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Control of Breathing in Invertebrate Model Systems

Harold J. Bell, Naweed I. Syed

10.1002/cphy.c100040

Source: Volume 2, Issue 3, July 2012

Published online: July 2012

Full Article on Wiley Online Library



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.jpghttp://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 2 and 3 in Kamenz & Prendini (98).
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 (98).
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 1 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 1 of Socha et al. (195), 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 2, 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 1 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 3 of Inoue et al. (93).


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.jpghttp://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 2 and 3 in Kamenz & Prendini (98).


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 (98).


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 1 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 1 of Socha et al. (195), 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 2, 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 1 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 3 of Inoue et al. (93).
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Article Title: Control of Breathing in Invertebrate Model Systems
 

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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