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Control of Breathing in Invertebrate Model Systems

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Abstract

The invertebrates have adopted a myriad of breathing strategies to facilitate the extraction of adequate quantities of oxygen from their surrounding environments. Their respiratory structures can take a wide variety of forms, including integumentary surfaces, lungs, gills, tracheal systems, and even parallel combinations of these same gas exchange structures. Like their vertebrate counterparts, the invertebrates have evolved elaborate control strategies to regulate their breathing activity. Our goal in this article is to present the reader with a description of what is known regarding the control of breathing in some of the specific invertebrate species that have been used as model systems to study different mechanistic aspects of the control of breathing. We will examine how several species have been used to study fundamental principles of respiratory rhythm generation, central and peripheral chemosensory modulation of breathing, and plasticity in the control of breathing. We will also present the reader with an overview of some of the behavioral and neuronal adaptability that has been extensively documented in these animals. By presenting explicit invertebrate species as model organisms, we will illustrate mechanistic principles that form the neuronal foundation of respiratory control, and moreover appear likely to be conserved across not only invertebrates, but vertebrate species as well. © 2012 American Physiological Society. Compr Physiol 2:1745‐1766, 2012.

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Figure 1. Figure 1.

The respiratory orifice, or “pneumostome,” of a common terrestrial slug, Arion rufus. The orifice is a muscular opening to the mantle cavity, the rudimentary lung where respiratory gas exchange occurs. A magnified image of the pneumostome (PN) is shown in the insert on the left, and is in the open state. When open, ambient air can be exchanged with mantle cavity air. The respiratory control system of the animal regulates the motor control over the opening and closing of the pneumostome, as well as the contraction and relaxation of the respiratory “pump” muscles in the mantle cavity walls.

Modified, with permission, from an original public domain image available from Wikimedia Commons (URL: http://upload.wikimedia.org/wikipedia/commons/9/9c/Arion_sp.jpg).
Figure 2. Figure 2.

SEM images showing the book lung structures in representative species of scorpions. (A) The book lungs reside on the inner surface of the ventral exoskeleton in the mesosoma. Pairs of book lungs are situated laterally on the sternites of the third to sixth visible opisthosomal segments. The particular species shown here is Broteochactas delicatus. (B) Each book lung has an opening called a spiracle present on the posteromedial margin of the book lung. This opening ranges from a slit‐like shape to an almost round opening, and controls air movement into and out of the atrium of the lung. This lung was observed in the species Brotheas granulatus.

Images taken with courtesy of The American Museam of Natural History. Originally appear as Figures and in Kamenz & Prendini ().
Figure 3. Figure 3.

Anatomy of the book lung organs. (A) Diagrammatic representation of a longitudinal histological section through the book lung. (B) SEM image of the surface of a book lung lamella viewed from airspace (scorpione species Centruroides exilicauda). A reticulate vein is indicated by the arrow that is directed to distal lamellar edge. (C) An SEM image showing the smooth distal edges of book lung lamellae (arrow) in the same species, from a posterior view.

Images taken with courtesy of the American Museum of Natural History. Originally appear as Figure 1A, and Plate 13 (B and C) in Kamenz & Prendini ().
Figure 4. Figure 4.

The fruit fly Drosophila melanogaster and the spiracular openings that gate the interface between atmospheric air and the tracheal system. In A, mesothoracic spiracles 1 and 2 are indicated (sp1 and sp2). The abdominal spiracles sp3 to 9 are also shown. B shows a scanning electron microscopic image of Drosophila and the anatomical position of the mesothoracic spiracles. The anterior spiracle (sp1) lies between propleura and mesopleura. The posterior spiracle sp2 is located between the basis of the haltere and the mesomera. C and D show the shape and size of the spiracle opening areas of sp1 and sp2, respectively. The metathoracic spiracle opening area is approximately 26% larger than the mesothoracic spiracle opening area. Values are means ± SD, N = 10 flies.

Figure and data with courtesy of The Company of Biologists 2006, originally published as Figure in Heymann and Lehmann. See reference (85).
Figure 5. Figure 5.

The insect tracheal system captured using phase‐contrast x‐ray imaging. (A) A high‐resolution composite image of the Carabid beetle, Pterostichus stygicus, viewed from the dorsoventral perspective, sacrificed and legs removed prior to imaging. The air‐filled tubes of the tracheal system can be clearly visualized. (B) A closeup view of one section of the prothorax, showing detail of the tracheal system and the branching pattern of individual tracheae. (C, D) Still frames from actual real‐time breathing activity over one half‐cycle of rhythmic tracheal collapse in a live carabid beetle (Platynus decentis) in the dorsoventral view. Time interval is 0.5 s. Total time of collapse and reinflation of the tubes is 1.0 s. The tracheal system clearly transition between collapsed (D) and expanded (C) states. This repeated breathing cycle actively pumps air through the air conduction system of the animal. Scale bars: A,B, 1 mm; C,D, 200 μm.

Images taken with courtesy of Socha et al. (2007), and originally appears in Figure of Socha et al. (), BMC Biol. 5:6.
Figure 6. Figure 6.

An image of the central ring ganglia of the brain from an air breathing fresh water pond snail, Lymnaea stagnalis. The image of the dorsal aspect of the brain was taken using a standard light microscope viewed at a combined 40× magnification. In this picture, the individual neuron cell bodies are clearly visible and can be individually discerned. The unique size and coloration and anatomical locations make many cells readily identifiable. The size of the cells also makes them incredibly amenable to electrophysiological investigation and experimental manipulation.

Figure 7. Figure 7.

The identified central respiratory interneuron 378, which is located in the suboesophageal ganglion of the flying insect Locusta migratoria. (A) A camera lucida drawing of the interneuron 378 as revealed using Lucifer yellow dye filling. The interneuron has a cell body on the anterior labial neuromere and a contralateral axon descending at least into the mesothoracic ganglion. (B) An intracellular recording from interneuron 378, showing that the cell is activated in phase with the electromyograph activity observed in the abdominal expiratory pump muscle 179. During intense ventilation, the peak activity in 378 coincided with the onset of expiratory muscle activity.

Figure taken with courtesy of the American Physiological Society. Originally appears in Ramirez (1998), J Neurophysiol 80:3137‐3147, as Figure , Panels A and B.
Figure 8. Figure 8.

A peripheral sensory organ in Lymnaea stagnalis. A shows the osphradium (Os) and its connecting nerve, the internal right parietal nerve (IrPn), are discernible from outside the animal through the thin layer of skin (removed for clarity) that partitions the internal organs from the external environment. The Os is situated adjacent to the respiratory orifice, the pneumostome (PN). Removing a thin layer of skin uncovers the Os, osphradial nerve (Osn) and IrPn. (B) The semi‐intact preparation was composed of the central ring ganglia, Os with surrounding PN tissue, and nerves joining the two structures. Note that the surrounding tissue was removed in this image for clarity. The insert shows the Os at a higher magnification.

Figure taken with courtesy of Wiley‐Blackwell (2007). Panels originally appear in Figure of Bell et al., reference (12).
Figure 9. Figure 9.

The inhibitory effect of a whole‐body withdrawal interneuron (RPeD11) on respiratory activity in Lymnaea stagnalis. In A, the spontaneously occurring respiratory rhythm as recorded from RPeD1, VJ, and VD4 is illustrated. The electrical stimulation of RPeD11 (bottom trace) interrupted the respiratory cycle in the middle of the expiratory phase (IP3I failed to induce its effects on the target RPeD1, VD4, and VJ cells). As a consequence, VD4 failed to fire and the respiratory rhythm was briefly terminated. Note that the subsequent episode of IP3I activity also failed to activate VD4. However, normal respiratory activity is resumed in the next cycle. In B, the termination of the respiratory rhythmic activity by RPeD11 is illustrated. Repeated stimulation of RPeD11 in an isolated central nervous system (CNS) preparation terminated the respiratory rhythmic activity as recorded from the interneurons RPeD1 and VD4 and a motor neuron VJ cell. RPeD11 was stimulated twice with an interval of 15 to 20 s.

Figure taken with courtesy of The Company of Biologists Ltd. (1996). Originally appears as Figure of Inoue et al. ().


Figure 1.

The respiratory orifice, or “pneumostome,” of a common terrestrial slug, Arion rufus. The orifice is a muscular opening to the mantle cavity, the rudimentary lung where respiratory gas exchange occurs. A magnified image of the pneumostome (PN) is shown in the insert on the left, and is in the open state. When open, ambient air can be exchanged with mantle cavity air. The respiratory control system of the animal regulates the motor control over the opening and closing of the pneumostome, as well as the contraction and relaxation of the respiratory “pump” muscles in the mantle cavity walls.

Modified, with permission, from an original public domain image available from Wikimedia Commons (URL: http://upload.wikimedia.org/wikipedia/commons/9/9c/Arion_sp.jpg).


Figure 2.

SEM images showing the book lung structures in representative species of scorpions. (A) The book lungs reside on the inner surface of the ventral exoskeleton in the mesosoma. Pairs of book lungs are situated laterally on the sternites of the third to sixth visible opisthosomal segments. The particular species shown here is Broteochactas delicatus. (B) Each book lung has an opening called a spiracle present on the posteromedial margin of the book lung. This opening ranges from a slit‐like shape to an almost round opening, and controls air movement into and out of the atrium of the lung. This lung was observed in the species Brotheas granulatus.

Images taken with courtesy of The American Museam of Natural History. Originally appear as Figures and in Kamenz & Prendini ().


Figure 3.

Anatomy of the book lung organs. (A) Diagrammatic representation of a longitudinal histological section through the book lung. (B) SEM image of the surface of a book lung lamella viewed from airspace (scorpione species Centruroides exilicauda). A reticulate vein is indicated by the arrow that is directed to distal lamellar edge. (C) An SEM image showing the smooth distal edges of book lung lamellae (arrow) in the same species, from a posterior view.

Images taken with courtesy of the American Museum of Natural History. Originally appear as Figure 1A, and Plate 13 (B and C) in Kamenz & Prendini ().


Figure 4.

The fruit fly Drosophila melanogaster and the spiracular openings that gate the interface between atmospheric air and the tracheal system. In A, mesothoracic spiracles 1 and 2 are indicated (sp1 and sp2). The abdominal spiracles sp3 to 9 are also shown. B shows a scanning electron microscopic image of Drosophila and the anatomical position of the mesothoracic spiracles. The anterior spiracle (sp1) lies between propleura and mesopleura. The posterior spiracle sp2 is located between the basis of the haltere and the mesomera. C and D show the shape and size of the spiracle opening areas of sp1 and sp2, respectively. The metathoracic spiracle opening area is approximately 26% larger than the mesothoracic spiracle opening area. Values are means ± SD, N = 10 flies.

Figure and data with courtesy of The Company of Biologists 2006, originally published as Figure in Heymann and Lehmann. See reference (85).


Figure 5.

The insect tracheal system captured using phase‐contrast x‐ray imaging. (A) A high‐resolution composite image of the Carabid beetle, Pterostichus stygicus, viewed from the dorsoventral perspective, sacrificed and legs removed prior to imaging. The air‐filled tubes of the tracheal system can be clearly visualized. (B) A closeup view of one section of the prothorax, showing detail of the tracheal system and the branching pattern of individual tracheae. (C, D) Still frames from actual real‐time breathing activity over one half‐cycle of rhythmic tracheal collapse in a live carabid beetle (Platynus decentis) in the dorsoventral view. Time interval is 0.5 s. Total time of collapse and reinflation of the tubes is 1.0 s. The tracheal system clearly transition between collapsed (D) and expanded (C) states. This repeated breathing cycle actively pumps air through the air conduction system of the animal. Scale bars: A,B, 1 mm; C,D, 200 μm.

Images taken with courtesy of Socha et al. (2007), and originally appears in Figure of Socha et al. (), BMC Biol. 5:6.


Figure 6.

An image of the central ring ganglia of the brain from an air breathing fresh water pond snail, Lymnaea stagnalis. The image of the dorsal aspect of the brain was taken using a standard light microscope viewed at a combined 40× magnification. In this picture, the individual neuron cell bodies are clearly visible and can be individually discerned. The unique size and coloration and anatomical locations make many cells readily identifiable. The size of the cells also makes them incredibly amenable to electrophysiological investigation and experimental manipulation.



Figure 7.

The identified central respiratory interneuron 378, which is located in the suboesophageal ganglion of the flying insect Locusta migratoria. (A) A camera lucida drawing of the interneuron 378 as revealed using Lucifer yellow dye filling. The interneuron has a cell body on the anterior labial neuromere and a contralateral axon descending at least into the mesothoracic ganglion. (B) An intracellular recording from interneuron 378, showing that the cell is activated in phase with the electromyograph activity observed in the abdominal expiratory pump muscle 179. During intense ventilation, the peak activity in 378 coincided with the onset of expiratory muscle activity.

Figure taken with courtesy of the American Physiological Society. Originally appears in Ramirez (1998), J Neurophysiol 80:3137‐3147, as Figure , Panels A and B.


Figure 8.

A peripheral sensory organ in Lymnaea stagnalis. A shows the osphradium (Os) and its connecting nerve, the internal right parietal nerve (IrPn), are discernible from outside the animal through the thin layer of skin (removed for clarity) that partitions the internal organs from the external environment. The Os is situated adjacent to the respiratory orifice, the pneumostome (PN). Removing a thin layer of skin uncovers the Os, osphradial nerve (Osn) and IrPn. (B) The semi‐intact preparation was composed of the central ring ganglia, Os with surrounding PN tissue, and nerves joining the two structures. Note that the surrounding tissue was removed in this image for clarity. The insert shows the Os at a higher magnification.

Figure taken with courtesy of Wiley‐Blackwell (2007). Panels originally appear in Figure of Bell et al., reference (12).


Figure 9.

The inhibitory effect of a whole‐body withdrawal interneuron (RPeD11) on respiratory activity in Lymnaea stagnalis. In A, the spontaneously occurring respiratory rhythm as recorded from RPeD1, VJ, and VD4 is illustrated. The electrical stimulation of RPeD11 (bottom trace) interrupted the respiratory cycle in the middle of the expiratory phase (IP3I failed to induce its effects on the target RPeD1, VD4, and VJ cells). As a consequence, VD4 failed to fire and the respiratory rhythm was briefly terminated. Note that the subsequent episode of IP3I activity also failed to activate VD4. However, normal respiratory activity is resumed in the next cycle. In B, the termination of the respiratory rhythmic activity by RPeD11 is illustrated. Repeated stimulation of RPeD11 in an isolated central nervous system (CNS) preparation terminated the respiratory rhythmic activity as recorded from the interneurons RPeD1 and VD4 and a motor neuron VJ cell. RPeD11 was stimulated twice with an interval of 15 to 20 s.

Figure taken with courtesy of The Company of Biologists Ltd. (1996). Originally appears as Figure of Inoue et al. ().
References
 1. Abdala APL, Rybak IA, Smith JC, Zoccal DB, Machado BH, St‐John WM, Paton JFR. Multiple pontomedullary mechanisms of respiratory rhythmogenesis. Resp Physiol Neurobiol 168: 19‐25, 2009.
 2. Alevizos A, Weiss K, Koester J. Synaptic actions of identified peptidergic neuron R15 in Aplysia. I. Activation of respiratory pumping. J Neurosci 11: 1263‐1274, 1991.
 3. Anderson JF, Prestwich KN. Respiratory gas exchange in spiders. Physiol Zool 55: 72‐90, 1982.
 4. Baker‐Herman TL, Mitchell GS. Phrenic long‐term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 22: 6239‐6246, 2002.
 5. Baker FC. The ecology of north american Lymneide. Science 49: 519‐521, 1919.
 6. Barra J‐A, Pequeux A, Humbert W. A morphological study on gills of a crab acclimated to fresh water. Tiss Cell 15: 583‐596, 1983.
 7. Batang ZB, Suzuki H, Miura T. Gill‐cleaning mechanisms of the burrowing mud shrimp Laomedia astacina (Decapoda, Thalassinidea, Laomediidae). J Crust Biol 21: 873‐884, 2001.
 8. Bavis RW, Mitchell GS. Long‐term effects of the perinatal environment on respiratory control. J Appl Physiol 104: 1220‐1229, 2008.
 9. Bedford JA, Lutz PL. Respiratory physiology of Aplysia Californica (J.E. Morton & C.M. Yonge, 1964) and Aplysia brasiliana (J.E. Morton & C.M. Yonge, 1964) upon aerial exposure. J Exp Mar Biol Ecol 155: 239‐248, 1992.
 10. Bekius R. The circulatory system of Lymnaea stagnalis (L.). Neth J Zool 22: 1‐58, 1972.
 11. Bell HJ. Respiratory control at exercise onset: An integrated systems perspective. Respir Physiol Neurobiol 152: 1‐15, 2006.
 12. Bell HJ, Inoue T, Shum K, Luk C, Syed NI. Peripheral oxygen‐sensing cells directly modulate the output of an identified respiratory central pattern generating neuron. Eur J Neurosci 25: 3537‐3550, 2007.
 13. Benjamin PR. Interneuronal network acting on snail neurosecretory neurons (yellow cells and yellow‐green cells of Lymnaea). J Exp Biol 113: 165‐185, 1984.
 14. Benjamin PR, Winlow W. The Distribution of 3 wide‐Acting synaptic inputs to identified neurons in the isolated brain of Lymnaea stagnalis (L). Comp Biochem Physiol A 70: 293‐307, 1981.
 15. Bergmiler E, Bielawski J. Role of the gills in osmotic regulation in the crayfish Astacus leptodactylus Esch. Comp Biochem Physiol A 37: 85‐91, 1970.
 16. Bill RG, Thurberg FP. Coughing: A new description of ventilatory reversals produced by the lobster, Homarus americanus. Comp Biochem Physiol A 80: 333‐336, 1985.
 17. Bradley TJ. Discontinuous ventilation in insects: Protecting tissues from O2. Respir Physiol Neurobiol 154: 30‐36, 2006.
 18. Brundage CM, Taylor BE. Neuroplasticity of the central hypercapnic ventilatory response: Teratogen‐induced impairment and subsequent recovery during development. Dev Neurobiol 70: 726‐735, 2010.
 19. Burrows M. Coordinating interneurones of locust which convey 2 patterns of motor commands ‐ their connections with ventilatory motoneurons. J Exp Biol 63: 735‐753, 1975.
 20. Burrows M. Interneurones coordinating the ventilatory movements of the thoracic spiracles in the locust. J Exp Biol 97: 385‐400, 1982.
 21. Bush BMH, Simmers AJ, Pasztor VM. Neural control of gill ventilation in decapod crustacea. In: Taylor EW, editor. The Neurobiology of the Cardiorespiratory System. Manchester: Manchester University Press, 1987, p. 80‐112.
 22. Bustami HP, Harrison JF, Hustert R. Evidence for oxygen and carbon dioxide receptors in insect CNS influencing ventilation. Comp Biochem Physiol A Mol Integr Physiol 133: 595‐604, 2002.
 23. Bustami HP, Hustert R. Typical ventilatory pattern of the intact locust is produced by the isolated CNS. J Insect Physiol 46: 1285‐1293, 2000.
 24. Byrne J, Castellucci V, Kandel ER. Receptive fields and response properties of mechanoreceptor neurons innervating siphon skin and mantle shelf in Aplysia. J Neurophysiol 37: 1041‐1064, 1974.
 25. Byrne JH. Identification and initial characterization of a cluster of command and pattern‐generating neurons underlying respiratory pumping in Aplysia californica. J Neurophysiol 49: 491‐508, 1983.
 26. Byrne JH, Castellucci VF, Carew TJ, Kandel ER. Stimulus‐response relations and stability of mechanoreceptor and motor neurons mediating defensive gill‐withdrawal reflex in Aplysia. J Neurophysiol 41: 402‐417, 1978.
 27. Byrne JH, Castellucci VF, Kandel ER. Contribution of individual mechanoreceptor sensory neurons to defensive gill‐withdrawal reflex in Aplysia. J Neurophysiol 41: 418‐431, 1978.
 28. Byrne JH, Koester J. Respiratory pumping: Neuronal control of a centrally commanded behavior in Aplysia. Brain Res 143: 87‐105, 1978.
 29. Carew TJ, Walters ET, Kandel ER. Classical‐conditioning in a simple withdrawal reflex in Aplysia‐Californica. JNeurosci 1: 1426‐1437, 1981.
 30. Castellucci V, Pinsker H, Kupfermann I, Kandel ER. Neuronal mechanisms of habituation and dishabituation of the gill‐withdrawal reflex in Aplysia. Science 167: 1745‐1748, 1970.
 31. Clarac F, Pearlstein E. Invertebrate preparations and their contribution to neurobiology in the second half of the 20th century. Brain Res Rev 54: 113‐161, 2007.
 32. Crabtree RL, Page CH. Oxygen‐sensitive elements in book gills of Limulus polyphemus. J Exp Biol 60: 631‐639, 1974.
 33. Croll RP. Sensory control of respiratory pumping in Aplysia californica. J exp Biol 117: 15‐27, 1985.
 34. Croll RP. Complexities of a simple system: New lessons, old challenges and peripheral questions for the gill withdrawal reflex of Aplysia. Brain Research Reviews 43: 266‐274, 2003.
 35. de Vlieger TA, Lever‐de Vries CH, Plesch BEC. Peripheral and central control of the pneumostome in Lymnaea stagnalis. In: Budapest JS, editor. Neurobiology of Invertebrates, Gastropoda Brain. Budapest: Akadémiai Kiadó, 1976, p. 624‐634.
 36. Decelle J, Andersen A, Hourdez S. Morphological adaptations to chronic hypoxia in deep‐sea decapod crustaceans from hydrothermal vents and cold seeps. Mar Biol 157: 1259‐1269, 2010.
 37. Denton JS, McCann FV, Leiter JC. CO2 chemosensitivity in Helix aspersa: Three potassium currents mediate pH‐sensitive neuronal spike timing. Am J Physiol Cell Physiol 292: C292‐C304, 2007.
 38. Diaz H, Rodriguez G. The branchial chamber in terrestrial crabs: A comparative study. Biol Bull 153: 485‐504, 1977.
 39. Dicaprio RA. Nonspiking interneurons in the ventilatory central pattern generator of the shore crab, Carcinus maenas. J Comp Neurol 285: 83‐106, 1989.
 40. Dickinson PS. Neuronal control of gills in diverse Aplysia species: Conservative evolution. J Comp Physiol A 139: 17‐23, 1980.
 41. Duncan FD, Forster TD, Hetz SK. Pump out the volume ‐ the effect of tracheal and subelytral pressure pulses on convective gas exchange in a dung beetle, Circellium bacchus (Fabricus). J Insect Physiol 56: 551‐558, 2010.
 42. Dunn TW, Montgomery EA, Syed NI. An action potential‐induced and ryanodine sensitive calcium transient dynamically regulates transmitter release at synapses between Lymnaea neurons. Synapse 63: 61‐68, 2009.
 43. Dyer MF, Uglow RF. Gill chamber ventilation and scaphognathite movements in Crangon crangon (L.). J Exp Mar Biol Ecol 31: 195‐207, 1978.
 44. Eldridge FL. Central integration of mechanisms in exercise hyperpnea. Med Sci Sports Exerc 26: 319‐327, 1994.
 45. Eldridge FL, Millhorn DE, Kiley JP, Waldrop TG. Stimulation by central command of locomotion, respiration and circulation during exercise. Respir Physiol 59: 313‐337, 1985.
 46. Erickson JT, Sposato BC. Autoresuscitation responses to hypoxia‐induced apnea are delayed in newborn 5‐HT‐deficient Pet‐1 homozygous mice. J Appl Physiol 106: 1785‐1792, 2009.
 47. Erlichman JS, Coates EL, Leiter JC. Carbonic anhydrase and CO2 chemoreception in the pulmonate snail Helix aspersa. Respir Physiol 98: 27‐41, 1994.
 48. Erlichman JS, Leiter JC. CO2 chemoreception in the pulmonate snail, Helix aspersa. Respir Physiol 93: 347‐363, 1993.
 49. Erlichman JS, Leiter JC. Central chemoreceptor stimulus in the terrestrial, pulmonate snail, Helix aspersa. Respir Physiol 95: 209‐226, 1994.
 50. Farley RD, Case JF, Roeder KD. Pacemaker for tracheal ventilation in the cockroach, Periplaneta americana (L.). J Insect Physiol 13: 1713‐1716, 1967.
 51. Farley RD, Case JF. Sensory modulation of ventilative pacemaker output in the cockroach, Periplaneta americana. J Insect Physiol 14: 591‐601, 1968.
 52. Farrelly CA, Greenaway P. Morphology and ultrastructure of the gills of terrestrial crabs (Crustacea, Gecarcinidae and Grapsidae) ‐ adaptations for air‐breathing. Zoomorph 112: 39‐49, 1992.
 53. Farrelly C, Greenaway P. Gas exchange through the lungs and gills in air‐breathing crabs. J Exp Biol 187: 113‐130, 1994.
 54. Feldman JL. Chapter 14–looking forward to breathing. Prog Brain Res 188: 213‐218, 2011.
 55. Feldman JL, Del Negro CA. Looking for inspiration: New perspectives on respiratory rhythm. Nat Rev 7: 232‐242, 2006.
 56. Feldman JL, Janczewski WA. The Last Word: Point:Counterpoint authors respond to commentaries on “the parafacial respiratory group (pFRG)/pre‐Botzinger complex (preBotC) is the primary site of respiratory rhythm generation in the mammal”. J Appl Physiol 101: 689, 2006a.
 57. Feldman JL, Janczewski WA. Counterpoint: The preBotC is the primary site of respiratory rhythm generation in the mammal. J Appl Physiol 100: 2096‐2097; discussions 2097‐2098, 2103‐2098, 2006b.
 58. Feng ZP, Klumperman J, Lukowiak K, Syed NI. In vitro synaptogenesis between the somata of identified Lymnaea neurons requires protein synthesis but not extrinsic growth factors or substrate adhesion molecules. J Neurosci 17: 7839‐7849, 1997.
 59. Ferguson GP, Benjamin PR. The whole‐body withdrawal response of Lymnaea stagnalis .2. Activation of central motoneurons and muscles by sensory input. J Exp Biol 158: 97‐116, 1991.
 60. Fewell JE. Protective responses of the newborn to hypoxia. Respir Physiol Neurobiol 149: 243‐255, 2005.
 61. Fewell JE, Ng VKY, Zhang C. Prior exposure to hypoxic‐induced apnea impairs protective responses of newborn rats in an exposure‐dependent fashion: Influence of normoxic recovery time. J Appl Physiol 99: 1607‐1612, 2005.
 62. Fincke T, Paul R. Book lung function in arachnids III. The function and control of the spiracles. J Comp Physiol B 159: 433‐441, 1989.
 63. Forster HV, Pan LG, Lowry TF, Serra A, Wenninger J, Martino P. Important role of carotid chemoreceptor afferents in control of breathing of adult and neonatal mammals. Respir Physiol 119: 199‐208, 2000.
 64. Frost WN, Kandel ER. Structure of the network mediating siphon‐elicited siphon withdrawal in Aplysia. J Neurophysiol 73: 2413‐2427, 1995.
 65. Garcia AJ, III, Zanella S, Koch H, Doi A, Ramirez JM. Chapter 3–networks within networks: The neuronal control of breathing. Prog Brain Res 188: 31‐50.
 66. Glanzman DL. Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Curr Biol 20: R31‐R36.
 67. Goodwin GM, McCloskey DI, Mitchell JH. Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J Physiol 226: 173‐190, 1972.
 68. Gozal D, Torres JE, Gozal YM, Nuckton TJ. Characterization and developmental aspects of anoxia‐induced gasping in the rat. Biol Neonate 70: 280‐288, 1996.
 69. Graham JB. Ecological and evolutionary aspects of integumentary respiration: Body size, diffusion, and the invertebrata. Amer Zool 28: 1031‐1045, 1988.
 70. Greenlee KJ, Harrison JF. Development of respiratory function in the American locust Schistocerca americana. I. Across‐instar effects. J Exp Biol 207: 497‐508, 2004.
 71. Greenspan RJ. An Introduction to Nervous Systems. Woodbury, NY: Cold Spring Harbor Laboratory Press, 2007.
 72. Greenspan RJ. No critter left behind: An invertebrate renaissance. Curr Biol 15: R671‐R672, 2005.
 73. Griffin AJ, Fahrenbach WH. Gill receptor arrays in the horseshoe crab (Limulus polyphemus). Tissue and Cell 9: 745‐750, 1977.
 74. Gullan PJ, Cranston PS. The Insects : An Outline of Entomology. Chichester, West Sussex, UK; Hoboken, NJ: Wiley‐Blackwel, 2010.
 75. Haque Z, Lee TK, Inoue T, Luk C, Hasan SU, Lukowiak K, Syed NI. An identified central pattern‐generating neuron co‐ordinates sensory‐motor components of respiratory behavior in Lymnaea. Eur J Neurosci 23: 94‐104, 2006.
 76. Harrison JF. Ventilatory mechanism and control in grasshoppers. Amer Zool 37: 73‐81, 1997.
 77. Harrison JF. Insect acid‐base physiology. Ann Rev Entomol 46: 221‐250, 2001.
 78. Harrison JF, Roberts SP. Flight respiration and energetics. Ann Rev Physiol 62: 179‐205, 2000.
 79. Hawkins RD, Kandel ER, Bailey CH. Molecular mechanisms of memory storage in Aplysia. Biol Bull 210: 174‐191, 2006.
 80. Hawksworth DL, Kalin‐Arroyo MT. Magnitude and distribution of biodiversity. In: Heywood V, editor. Global Biodiversity Assessment. Cambridge, UK: Cambridge University Press, 1995, p. 107‐191.
 81. Haydon PG, Winlow W. Morphology of the giant dopamine‐containing neuron, RPeD1, in Lymnaea stagnalis Revealed by Lucifer Yellow Ch. J Exp Biol 94: 149‐158, 1981
 82. Henderson DR, Johnson SM, Prange HD. CO2 and heat have different effects on directed ventilation behavior of grasshoppers Melanoplus differentialis. Respir Physiol 114: 297‐307, 1998.
 83. Hermann PM, Bulloch AG. Developmental plasticity of respiratory behavior in Lymnaea. Behav Neurosci 112: 656‐667, 1998.
 84. Hexter SH. Lungbook microstructure in Tegenaria sp. Bull Br Arachnol Soc 7: 323‐326, 1982.
 85. Heymann N, Lehmann F‐O. The significance of spiracle conductance and spatial arrangement for flight muscle function and aerodynamic performance in flying Drosophila. J Exp Biol 209: 1662‐1677, 2006.
 86. Hill AA, Garcia AJ, III, Zanella S, Upadhyaya R, Ramirez JM. Graded reductions in oxygenation evoke graded reconfiguration of the isolated respiratory network. J Neurophysiol 105: 625‐639, 2011.
 87. Hill AAV, Van Hooser SD, Calabrese RL. Half‐center oscillators underlying rhythmical movements. In: Arbib MA, editor. The Handbook of Brain Theory and Neural Networks. Boston: MIT Press, 2003.
 88. Hooper SL, DiCaprio RA. Crustacean motor pattern generator networks. Neuro‐Signals 13: 50‐69, 2004. doi:10.1159/000076158
 89. Hughes GM, Knights B, Scammell CA. The distribution of PO2 and hydrostatic pressure changes within the branchial chambers in relation to gill ventilation of the shore crab Carcinus maenas l. J Exp Biol 51: 203‐220, 1969.
 90. Hughes GM, Mill PJ. Patterns of ventilation in dragonfly larvae. J Exp Biol 44: 317‐333, 1966.
 91. Hustert R. Neuromuscular coordination and proprioceptive control of rhythmical abdominal ventilation in intact Locusta migratoria migratorioides. J Comp Physiol A 97: 159‐179, 1975.
 92. Inoue T, Haque Z, Lukowiak K, Syed NI. Hypoxia‐induced respiratory patterned activity in Lymnaea originates at the periphery. J Neurophysiol 86: 156‐163, 2001.
 93. Inoue T, Takasaki M, Lukowiak K, Syed NI. Inhibition of the respiratory pattern‐generating neurons by an identified whole‐body withdrawal interneuron of Lymnaea stagnalis. J Exp Biol 199: 1887‐1898, 1996.
 94. Ivanchenko MV, Thomas N, Selverston AI, Rabinovich MI. Pacemaker and network mechanisms of rhythm generation: Cooperation and competition. J Theor Biol 253: 452‐461, 2008.
 95. Janse C, van der Wilt GJ, van der Plas J, van der Roest M. Central and peripheral neurones involved in oxygen perception in the pulmonate snail Lymnaea stagnalis (Mollusca, Gastropoda). Comp Biochem Physiol A 82: 459‐469, 1985.
 96. Jones JD. Aspects of respiration in Planorbis corneus L. and Lymnaea stagnalis L. (Gastropoda: Pulmonata). Comp Biochem Physiol 4: 1‐29, 1961.
 97. Kamardin NN, Shalanki Y, Rozha KS, Nozdrachev AD. Studies of chemoreceptor perception in mollusks. Neurosci Behav Physiol 31: 227‐235, 2001.
 98. Kamenz C, Prendini L. An atlas of book lung fine structure in the order scorpions (Arachnida). Bull Am Mus Nat Hist 316: 1‐359, 2008.
 99. Kammer AE. Respiration and the generation of rhythmic outputs in insects. Fed Proc 35: 1992‐1999, 1976.
 100. Kandel ER. The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030‐1038, 2001.
 101. Kandel ER. The biology of memory: A forty‐year perspective. J Neurosci 29: 12748‐12756, 2009.
 102. Kandel ER, Kupfermann I. The functional organization of invertebrate ganglia. Ann Rev Physiol 32: 193‐258, 1970.
 103. Kendler KS, Greenspan RJ. The nature of genetic influences on behavior: Lessons from “simpler” organisms. Am J Psychiatry 163: 1683‐1694, 2006.
 104. Khan AM, Spencer GE. Novel neural correlates of operant conditioning in normal and differentially reared Lymnaea. J Exp Biol 212: 922‐933, 2009.
 105. Kline DD. Plasticity in glutamatergic NTS neurotransmission. Respir Physiol Neurobiol 164: 105‐111, 2008.
 106. Kupfermann I, Carew TJ. Behavior patterns of Aplysia californica in its natural environment. Behavioral Biology 12: 317‐337, 1974.
 107. Kupfermann I, Carew TJ, Kandel ER. Local, reflex, and central commands controlling gill and siphon movements in Aplysia. J Neurophysiol 37: 996‐1019, 1974.
 108. Lahiri S, Roy A, Baby SM, Hoshi T, Semenza GL, Prabhakar NR. Oxygen sensing in the body. Prog Biophys Mol Biol 91: 249‐286, 2006.
 109. Lal A, Oku Y, Hulsmann S, Okada Y, Miwakeichi F, Kawai S, Tamura Y, Ishiguro M. Dual oscillator model of the respiratory neuronal network generating quantal slowing of respiratory rhythm. J Comput Neurosci 30: 225‐240, 2011.
 110. Lehmann F‐O. Matching spiracle opening to metabolic need during flight in drosophila. Science 294: 1926‐1929, 2001.
 111. Levy M, Achituv Y, Susswein A. Relationship between respiratory pumping and oxygen consumption in Aplysia depilans and Aplysia fasciata. J Exp Biol 141: 389‐405 1989.
 112. Levy M, Levy I, Susswein AJ. Respiratory pumping in Aplysia fasciata in natural and artificial tide pools. J Comp Physiol A 180: 81‐89, 1997.
 113. Lewis GW, Miller PL, Mills PS. Neuromuscular mechanisms of abdominal pumping in locust. J Exp Biol 59: 149‐168, 1973.
 114. Lighton JRB, Fielden LJ. Gas exchange in wind spiders (Arachnida, Solphugidae): Independent evolution of convergent control strategies in solphugids and insects. J Insect Physiol 42: 347‐357, 1996.
 115. Lindberg DR, Ponder WF. The influence of classification on the evolutionary interpretation of structure ‐ a re‐evaluation of the evolution of the pallial cavity of gastropod molluscs. Org Divers Evol 1: 273‐299, 2001.
 116. Locke M. The co‐ordination of growth in the tracheal system of insects. Q J Microsc Sci 99: 373‐391, 1958.
 117. Lovett‐Barr MR, Mitchell GS, Satriotomo I, Johnson SM. Serotonin‐induced in vitro long‐term facilitation exhibits differential pattern sensitivity in cervical and thoracic inspiratory motor output. Neuroscience 142: 885‐892, 2006.
 118. Lowe MR, Spencer GE. Perturbation of the activity of a single identified neuron affects long‐term memory formation in a molluscan semi‐intact preparation. J Exp Biol 209: 711‐721, 2006.
 119. Lucu C. Ionic regulatory mechanisms in crustacean gill epithelia. Comp Biochem Physiol 97A: 297‐306, 1990.
 120. Lukowiak K. Central pattern generators: Some principles learned from invertebrate model systems. J Physiol (Paris) 85: 63‐70, 1991.
 121. Lukowiak K, Cotter R, Westly J, Ringseis E, Spencer G, Syed N. Long‐term memory of an operantly conditioned respiratory behaviour pattern in Lymnaea stagnalis. J Exp Biol 201: 877‐882, 1998.
 122. Lukowiak K, Martens K, Orr M, Parvez K, Rosenegger D, Sangha S. Modulation of aerial respiratory behaviour in a pond snail. Respir Physiol Neurobiol 154: 61‐72, 2006.
 123. Lukowiak K, Ringseis E, Spencer G, Wildering W, Syed N. Operant conditioning of aerial respiratory behaviour in Lymnaea stagnalis. J Exp Biol 199: 683‐691, 1996.
 124. Lukowiak K, Sangha S, Scheibenstock A, Parvez K, McComb C, Rosenegger D, Varshney N, Sadamoto H. A molluscan model system in the search for the engram. J Physiol Paris 97: 69‐76, 2003.
 125. Lukowiak K, Syed N. Learning, memory and a respiratory central pattern generator. Comp Biochem Physiol A 124: 265‐274, 1999.
 126. Maina JN. The morphology of the lung of a tropical terrestrial slug Trichotoxon copleyi (Mollusca: Gastropoda: Pulmonata): A scanning and transmission electron microscopic study. J Zoology 217: 355‐366, 1989.
 127. Maitland DP. A highly complex invertebrate lung the gill chambers of the soldier crab Mictyris longicarpus. Naturwissenschaften 74: 293‐295, 1987.
 128. Maitland DP, Maitland A. Penetration of water into blind‐ended capillary tubes and its bearing on the functional design of the lungs of soldier crabs Mictyris longicarpus. J Exp Biol 163: 333‐344, 1992.
 129. Marder E. Motor pattern generation. Curr Opin Neurobiol 10: 691‐698, 2000.
 130. Marder E, Bucher D, Schulz DJ, Taylor AL. Invertebrate central pattern generation moves along. Curr Biol 15: R685‐R699, 2005.
 131. Marder E, Calabrese RL. Principles of rhythmic motor pattern generation. Physiol Rev 76: 687‐717, 1996.
 132. Martens KR, De Caigny P, Parvez K, Amarell M, Wong C, Lukowiak K. Stressful stimuli modulate memory formation in Lymnaea stagnalis. Neurobiol Learn Mem 87: 391‐403, 2007.
 133. McMahon BR. Respiratory and circulatory compensation to hypoxia in crustaceans. Respir Physiol 128: 349‐364, 2001.
 134. Mendelson M. Oscillator neurons in crustacean ganglia. Science 171: 1170‐1173, 1971.
 135. Mill PJ. Neural patterns associated with ventilatory movements in dragonfly larvae. J Exp Biol 52: 167‐175, 1970.
 136. Mill PJ, Hughes GM. Nervous control of ventilation in dragonfly larvae. J Exp Biol 44: 297‐316, 1966.
 137. Miller PL. Respiration in the desert locust .1. The control of ventilation. J Exp Biol 37: 224‐236, 1960a.
 138. Miller PL. Respiration in the desert locust .2. The control of the spiracles. J Exp Biol 37: 237‐263, 1960b.
 139. Miller PL. Respiration in the desert locust .3. Ventilation and the spiracles during flight. J Exp Biol 37: 264‐278, 1960c.
 140. Miller PL, Beament JWL, Trehernc JE, Wigglesworth VB. The regulation of breathing in insects. In: Advances in Insect Physiology. London (Engl): Academic Press, 1966, p. 279‐354.
 141. Milsom WK. The phylogeny of central chemoreception. Resp Physiol Neurobiol 173: 195‐200, 2010.
 142. Mitchell GS, Babb TG. Layers of exercise hyperpnea: Modulation and plasticity. Respir Physiol Neurobiol 151: 251‐266, 2006.
 143. Mitchell GS, Johnson SM. Neuroplasticity in respiratory motor control. J Appl Physiol 94: 358‐374, 2003.
 144. Molkov YI, Abdala AP, Bacak BJ, Smith JC, Paton JF, Rybak IA. Late‐expiratory activity: Emergence and interactions with the respiratory CpG. J Neurophysiol 104: 2713‐2729, 2010.
 145. Montarolo P, Goelet P, Castellucci V, Morgan J, Kandel E, Schacher S. A critical period for macromolecular synthesis in long‐term heterosynaptic facilitation in Aplysia. Science 234: 1249‐1254, 1986.
 146. Moore SJ. Some spider organs as seen by the scanning electron microscope, with special reference to the book‐lung. Bull Br Arachnol Soc 3: 177‐187, 1976.
 147. Morton JE. Molluscs: An Introduction to their Form and Functions. New York: Harper and Brothers, 1960.
 148. Mulloney B, Harness PI, Hall WM. Bursts of information: Coordinating interneurons encode multiple parameters of a periodic motor pattern. J Neurophysiol 95: 850‐861, 2006.
 149. Myers TB, Fisk FW. Breathing movements of the Cuban burrowing cockroach. Ohio J Sci 62: 253, 1962.
 150. Nation JL. Insect Physiology and Biochemistry. Boca Raton: CRC Press/Taylor & Francis, 2008.
 151. Nattie E, Li A. Central chemoreception 2005: A brief review. Auton Neurosci 126‐127: 332‐338, 2006.
 152. Nattie E, Li A. Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol 106: 1464‐1466, 2009.
 153. Onimaru H, Homma I. Point: The PFRG is the primary site of respiratory rhythm generation in the mammal. J Appl Physiol 100: 2094‐2095, 2006.
 154. Onimaru H, Ikeda K, Kawakami K. Phox2b, RTN/pFRG neurons and respiratory rhythmogenesis. Respir Physiol Neurobiol 168: 13‐18, 2009.
 155. Onimaru H, Kumagawa Y, Homma I. Respiration‐related rhythmic activity in the rostral medulla of newborn rats. J Neurophysiol 96: 55‐61, 2006.
 156. Opell BD. The respiratory complementarity of spider book lung and tracheal systems. J Morphol 236: 57‐64, 1998.
 157. Otto D, Janiszewski J. Interneurones originating in the suboesophageal ganglion that control ventilation in two cricket species: Effects of the interneurones (SD‐AE neurones) on the motor output. J Insect Physiol 35: 483‐491, 1989.
 158. Page CH. Localization of limulus polyphemus oxygen sensitivity. Biol Bull 144: 383‐390, 1973.
 159. Page CH, Crabtree RL. Oxygen sensitivity in limulus‐polyphemus. Am Zool 12: 687‐688, 1972.
 160. Page LR. Modern insights on gastropod development: Reevaluation of the evolution of a novel body plan. Integ Comp Biol 46: 134‐143, 2006.
 161. Pearson KG. Burst generation in coordinating interneurons of the ventilatory system of the locust. J Comp Physiol A 137: 305‐313, 1980.
 162. Peever J. The ins and outs of deep breathing ‐ mechanisms of respiratory motor plasticity. J Appl Physiol 109: 265‐6, 2010.
 163. Peng YJ, Nanduri J, Yuan G, Wang N, Deneris E, Pendyala S, Natarajan V, Kumar GK, Prabhakar NR. NADPH oxidase is required for the sensory plasticity of the carotid body by chronic intermittent hypoxia. J Neurosci 29: 4903‐4910, 2009.
 164. Pickard RS, Mill PJ. Ventilatory muscle activity in intact preparations of Aeshnid dragonfly larvae. J Exp Biol 56: 527‐536, 1972.
 165. Pickard RS, Mill PJ. Ventilatory movements of abdomen and branchial apparatus in dragonfly larvae (Odonata‐Anisoptera). J Zool 174: 23‐40, 1974.
 166. Piepoli M, Clark AL, Coats AJ. Muscle metaboreceptors in hemodynamic, autonomic, and ventilatory responses to exercise in men. Am J Physiol 269: H1428‐H1436, 1995.
 167. Pittenger C, Kandel ER. In search of general mechanisms for long‐lasting plasticity: Aplysia and the hippocampus. Philos Trans R Soc Lond B Biol Sci 358: 757‐763, 2003.
 168. Plateau F. Recherches experimentales sur les mouvements respiratoires des insectes. Mem Acad Roy Belg 45: 219ff, 1882.
 169. Ramirez J‐M. Reconfiguration of the respiratory network at the onset of locust flight. J Neurophysiol 80: 3137‐3147, 1998.
 170. Ramirez JM, Pearson KG. Alteration of the respiratory system at the onset of locust flight .1. Abdominal pumping. J Exp Biol 142: 401‐424, 1989a.
 171. Ramirez JM, Pearson KG. Distribution of intersegmental interneurones that can reset the respiratory rhythm of the locust. J Exp Biol 141: 151‐176, 1989b.
 172. Rascon B, Henry JR, Harrison JF, Fezzaa K, Lee WK, Socha JJ. Peering inside the insect thorax: An examination of thoracic autoventilation in live insects using synchrotron x‐rays. Integr Comp Biol 45: 1181‐1181, 2005.
 173. Regehr WG, Pine J, Cohan CS, Mischke MD, Tank DW. Sealing cultured invertebrate neurons to embedded dish electrodes facilitates long‐term stimulation and recording. J Neurosci Methods 30: 91‐106, 1989.
 174. Reid SG, Sundin L, Kalinin AL, Rantin FT, Milsom WK. Cardiovascular and respiratory reflexes in the tropical fish, traira (Hoplias malabaricus): CO2/pH chemoresponses. Respir Physiol 120: 47‐59, 2000.
 175. Richerson GB, Wang W, Hodges MR, Dohle CI, Diez‐Sampedro A. Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp Physiol 90: 259‐266; discussion 266‐259, 2005.
 176. Richter DW, Bischoff A, Anders K, Bellingham M, Windhorst U. Response of the medullary respiratory network of the cat to hypoxia. J Physiol 443: 231‐256, 1991.
 177. Robertson RM, Pearson KG. Interneurons in the flight system of the locust ‐ distribution, connections, and resetting properties. J Comp Neurol 215: 33‐50, 1983.
 178. Rosenegger D, Parvez K, Lukowiak K. Enhancing memory formation by altering protein phosphorylation balance. Neurobiol Learn Mem 90: 544‐552, 2008.
 179. Rosenegger D, Wright C, Lukowiak K. A quantitative proteomic analysis of long‐term memory. Mol Brain 3: 9, 2010.
 180. Ruthensteiner B. Homology of the pallial and pulmonary cavity of gastropods. J Moll Stud 63: 353‐367, 1997.
 181. Sangha S, Scheibenstock A, Lukowiak K. Reconsolidation of a long‐term memory in Lymnaea requires new protein and RNA synthesis and the soma of right pedal dorsal 1. J Neurosci 23: 8034‐8040, 2003.
 182. Sangha S, Scheibenstock A, McComb C, Lukowiak K. Intermediate and long‐term memories of associative learning are differentially affected by transcription versus translation blockers in Lymnaea. J Exp Biol 206: 1605‐1613, 2003.
 183. Sangha S, Scheibenstock A, Morrow R, Lukowiak K. Extinction requires new RNA and protein synthesis and the soma of the cell right pedal dorsal 1 in Lymnaea stagnalis. J Neurosci 23: 9842‐9851, 2003.
 184. Sattelle D, Buckingham S. Invertebrate studies and their ongoing contributions to neuroscience. Invert Neurosci 6: 1‐3, 2006.
 185. Scheibenstock A, Krygier D, Haque Z, Syed N, Lukowiak K. The Soma of RPeD1 must be present for long‐term memory formation of associative learning in Lymnaea. J Neurophysiol 88: 1584‐1591, 2002.
 186. Schmitz A, Perry SF. Respiratory system of arachnids. I. Morphology of the respiratory system of Salticus scenicus and Euophrys lanigera (Arachnida, Araneae, Salticidae). Arthropod Struct Dev 29: 3‐12, 2000.
 187. Schmitz A, Perry SF. Bimodal breathing in jumping spiders: Morphometric partitioning of the lungs and tracheae in Salticus scenicus (Arachnida, Araneae, Salticidae). J Exp Biol 204: 4321‐4334, 2001.
 188. Schmitz A, Perry SF. Respiratory organs in wolf spiders: Morphometric analysis of lungs and tracheae in Pardosa lugubris (L.) (Arachnida, Araneae, Lycosidae). Arthropod Struct Dev 31: 217‐230, 2002.
 189. Smith JC, Abdala APL, Rybak IA, Paton JFR. Structural and functional architecture of respiratory networks in the mammalian brainstem. Philo Trans R Soc London B 364: 2577‐2587, 2009.
 190. Socha JJ, Cox L, Lee WK, Means M, Tolley J. Under pressure: The biomechanical mechanism of rhythmic tracheal compression in carabid beetles. Integr Comp Biol 50: E164‐E164, 2010.
 191. Socha JJ, Fezzaa K, Lee WK, Waters JS, Westneat MW. Tracheal compression patterns involved in gas exchange in the ground beetle, Platynus decentis. Integr Comp Biol 44: 748‐748, 2004.
 192. Socha JJ, Förster TD, Greenlee KJ. Issues of convection in insect respiration: Insights from synchrotron X‐ray imaging and beyond. Resp Physiol Neurobiol 173: S65‐S73, 2010.
 193. Socha JJ, Lee W‐K, Harrison JF, Waters JS, Fezzaa K, Westneat MW. Correlated patterns of tracheal compression and convective gas exchange in a carabid beetle. J Exp Biol 211: 3409‐3420, 2008.
 194. Socha JJ, Lee WK, Westneat MW. Beetle respiration mechanics analyzed with synchrotron X‐ray imaging. Integr Comp Biol 43: 982‐982, 2003.
 195. Socha JJ, Westneat MW, Harrison JF, Waters JS, Lee WK. Real‐time phase‐contrast x‐ray imaging: A new technique for the study of animal form and function. BMC Biology 5: 1‐15, 2007.
 196. Stoll CJ. Sensory systems involved in the shadow response of Lymnea stagnalis as studied with the use of habituation phenomema. Proc Kon Ned Akad Wetensch 75C: 342‐351, 1972.
 197. Sundin L, Burleson ML, Sanchez AP, Amin‐Naves J, Kinkead R, Gargaglioni LH, Hartzler LK, Wiemann M, Kumar P, Glass ML. Respiratory chemoreceptor function in vertebrates comparative and evolutionary aspects. Integr Comp Biol 47: 592‐600, 2007.
 198. Swain R, Marker PF, Richardson AMM. Comparison of the gill morphology and branchial chambers in two fresh‐water Crayfishes from Tasmania: Astacopsis franklinii and Parastacoides tasmanicus. J Crust Biol 8: 355‐363, 1988.
 199. Syed NI, Bulloch AG, Lukowiak K. In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 250: 282‐285, 1990.
 200. Syed NI, Bulloch AG, Lukowiak K. The respiratory central pattern generator (CPG) of Lymnaea reconstructed in vitro. Acta Biol Hung 43: 409‐419, 1992.
 201. Syed NI, Ridgway RL, Lukowiak K, Bulloch AG. Transplantation and functional integration of an identified respiratory interneuron in Lymnaea stagnalis. Neuron 8: 767‐774, 1992.
 202. Syed NI, Winlow W. Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones. J Exp Biol 158: 37‐62, 1991a.
 203. Syed NI, Winlow W. Respiratory behavior in the pond snail Lymnaea stagnalis. I. Behavioral analysis and the identification of motor neurons. J Comp Physiol A 169: 541‐555, 1991b.
 204. Syed NI, Winlow W. Respiratory behavior in the pond snail Lymnaea stagnalis. II. Neual elements of the central pattern generator (CPG). J Comp Physiol A 169: 557‐568, 1991c.
 205. Syed NI, Zaidi H, Lovell P. In vitro reconstruction of neuronal circuits: A simple model system approach. In: Windhorst U, Johansson H, editors. Modern Techniques in Neuroscience Research. Berlin: Springer‐Verlag, 1999, p. 361‐377.
 206. Taylor BE, Lukowiak K. The respiratory central pattern generator of Lymnaea: A model, measured and malleable. Respir Physiol 122: 197‐207, 2000.
 207. Thoby‐Brisson M, Karlen M, Wu N, Charnay P, Champagnat J, Fortin G. Genetic identification of an embryonic parafacial oscillator coupling to the preBotzinger complex. Nat Neurosci 12: 1028‐1035, 2009.
 208. Thompson C, Page CH. Nervous control of respiration ‐ oxygen‐sensitive elements in prosoma of Limulus‐Polyphemus. J Exp Biol 62: 545‐554, 1975.
 209. Thompson S, Watson WH, III. Central pattern generator for swimming in Melibe. J Exp Biol 208: 1347‐1361, 2005.
 210. Walters ET, Carew TJ, Kandel ER. Classical‐conditioning in Aplysia‐Californica. Proc Nat Acad Sci 76: 6675‐6679, 1979.
 211. Wasserthal LT. Flight‐motor‐driven respiratory air flow in the hawkmoth Manduca sexta. J Exp Biol 204: 2209‐2220, 2001.
 212. Waters JS, Socha JJ. Mechanics of tracheal compression in the bessbug, Popilius disjunctus. Integ Comp Biol 45: 1209‐1209, 2005.
 213. Webb B. Robots in invertebrate neuroscience. Nature 417: 359‐363, 2002.
 214. Wedemeyer H, Schild D. Chemosensitivity of the osphradium of the pond snail Lymnaea‐Stagnalis. J Exp Biol 198: 1743‐1754, 1995.
 215. Weis‐Fogh T. Diffusion in insect wing muscle, the most active tissue known. J Exp Biol 41: 229‐256, 1964.
 216. Weis‐Fogh T. Respiration and tracheal ventilation in locusts and other flying insects. J Exp Biol 47: 561‐587, 1967.
 217. Westneat MW, Betz O, Blob RW, Fezzaa K, Cooper WJ, Lee W‐K. Tracheal respiration in insects visualized with synchrotron x‐ray imaging. Science 299: 558‐560, 2003.
 218. Wigglesworth VB. A theory of tracheal respiration in insects. Proc Roy Soc Lond B 106: 229‐250, 1930.
 219. Wigglesworth VB. The respiration of insects. Biol Rev 6: 181‐220, 1931.
 220. Wilkens J, Young R, DiCaprio R. Responses of the isolated crab ventilatory central pattern generators to variations in oxygen tension. J Comp Physiol B: Biochem Syst Environ Physiol 159: 29‐36, 1989.
 221. Wilkens JL, McMahon BR. Aspects of branchial irrigation in the lobster Homarus americanus. I. Functional analysis of scaphognathite beat, water pressures and currents. J Exp Biol 56: 469‐479, 1972.
 222. Wilkens JL, Young RE. Patterns and bilateral coordination of scaphognathite rhythms in the lobster Homarus americanus. J Exp Biol 63: 219‐235, 1975.
 223. Wilson D. The central nervous control of locust flight. J Exp Biol 38: 471‐490, 1961.
 224. Winlow W, Benjamin PR. Postsynaptic effects of a multiaction giant interneurone on identified snail neurones. Nature 268: 263‐265, 1977.
 225. Winlow W, Haydon PG, Benjamin PR. Multiple postsynaptic actions of the giant dopamine‐containing neuron RPeD1 of Lymnaea‐Stagnalis. J Exp Biol 94: 137‐148, 1981.
 226. Winlow W, Syed NI. The respiratory central pattern generator of Lymnaea. Acta Biol Hung 43: 399‐408, 1992.
 227. Woodman JD, Cooper PD, Haritos VS. Neural regulation of discontinuous gas exchange in Periplaneta americana. J Insect Physiol 54: 472‐480, 2008.
 228. Wu JY, Cohen LB, Falk CX. Neuronal activity during different behaviors in Aplysia: A distributed organization? Science 263: 820‐823, 1994.
 229. Yaqoob N, Schwerte T. Cardiovascular and respiratory developmental plasticity under oxygen depleted environment and in genetically hypoxic zebrafish (Danio rerio). Comp Biochem Physiol A Mol Integr Physiol 156: 475‐484.
 230. Zhang Z‐Q, Shear WA. Linnaeus tercentenary and invertebrate taxonomy: An introduction. Zootaxa 1668: 7‐10, 2007.
 231. Zinebi H, Simmers J, Truchot JP. A peripheral arterial O2‐sensitive pathway to the respiratory oscillator of the shore crab Carcinus Maenas. J Exp Biol 148: 181‐199, 1990.
 232. Zoond A, Charles E. Studies in the localisation of respiratory exchange in invertebrates: I. The respiratory mechanism of the fresh‐water crab Potamonautes. J Exp Biol 8: 250‐257, 1931.

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Harold J. Bell, Naweed I. Syed. Control of Breathing in Invertebrate Model Systems. Compr Physiol 2012, 2: 1745-1766. doi: 10.1002/cphy.c100040