth.

The contribution of the swimbladder to buoyancy in teleosts andthe mechanisms for adjusting swimbladder volume have been thesubjects of study in a variety of teleost species over the last 150 years.This work has been reviewed extensively by a number of authors(Harden-Jones and Marshall, 1953; Denton, 1961; Alexander, 1966;Fänge, 1966; Steen, 1970; Fänge, 1976; Blaxter and Tytler, 1978;Fänge, 1983; Alexander, 1993) and more recently by Pelster (1997,2009). Specific aspects of the operation of the swimbladder, includingthe autonomic control of mechanisms influencing its volume, werealso addressed by these reviewers as well as by Nilsson (1983, 2009)and Campbell and McLean (1994). These reviews have providedconcise perspectives on historical and modern advancements in thefield, and it is not our intent here to repeat the breadth of coverage of

Autonomic Neuroscience: Basic and Clinical 165 (2011) 140–148

⁎ Corresponding author.E-mail address: [email protected] (R.P. Croll).

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these works. Instead, our aims are to summarize the physiologicalmechanisms known to be involved in inflation and deflation reflexesgoverning both physostomous and physoclistous swimbladders andto suggest areas where further research should be focused.

2. Functional framework for neural control of swimbladder volume

The regulation of buoyancy can be considered a homeostaticfunction in the broad sense that this process acts to maintain acomponent of the internal milieu of the body (gas volume enclosed inthe swimbladder) at a near-optimal level to attain neutral buoyancyin the face of environmental changes (in this case, moving to a newposition in the water column). In order to achieve homeostasis, theoutflow of the autonomic nervous system is directed to a wide varietyof visceral effector targets, including the swimbladder, to control theinternal milieu by a series of reflexes operating as negative feedbackloops. The morphology of the autonomic nervous system across thevertebrate phyla is considered elsewhere in this volume (Nilsson,2010), so here we will focus on the autonomic control of effectors inthe swimbladder that are involved in regulating its volume.

Swimbladder morphology varies widely among teleosts (i.e.,Harder, 1975) but the function of this organ has been studied indetail in only a few of these species. Nevertheless, the broad outlinesof autonomic control of swimbladder volume have been established.That is, reflex mechanisms controlling effectors in the swimbladdersystem act to inflate or deflate the swimbladder to compensate forchanges in depth. In all teleosts the swimbladder is embryologicallyderived from the gut, yet the function of buoyancy regulation has beenproposed to have evolved secondarily to a respiratory function insome teleost lines (Randall et al., 1981; Berenbrink et al., 2005), so thepatterns of autonomic innervation of the swimbladder may haveparallels with those of the gut or the lung.

The innervation of the teleost gut has been relatively well-studiedthroughout the vertebrates including fishes (reviewed elsewhere inthis volume by Holmgren and Olsson, 2010; Olsson and Holmgren,2010), and while the swimbladder certainly has effector elements incommon with the gut (i.e., smooth muscle, vascularization), special-ized functions in the swimbladder such as the capability for gassecretion are not present in the gut. The lungs of lungfish also havefeatures in common with the swimbladder (i.e., vasculaturized wall,thin epithelium for gas exchange), yet even though the physiology ofgas exchange in lungfishes has been reasonably well studied(reviewed by Perry et al., 2001 and others), there is still a relativepaucity of information about the neurobiology of respiration in thisgroup of fishes (Campbell andMcLean, 1994; Sandblom and Axelsson,2010). Moreover, as with the gut, the gas-secreting components in theswimbladder are not present in the lung.

It is thus clear that, while there are features of effector control thatare common to the teleost gut, lung and swimbladder, as the latterorgan contains components not present in either of the other two, theoverall control of swimbladder function is likely to involve central andperipheral autonomic circuitry specific to this organ. Further, suchcircuitry is likely to be unique to this vertebrate group. Therefore wefeel that principles derived from work on the gut and lung mayprovide only limited insight into the mechanisms involved inswimbladder control, a conclusion that was also reached by Campbelland McLean (1994). This contention is supported by the results ofrecent studies examining the neurobiology of the swimbladder indetail in the succeeding outline.

The general principles of integrative autonomic control of theswimbladder established to date have emerged from analyses of thestructure, physiology, innervation patterns and neural control of theeffectors involved in regulating swimbladder volume in specificteleost models. In the following sections we consider these effectors,their innervation and how these effectors are controlled in reflex-mediated inflation and deflation of the swimbladder. From this basis

we identify the major gaps in our current knowledge of this system,and what experimental models could be used to further investigate it.

3. Inflation of the swimbladder

3.1. Inflation mechanisms common to physostomes and physoclists

After its evagination from the foregut, the swimbladder ofphysostomous fishes remains connected to the gut by a patentpneumatic duct in the adult, as shown in Fig. 1, thus offering one routefor direct exchange of gas with the environment via the esophagus. Inphysoclistous fishes this connection is lost during the developmentalprocess. Transfer of gas, primarily O2, as well as in some cases CO2 andN2, from the bloodstream to the swimbladder lumen is therefore theprimary mechanism for swimbladder inflation in physoclistous fishes,but is also commonly encountered in physostomous fishes. Thisoccurs by passive diffusion across the swimbladder wall fromcapillaries in which there is a higher partial pressure of gas than inthe organ (Steen, 1970). The elements necessary for this process(reviewed by Pelster, 2009 and others) include first, a localmechanism to increase the partial pressure of gas in the bloodstreamabove that in the swimbladder lumen by promoting dissociation of O2

from the hemoglobin; and second, a mechanism for retaining the highpartial pressure of gas within this system by back-diffusion andcountercurrent concentration in the rete mirabile, an organization ofclosely parallel arterial and venous blood vessels associated with theswimbladder (as will be described later). There are thus two generaltargets for neural control of swimbladder inflation based on gastransfer from the bloodstream: activity of the epithelial cells involvedin acidification of the blood, and vasomotion to adjust vascular calibreand thus blood flow in arteries and veins associatedwith the secretoryapparatus and with the rete.

3.1.1. Gas secretionIn the swimbladders of many teleosts, such as goldfish, cod, wrasse

and perch, the specialized secretory cells involved in creating asuitable environment for raising the partial pressure of O2 in thevasculature are located in a circumscribed region of the wall of theswimbladder termed the gas gland (Fänge, 1953, 1983; Nilsson,2009). On the other hand, in other teleosts such as the eel, thesesecretory cells are distributed throughout the epithelium lining theswimbladder (Pelster, 1997, 2009). A broad description of secretoryepithelial cells has been compiled by Fänge (1983) and the histologyand function of these cells has more recently been addressed in detailby Pelster and co-workers in the eel, a physostome, and perch, aphysoclist (Würtz et al., 1999; Prem et al., 2000; eel: Prem and Pelster,

Fig. 1. Swimbladder in a typical cyprinid fish. A: Schematic diagram showing theanterior chamber (AC), posterior chamber (PC), communicating duct (CD) andpneumatic duct (PD) attached to the esophagus (E). B: X-ray of a zebrafish showingthe swimbladder in situ (see Robertson et al. (2008) for details). Scale bar=4 mm.

141F.M. Smith, R.P. Croll / Autonomic Neuroscience: Basic and Clinical 165 (2011) 140–148


2000). Secretory cells are generally polyhedric with a relatively largecytoplasm that contains glycogen deposits and carbonic anhydrase,and are in close proximity to capillaries. These cells are specialized torelease primarily hydrogen ions and lactate into adjacent capillaries tolower the local pH.

The net effect of acidification of the blood adjacent to the secretoryepithelium is to increase the local partial pressure of O2 (PO2) as aresult of offloading from the hemoglobin due to combined Root andBohr effects (Kuhn et al., 1963; summarized by Steen, 1970; Pelster,2009). In addition, the local increase in solute concentration due to ionsecretion causes a decrease in the solubility of O2 as well as of otherblood gases, including N2 and CO2, designated as the “salting-out”effect (see Pelster et al., 1990). Together these mechanisms, alongwith a countercurrent concentration-multiplying system in the retialvasculature associated with the gas gland (as will be discussed later)raise the gas partial pressures high enough in the plasma adjacent tothe epithelium to create a net positive diffusion gradient between theblood and the swimbladder lumen.

Reviews by Nilsson (2009) and Campbell andMcLean (1994) havesummarized what is known of the autonomic control of secretoryepithelial cells in the swimbladder. The consensus appears to be that,at least in some species, the activity of these cells is controlled bycranial autonomic postganglionic fibres. It has long been known thatvagal activity could increase gas gland secretion (Bohr, 1894, quotedby Nilsson, 2009), while atropine, a muscarinic cholinergic antagonist,reduces such activity (Fänge et al., 1976). However, work on the codby Ewart and Driedzic (1990) showed that both adenaline (ADR),released from some spinal autonomic postganglionic nerve terminalsin fishes as well as circulating in the blood (Abrahamsson and Nilsson,1976), and acetylcholine (ACh, the major neurotransmitter releasedfrom cranial autonomic postganglionic terminals) could increaselactate production in the in vitro gas gland. Yet to date there is noconvincing direct evidence of innervation of secretory cells by eitheradrenergic or cholinergic axons. However, innervation of thesecretory region of the gas gland in the wrasse by nerve fibrescontaining vasoactive intestinal polypeptide (VIP) has been demon-strated, and VIP applied to the cod swimbladder increased gassecretion (Lundin and Holmgren, 1991). It is possible that VIP could beco-released from cholinergic terminals (Burnstock, 2002) in theswimbladder but the role of this peptide relative to that of ACh in thecontrol of secretion is as yet uncertain. Furthermore, Olsson andHolmgren (1994) reported the presence of the VIP-related neuro-peptide pituitary adenylate cyclase-activating polypeptide (PACAP)along with VIP in terminals within the swimbladder wall of both codand trout. This peptide has similar functions to VIP, and its co-locationwith the latter peptide in the swimbladder suggests that the role ofPACAP may be complementary to VIP in this organ.

In some physostomes the gas gland is poorly developed or absent(Fänge, 1976). In the zebrafish swimbladder, for instance, there is noidentifiable gross structure resembling the gas gland of other swim-bladders (Finney et al., 2006). It is possible that in the zebrafishswimbladder secretory epithelial cells could be scattered throughoutthe swimbladderwall, as in theeel (Pelster, 1997), but nocellsfitting thedescription of typical secretory cells given previously, were detectedwithin the zebrafish swimbladder system. This finding suggests thatsome species have little or no capacity for gas transfer from the blood tothe swimbladder lumen. In support of this, recent work has confirmedthat adult zebrafish, in which swimbladder volume was artificiallydecreased by exposure to brief negative pressure, did not reinflate theirswimbladders if denied access to surface air for up to 2 wk,whereas fishthat were allowed air access reinflated this organ within a few hours (J.Zeggil, and M.R. Stoyek, unpublished).

3.1.2. Gas gland vasculatureThe rate of transfer of gas from the blood stream into the

swimbladder is critically dependent not only on the acidification of

the blood near the secretory epithelium, but also upon an adequateblood supply to this tissue. Blood enters the swimbladder system fromthe arterial supply via a swimbladder artery branching either from thedorsal aorta or from the mesenteric arterial system (Fänge, 1953).Commonly the swimbladder artery feeds two capillary beds in series.In the first of these, multiple arterial capillaries afferent to the gasgland are arranged in parallel with venous capillaries efferent to thegland, together forming the rete mirabile. In the second vascular bed,downstream of the afferent arterioles of the rete mirabile, capillariesare closely apposed to the secretory epithelial cells where PO2

becomes elevated from the effects of blood acidification (Steen,1970; Fänge, 1983). Blood leaving this bed then courses through theefferent venous capillaries of the rete mirabile. The close apposition ofarterial and venous vessels in the rete mirabile facilitates back-diffusion of gases between efferent venous and afferent arterial blood.The rete mirabile thus functions as a countercurrent concentrationmultiplier for gas recovery as well as recovery of lactate and hydrogenions from blood leaving the gland and is essential in maintaining highvalues of gas partial pressures and low pH within the gland in the faceof a substantial flow of blood through this system. The physiologicalmechanism of countercurrent multiplication underlying the functionof the rete mirabile has been thoroughly investigated (Kuhn et al.,1963; reviewed in Steen, 1970). The anatomy of the rete mirabile ishighly variable among species in terms of length, number anddiameter of retial vessels, and diffusion distance across the arterio-venous endothelia (Steen, 1970; Fänge, 1983), all of which will affectthe efficiency of gas transfer from efferent to afferent vessels.

The major circulatory factor affecting the contribution of the retemirabile to the deposition of O2 into the swimbladder lumen appearsto be the magnitude of blood flow through this structure; for instance,Pelster and Scheid (1992) have shown in the eel that there was adirect correlation not only between epithelial secretory activity andO2 deposition but also between rate of retial blood flow and rate of gastransfer into the lumen. Blood flow to the secretory epithelium can bemodified by exogenously applied adrenergic, cholinergic, peptidergic,nitrergic and purinergic agonists but the effects of these agents arecomplex and not consistent among species. Both noradrenaline (NA)and ADR, found in adrenergic postganglionic terminals in fishes(Abrahamsson and Nilsson, 1976), act at α- and β-adrenergicpostjunctional receptors, and have been implicated in control ofvascular calibre in the rete mirabile and associated blood vessels. In eeland cod swimbladders, ADR, NA and phenylephrine inhibit blood flowvia α-adrenergically-mediated vasoconstriction (Stray-Pedersen,1970; Nilsson, 1972; Pelster, 1994). On the other hand, one or moreof ADR, NA, and the β-adrenergic agonist isoproterenol could evokevasodilation and increased blood flow to the secretory epithelium inthe eel (Stray-Pedersen, 1970; Pelster, 1994). This finding may becontroversial, however, because Schwerte et al (1999) reported thatβ-adrenergic stimulation had no effect on such blood flow in thisspecies. Nilsson (1972) also found a lack of β-adrenergic effects onblood flow in the gas gland of the cod swimbladder.

In physoclists and in some physostomes that are capable of livingat great depths and thus secreting gas at very high pressures into theswimbladder lumen, the rete mirabile is highly developed tomaximizethe number and paralleled length of vessels and to minimize thecalibre of individual vessels (i.e., Fänge, 1976, 1983). These anatomicaladaptations maximize the efficiency of countercurrent concentrationmultiplication of gases within the system. Conversely, in somephysostomes in which gas secretion is reduced (for example, somecyprinids; Fänge, 1983) vascular bundles involved in countercurrentexchange tend to be less well developed. An extreme case is thezebrafish, which may not be capable of gas transfer from thebloodstream to the swimbladder lumen. In this species there appearsto be a vestigial form of rete, consisting of only 4 arterioles and 5venules interleaved in parallel for a length of 1–2 mm, locatedbilaterally on the cranio-lateral aspect of the posterior chamber

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(Fig. 2; Finney et al., 2006). These blood vessels are innervated bytyrosine hydroxylase (TH)-positive varicosities (Fig. 3; Finney et al.,2006; Dumbarton et al., 2010). Furthermore, Dumbarton et al. (2010)reported NA-mediated constriction of swimbladder blood vessels that

was mimicked by the α-adrenergic agonists clonidine and phenyl-ephrine. These responses conform to the general pattern of vascularresponses to adrenergic stimulation reported in the swimbladders ofother teleosts (Nilsson, 1972, 1984; Pelster, 1994). It thus appears

Fig. 2. Autonomic effectors in the zebrafish swimbladder; schematic diagrams show vasculature (A) andmusculature (B). C: Highmagnification views of an artery (Art) and adjacentvein (Vein) revealed by DAB reaction for erythrocyte-bound peroxidase. D: Multiple, small, intensely staining arteries paralleled by less intensely staining veins form a vestigial retemirabile close to the junction of the pneumatic duct and the posterior chamber. E: Patterns of branching of arteries and veins in the microcirculation associated with the lateralmuscle band. Breaks in vessels (arrows) occurred when mounting the swim bladder on the microscope slide. F: Phalloidin-rhodamine staining of muscle at the junction of theesophagus (to the left) with the pneumatic duct (to the right). G: Enlarged view (and rotated approximately 45° clockwise) of striated myocytes in the boxed area in F. H: Smoothmuscle fibres are organized in bands running along each side of the posterior chamber wall. I: Separate layers of circumferential fibres (C-fibres) and longitudinal fibres (L-fibres) inthe lateral muscle band of the posterior chamber. J: The majority of muscle fibres in ventral band of the anterior chamber were oriented circumferentially and were frequentlybundled into overlapping fascicles (brackets). K: Near communicating duct, circumferential fibres (C) of the ventral band of the anterior chamber are interwoven with radial fibres(R). Scale bars=20 μm in C; 75 μm in D; 200 μm in E; 100 μm in F, H; 50 μm in G; 20 μm in I; 50 μm in J and K.Modified from Finney et al. (2006), Dumbarton et al. (2010).



that, even though the countercurrent concentration capability ofthese paralleled vessels may be lost in zebrafish, the autonomiccontrol of blood flow to downstream structures is conserved.

Acetylcholine as well as cholinergic agonists produced consistentvasoconstrictive responses in the gas secretion systems of both thecod (Nilsson, 1972) and the eel (Stray-Pedersen, 1970), so it appearsthat there are cholinergic in addition to adrenergic receptors in thevasculature in this region. Non-adrenergic, non-cholinergic (NANC)neurotransmitters also influence gas gland blood flow and arepresent in swimbladder vascular innervation. VIP, applied exoge-nously to the swimbladder, causes vasodilation of the vasculaturesupplying the gas-secreting tissue in both cod (Lundin and Holmgren,1984) and eel, as does adenosine and nitric oxide-releasing agents inthe latter species (Schwerte et al., 1999). VIP (Lundin and Holmgren,1984; Schwerte et al., 1999) as well as substance P (Lundin andHolmgren, 1984, 1989) have been detected in axon terminalsassociated with the vasculature in the gas-secreting tissues of thecod, eel and other teleosts. VIP, NPY, NADPH-diaphorase, glycine andserotonin-positive terminals have also been found to be associatedwith blood vessels in the zebrafish swimbladder (Finney et al., 2006;Dumbarton et al., 2010).

The effects on blood flow to the gas gland of neurotransmittersreleased by electrically stimulating spinal autonomic and vagalbranches innervating the swimbladder, have been investigated inrelatively few studies. This type of experiment is confounded by thefact that in most vertebrates, at least some branches of the vagusnerve innervating peripheral organs contain adrenergic as well ascholinergic fibres (i.e., Pick, 1970; Nilsson, 1983, 2010), so appropriatepharmacological blockade must be used in conjunction with nervestimulation to dissect cholinergic from adrenergic effects. In the cod,stimulation of branches of both the splanchnic nerve and thevagosympathetic trunk to the swimbladder causes vasoconstriction(Nilsson, 1972; Wahlqvist, 1985), an effect that is mediated by α-

adrenergic receptors (Nilsson, 1972). In the eel, Stray-Pedersen(1970) reported that gas gland blood flow was reduced byvagosympathetic trunk stimulation, a response that was alsoeliminated by α-adrenergic blockade. However, in the same speciesSchwerte et al. (1997) found that stimulation of this nerve evokedvasodilationwithin the rete mirabile, an effect not blocked either byα-or β-adrenergic antagonists, or by atropine, a muscarinic cholinergicantagonist. These authors proposed that neurally induced vasodila-tion in the eel swimbladder was due to the release of one or moreNANC neurotransmitters, as discussed previously.

3.2. Non-secretory inflation mechanisms in physostomes

While many physostomes have the capability for filling theswimbladder with gas transferred from the blood, as describedpreviously, all physostomes so far examined also appear to be able tofill the swimbladder by swallowing air obtained from the surface orfrom gas bubbles in the water column. This process involves acomplex series of steps that includes aspirating gas into the buccalcavity, then forcing it into the rostral esophagus and along thepneumatic duct into the swimbladder (Rieger and Summerfelt, 1998).At each step, the appropriate pressure differences in the passagewaysinvolved must be manipulated to ensure that gas moves toward theswimbladder. This requires coordinated neural control of the mouth,buccal and opercular pumps, contractility of the striated (and possiblysmooth) muscle in the wall of the proximal esophagus, the tension inthe sphincter at the esophagus-pneumatic duct junction (if asphincter is present), contractility of smooth muscle along thepneumatic duct, diameter of the ostium of the pneumatic duct intothe swimbladder, and wall tension in the swimbladder chamber(s).Since striated or smooth myocytes, or both together, may be presentin some of these structures (Finney et al., 2006), both branchiomericmotor innervation and autonomic innervation would be involved in

Fig. 3. Innervation of the zebrafish swimbladder. A: Schematic diagram of overall innervation pattern. B: NADPH-diaphorase activity reveals putative cell bodies (arrowheads)clustered around a blood vessel (BV) in the anterior chamber. C: Similar cell bodies are observed when staining with antibodies against the neural subtype of nitric oxide synthetase(nNOS). D: Varicose neurites exhibiting vasoactive intestinal peptide (VIP)-immunoreactivity are densely distributed in the wall of the anterior chamber. E: Fibres and putative cellbodies exhibit GABA-like immunoreactivity in the anterior chamber. F: Neuropeptide-Y (NPY) immunoreactivity is located in “terminal baskets” surrounding a group of putativecells in the lateral muscle band of the posterior chamber. G: Varicose fibres exhibiting tyrosine hydroxylase (TH) immunoreactivity are often associated with blood vessels but alsolocated throughout the lateral muscle band of the posterior chamber. Scale bars=50 μm in B, C, G; 100 μm in D, E; 30 μm in F.Modified from Finney et al. (2006) and Dumbarton (2008).



their control. However, very little is known about the physiology offilling the swimbladder via the pneumatic duct, let alone its controland coordination by the nervous system.

Yet the importance of this process to physostomous fishes cannotbe denied. In fish such as the zebrafish, which do not seem capable offilling their swimbladders by gas transfer from the blood (Finney et al.,2006), forcing air into the swimbladder via the pneumatic duct is theonly way for inflation to occur. Moreover, if developing zebrafishlarvae (and those of many other species) are prevented fromaccessing air at the surface or in the form of submerged bubbles,these organisms cannot fill the swimbladder and will not developfurther (Goolish and Okutake, 1999).

4. Deflation of the swimbladder

4.1. Deflation mechanisms common to physostomes and physoclists

In swimbladder-bearing teleosts at or near neutral buoyancy, gasin the swimbladder is normally maintained at a pressure aboveambient water pressure (“excess pressure”, Alexander, 1959). There istherefore a net diffusion gradient between the swimbladder lumenand the surrounding tissues. The walls of most swimbladders arerelatively impermeable to gas due to specialized structural compo-nents, such as guanine crystals or parallel arrangements of collagenfibres (Fänge, 1966; Lapennas and Schmidt-Neilsen, 1977) that limitthe rate of gas loss by diffusion through the walls. The small butcontinuous loss of gas via this route would be too slow to constitute areliable form of controlled deflation. All physoclists and somephysostomes, therefore, possess a specialized region of the swim-bladder wall which allows the rapid and controlled resorption of gasfrom the lumen (reviewed by Fänge, 1983, and others).

In the resorptive region, the epithelium is thin and the laminapropria is highly vascularized; both of these features promote therapid diffusion of gas from the swimbladder lumen across theresorptive epithelium and into the venous blood draining theswimbladder. In addition, there are structural and muscular specia-lizations in the swimbladder mucosa associated with the resorptionsite to control the conformation of the epithelium across whichdiffusion occurs, or the accessibility of this epithelium to the gas in thelumen (summarized by Nilsson, 2009). This arrangement thus offerstwo general targets for neural control of resorption: vasomotion of theafferent and efferent resorbing vessels to modify blood flow; andactive adjustment of the access of the exchange epithelium to the gasin the lumen.

In the eel the major site of gas resorption from the swimbladder isthe highly vascularizedwall of the enlarged pneumatic duct (Scheid etal., 1990). Available evidence indicates that the pneumatic duct wall isrelaxed by β-adrenergic stimulation while the wall of the swim-bladder proper is contracted by α-adrenergic receptor activation;together these actions would presumably force gas from the swim-bladder into the pneumatic duct to facilitate resorption (Nilsson andFänge, 1967). In other physoclists the resorptive epithelium is isolatedfrom the gas in the swimbladder lumen either by extensive folds of themucosa at the edges of this epithelium, called the oval, or by adiaphragm separating resorptive and secretory regions. The oval,present in the swimbladder of such species as the toadfish, cod andperch, consists of a circular or oval-shaped mucosal fold containingsmooth muscle in the form of a circumferential sphincter that drawstogether the free edge of the oval over the resorptive epithelium, and aset of radial muscle fibres that act to pull the oval open to expose theepithelium(Fänge, 1976). In the swimbladder of thewrasse a thickenedring of mucosa containing a sphincter of smooth muscle forms adiaphragm closing off the resorptive region from the secretory region(Fänge et al., 1976); this structure is thus functionally equivalent tothe oval.

Smooth muscles of both the diaphragm and the oval appear to beinnervated mainly by adrenergic fibres, and the effects on thesestructures mediated by adrenergic receptors have been demonstratedin studies using both nerve stimulation and exogenous application ofneurochemical agents (comprehensively reviewed by Campbell andMcLean, 1994; Nilsson, 2009). The oval is opened by constriction ofthe radial muscles and relaxation of the circular muscles, mediated byα- and β-adrenergic receptors, respectively. In this structure, there isanatomical evidence of adrenergic innervation of both muscle groups,and electrical stimulation of the vagosympathetic trunk evokedopening of the oval (Nilsson, 1972). There seems to be little or norole for cholinergic control of this function. In the wrasse thediaphragm musculature and that of the mucosa associated with theresorptive epithelium was relaxed by β-adrenergic stimulation(Fänge et al., 1976); these authors also demonstrated the presenceof adrenergic innervation of this musculature. Moreover, ACh causedisolatedmuscle from the resorptive region to contract, but cholinergicinnervation has not yet been demonstrated in this region.

It is clear from the previous discussion that the spinal autonomicoutflow, operating through both α- and β-adrenergic receptorsdifferentially distributed on the effectors involved, plays a majorrole in deflation by controlling gas transfer between the swimbladderand the circulation in those teleosts in which this issue has beenstudied. However, the role of the cranial autonomic outflow in thecontrol of deflation remains obscure.

4.2. Deflation mechanisms in physostomes

In teleosts in which the chief mechanism for deflation is by passageof gas along the pneumatic duct, the major control point formaintaining internal gas pressure is likely a sphincter or constrictionat the pneumatic duct-esophageal junction (Fig. 1). There may also beother restriction sites within the swimbladder system, such as thecommunicating duct between the anterior and posterior chambersthat are found in the cyprinid swimbladder, where gas passagemay becontrolled. Thus, in order to empty the swimbladder, one or more ofthese restrictions must be opened to allow the escape of gas.

In addition to opening the appropriate gas passages, the pressurein the swimbladder lumen must be higher than the ambientenvironmental pressure in order for gas to leave the system. Insome cyprinid species in which internal swimbladder pressure hasbeen measured directly or estimated, this pressure is higher than theambient pressure; for instance, Alexander (1959) showed thatswimbladder pressure can exceed ambient pressure by up to100 mm Hg. However, not all physostomes have such a high excesspressure; for example, Robertson et al. (2008) found an excesspressure of only +8 mm Hg in the zebrafish swimbladder, so in somespecies the pressure within the lumen may need to be increasedactively to expel gas from the swimbladder. Most physostomes havesmooth muscle in at least a portion of the swimbladder wall(Alexander, 1966), and presumably contraction of this musculaturecan generate enough internal pressure to force gas along thepneumatic duct after this duct and its associated restrictions arerelaxed. Both the patency of restrictions (assuming there aresphincters or other arrangements of musculature in nearby structuresfor controlling diameter) and tension in swimbladder wall muscula-ture can be controlled by the autonomic nervous system. Deflation ofthe swimbladder would thus involve relaxation of smooth muscle atrestriction sites but increased contractility of muscle fibres in theswimbladder wall to raise its tension. Such complex differentialcontrol presumably requires diverse receptor types on the muscula-ture and a high degree of coordination of autonomic outflow to theseeffectors, but little is known to date of the function of the effectorsresponsible for active expulsion of gas from the physostomeswimbladder, or the autonomic control of such effectors.



Recent work, however, has begun to address these issues byexploiting the zebrafish, in which the expulsion of gas through thepneumatic duct appears to be the chief mechanism of swimbladderdeflation. A large concentration of striated and smooth muscle fibresis located at the junction of the pneumatic duct with the esophagus,likely acting as a sphincter to regulate passage of gases in and out ofthe entire swimbladder system (Fig. 2; Finney et al., 2006). This regionis innervated by cholinergic axons, revealed by choline acetyltrans-ferase (ChAT)-like immunoreactivity, showing terminals associatedwith myocytes. It is presently unclear, however, whether striated orsmooth muscle fibres or both are cholinergically innervated in thisregion; it is conceivable that striated myocytes may be underbranchiomeric control while smooth muscle may be governed bycranial autonomic postganglionic axons. Nevertheless, such innerva-tion is likely to play an important role in the control of gas passage byconstricting the gateway to the swimbladder system in this species.Moreover it is interesting to note in the context of cholinergicinnervation of this system that, in the zebrafish, such innervationappeared to be confined to the sphincter region alone since no ChAT-positive axons were detected elsewhere in the swimbladder (Finneyet al., 2006).

In addition to the muscle fibres at the junction of the pneumaticduct and esophagus, other muscles are present in the wall of theswimbladder and the organization of the myocytes appears to beconsistent with the capacity for controlling volume by “burping” gasout of the swimbladder system via the pneumatic duct, esophagus andmouth (the “gasspuckreflex”, see Fänge, 1976 and others). Bands ofsmooth muscle are present along lateral aspects of the posteriorchamber and the ventral aspect of the anterior chamber in thezebrafish (Fig. 2; Finney et al., 2006; Robertson et al, 2007; Dumbartonet al., 2010). These muscles are mostly oriented circumferentially sothat when they contract the diameter of the swimbladder woulddecrease. Furthermore, Dumbarton et al. (2010) also found a series ofregular corrugations in the walls of both chambers of the zebrafishswimbladder, oriented parallel to the long axis of the chambers andorthogonally to the majority of the muscle fibres and proposed thatthese act as accordion folds which permit small changes in the tone ofthe swimbladder muscle to accommodate relatively large changes inswimbladder volume by adjusting wall tension.

There are also longitudinally oriented fibres in the muscle bands ofboth chambers in the zebrafish swimbladder as well as fibres orientedradially near the ends of the chambers (Fig. 2; Finney et al., 2006;Robertson et al., 2007; Dumbarton et al., 2010). Presumably contrac-tions of these longitudinal and radial fibres are coordinated to prevent“ballooning” of the ends of the swimbladder upon contraction of thecircumferential fibres. Moreover the radial fibres in the chamber wallsadjacent to the communicating duct connecting the two chambers(Fig. 2) may also be involved in controlling the patency of this duct.

Tyrosine hydroxylase-positive axons were abundant over the fullextent of the lateral muscle bands of the posterior chamber (Fig. 3;Finney et al., 2006; Dumbarton et al., 2010) and in musculature on theventral aspect of the anterior chamber (Finney et al., 2006;Dumbarton et al., 2010) of the zebrafish swimbladder. These findingsstrongly suggest that at least a portion of the musculature of theswimbladder is under adrenergic control. This is in fact the case;Dumbarton et al. (2010) have demonstrated that application of NAcauses contraction of smooth muscle of the anterior chamber in bothin vitro preparations of isolated tissue rings and in the whole zebrafishswimbladder in situ. In the latter experiments, muscle contractionresulted in a significant decrease in anterior (but not posterior)chamber volume (shown in Fig. 4) and the passage of gas out of thepneumatic duct. The effects of NA on the anterior chamber weremimicked by isoproterenol and blocked by timolol, a general β-adrenergic antagonist widely used in studies of mammalian adrenor-eceptor function. While the efficacy of the latter agent has not beenextensively investigated in fishes, studies in the trout heart (Gamperl

et al., 1994) and tilapia adipocytes (Vianen et al., 2002) have shownthat it is a potent piscine β-adrenergic antagonist. The finding that β-adrenergic stimulation can drive swimbladder deflation in thezebrafish is novel, but it is as yet unclear how activation of thisreceptor subtype elicits smooth muscle contraction in this organ.

5. Concluding remarks: emerging concepts in neural regulation ofswimbladder volume

In this review we have dissected the swimbladder system into themajor components in which autonomic regulation of volume has beeninvestigated. The swimbladder takes a wide variety of forms amongteleosts and from the previous discussion it is clear that the neuralcontrol of inflation and deflation of this organ may exhibit as muchdiversity in innervation pattern, variety of neurotransmitters in-volved, and effects of these on target tissues as do the swimbladdersthemselves. There is broad consensus that the cranial autonomic(parasympathetic) innervation facilitates swimbladder inflation,while the primary role of the spinal autonomic (sympathetic)innervation is in deflation. However, there is also evidence ofcholinergic involvement in deflation and adrenergic involvement ininflation in some species, so the boundaries of influence of theseautonomic divisions on the swimbladder are not yet clear. Theseautonomic limbs have traditionally been considered to operateantagonistically; that is, when one limb is active the other iswithdrawn. However the balance of recent anatomical, neurochem-ical and physiological evidence indicates that autonomic control of theswimbladder effectors is much more likely to operate cooperativelyand synergistically rather than antagonistically.

The classical model of peripheral autonomic pathways controllingthe viscera through simple pre- to postganglionic relays, segregatedinto cranial and spinal outflow pathways, was formulated by Langley(1921) and Cannon (1915). In this model the traditional autonomic

Fig. 4. Application of norepinephrine (NE) to in situ swimbladder evokes smoothmuscle contractions in anterior chamber that reduced volume and increased pressure.A: Left lateral view of swimbladder before application of NE (dorsal is upward andcranial to the left). The outlines of the anterior (AC) and posterior (PC) chambers areindicated by dotted lines. B: Same specimen as in A, after exposure to NE (10−5 M,10 min in bath perfusate). Changes in the outline of the anterior chamber (to arrows)from the control outline (dotted line as in A) indicate that NE application decreased thechamber volume. Posterior chamber shifted position (indicated by arrowheads) but didnot change its volume during NE exposure. Scale bar: 1 mm.Modified from Dumbarton (2008) and Dumbarton et al. (2010).



neurotransmitters ACh and NA/ADR, released from cranial and spinalneuroeffector junctions, activate the visceral effector targets. Some ofthe studies of swimbladder control have focused on the effects of thetraditional neurotransmitters on targets in this organ, in the beliefthat mechanisms of buoyancy regulation by the autonomic nervoussystemmay be explained by determining the pharmacological actionsof these neurotransmitters. However, in the last three decades ourunderstanding of the organization of the peripheral autonomicnervous system has greatly advanced. Investigations using modernanatomical and electrophysiological techniques have shown thatneurons in peripheral autonomic ganglia integrate afferent informa-tion from multiple sources, communicate with each other, andexpress a wide variety of neurotransmitters and neuromodulators(Jänig, 2006; Jänig and McLachlan, 1992). In the swimbladder,virtually all recent studies of autonomic function have foundadditional layers of complexity not accounted for by the classicalrelay model. The presence of adrenergic postganglionic axons in thevagal rami coursing to the swimbladder is but one example of this.

Furthermore, there are numerous reports of NANC neurotrans-mitters in autonomic nerve terminals throughout the swimbladder.The presence of these neurochemicals constitutes an as yet poorlyunderstood aspect of this control system. Given the diversity of NANCneurotransmitters known to be co-localized in postganglionicneurons of both the spinal and cranial autonomic systems throughoutthe vertebrates (Nilsson, 2010), there is a strong likelihood that therelease of the traditional autonomic neurotransmitters NA, ADR orAChmay not in fact be the primary function of some of these neurons.Furthermore, in all vertebrate groups, some subpopulations ofperipheral autonomic neurons have been identified that do notcontain the traditional autonomic postganglionic neurotransmitters.For instance, in the swimbladder, Finney et al. (2006) and others haveshown that some peptidergic axons innervating the swimbladderconstitute a different subpopulation, and are differentially distributedwithin the organ, than axons containing ACh or NA/ADR. These resultsstrongly support the concept of diverse, neurochemically-identifiableand function-specific neural control pathways within the vertebrateviscera (Jänig and McLachlan, 1992; Morrison, 2002; Jänig, 2006).

In comparison with mammals, fishes remain underinvestigated inthe area of receptor diversity at the neuroeffector junctions and atsynapses in the peripheral autonomic nervous system. Within theswimbladder, the variety of postjunctional receptor subtypes foundfor each of the neurotransmitters is large and still growing as the fieldprogresses. The fact that just one neurochemical can have a widerange of postjunctional effects, coupled with the potential for co-release of two or more neurochemicals from a single autonomicterminal, makes the possibilities for autonomic activation of effectorsor modulation of their activity in the swimbladder system very largeindeed.

We therefore believe that the pool of neurons innervating theteleost swimbladder should be considered as a heterogeneous butintegrated population dedicated to controlling local, regional andglobal aspects of swimbladder volume through neurochemicallycoded, function-specific pathways that target particular groups ofeffectors within the swimbladder system. Such a model opens thepossibilities of interactions between transmitters released fromdifferent types of neuroeffector junctions at the targets, along withintegrative effects of anatomical connections between postganglionicefferent neurons cross-talking at the level of their ganglia.

Still, the organizational details of the neuroanatomical substratesfor control of swimbladder volume remain obscure for any species sofar investigated. New techniques such as advanced immunohisto-chemistry, confocal microscopy and innovations in neural pathwaytracing are beginning to be applied to neuroanatomical studies ofswimbladder innervation. These studies are essential in laying thegroundwork for further analysis of the neurophysiological andpharmacological properties of these neurons. Furthermore, an

understanding of the neuroanatomical substrate of this system willhelp design new experiments to investigate the neuroeffectormechanisms responsible for adjusting swimbladder volume. In thiscontext, work in cyprinid physostomes such as the zebrafish andgoldfish, and perhaps in small physoclistous fishes such as medaka orkillifish, where the swimbladders are small and relatively accessiblefor experimental manipulation and visualization, should providerapid advancement of the field. The use of these model laboratoryspecies should also permit insights into the development of neuralcontrol of buoyancy during ontogeny, a topic which has only garnereda small amount of attention to date (Robertson et al., 2007; Lindseyet al., 2009).

In conclusion, there is no doubt that swimbladder volume iscontrolled by the autonomic nervous system to regulate buoyancy,and possibly the pitch of the body relative to the horizontal plane, aspart of the constellation of autonomic control mechanisms acting tomaintain homeostasis. As we have outlined previously, within theswimbladder tissues the effector cells concerned with alteringvolume, and some of their basic mechanisms of neural control, arereasonably well understood. Yet we still do not fully understand themost basic neuroanatomy of even the efferent arcs of the reflexesproposed by Fänge and others more than 50 years ago to driveinflation and deflation of this organ. Moreover little is known of thesources of afferent drive for these reflexes, nor of the central circuitrygoverning efferent outflow to the swimbladder. What is obvious isthat coordinating the balance of activities of effectors for inflation anddeflation is a very complex task, requiring neural circuitry of muchgreater sophistication than the classical model of autonomic efferentcontrol encompasses. Elucidating the details of the neuroanatomicalsubstrates for function-specific pathways within the swimbladder inselected teleost species will represent a significant advance inunderstanding fundamental principles of organization of the neuralnetwork engaged in regulating buoyancy. It is our belief that suchprinciples will be applicable not only to control of the broad variety ofteleost swimbladders, but will also help clarify some generalprinciples underlying organ-dedicated control systems that haveevolved to maintain homeostasis throughout the vertebrates.

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