The lamprey respiratory network: Some evolutionary aspects
Introduction
Breathing is a complex behaviour that requires sophisticated control mechanisms enabling animals to respond properly to physiological challenges and changing environmental conditions. Like locomotion and other rhythmic behaviours for which the motor pattern is generated within the brainstem and/or spinal cord without the need for peripheral or suprapontine inputs, breathing originates from a central rhythmogenic circuit. It is well known that there are similarities in the topography and functional characteristics between groups of respiration-related neurons in the hindbrain of different vertebrate groups (see e.g. Taylor et al., 1999, 2010). Therefore, a comparative approach among vertebrates may provide important insights into how multiple rhythmic circuits become functionally intertwined to produce and coordinate respiratory behaviours. There are also important differences related to the specific modes of vertebrates’ respiration. Fish typically propel water in a unidirectional fashion over the gills using ventilatory muscles operating around the jaws, the branchial muscles and the opercular muscles in teleosts. In the amphibian tadpole larvae ventilation is maintained by the activity of cranial muscles, while in the adult amphibians a buccal force pump contributes to both gill and lung breathing. Reptiles are the first group of vertebrates to use a thoracic aspiration pump to ventilate the lungs. Although they typically lack a diaphragm per se, the presence of the diaphragmaticus muscle contributes to creating the negative pressure necessary for lung ventilation. In mammals, lung ventilation is realized through coordinate contractions of diaphragmatic, intercostal and/or abdominal muscles along with some accessory respiratory muscles. The respiratory system in birds resembles that of mammals, but they lack a diaphragm and their lungs are ventilated by volume changes in the air sacs.
In the present review, we examine the main characteristics of the control of breathing in vertebrates and, in particular, we describe the main results of our studies concerning neural mechanisms involved in respiratory rhythm generation and its modulation within the lamprey respiratory network. The lamprey central nervous system may represent an ideal model to provide insights into the basic neural mechanisms of rhythmic activities, such as locomotion and respiration, owing to the presence of fewer neurons than in higher vertebrates and the experimental advantage that it can be maintained in vitro along with spontaneous respiratory activity (Grillner, 2003, 2006).
Section snippets
A few notes on evolutionary aspects of vertebrate respiration
The mammalian breathing rhythm arises from the preBötzinger complex (preBötC), a medullary neural network essential for normal breathing and widely recognized as necessary and sufficient to generate the inspiratory phase of respiration (Smith et al., 1991; for reviews see Feldman et al., 2013; Del Negro et al., 2018). This region has been identified in several mammal species, including goats, cats, rabbits, rats, mice and humans (Smith et al., 1991; Schwarzacher et al., 1995, 2011; Ramirez et
Characterization of the lamprey pTRG
Breathing in the adult lamprey is produced by synchronous contractions of the branchial muscles that pump water in and out of gill pores. Exhalation is the only active process produced by muscle contractions which compress the branchial basket, while inhalation is passive and occurs when the branchial basket expands by passive recoil during muscle relaxation, drawing fresh water back into the sacs (Rovainen, 1977, 1979). The respiratory motoneurons are located in three distinct motor nuclei,
General features
The crucial role of the pTRG in lamprey respiratory rhythm generation recalls that attributed to the mammalian preBötC (see e.g. Smith et al., 1991; Bongianni et al., 2016; Cinelli et al., 2017; Del Negro et al., 2018; Ramirez and Baertsch, 2018). The two rhythm generators exhibit many similarities. Excitatory and inhibitory amino acids have a prominent role in both neural networks that are under extensive neuromodulatory control and display sensitivity to opioids, substance P (SP),
Final considerations
Attempts to draw homologies between the central respiratory rhythm generator of the lamprey and that of mammals could appear speculative since the muscles and pumps used to ventilate the respiratory system are completely different, i.e. a buccal/branchial force pump in lampreys versus an aspiration pump in mammals. However, similarly to other neurophysiological features (see e.g. Grillner and El Manira, 2020), some prominent similarities between the pTRG and the preBötC indicate that the main
Authors contributions
All Authors prepared figures, drafted manuscript, edited and revised manuscript and approved final version of the manuscript.
Acknowledgements
This study was supported by grants from the University of Florence and from the Ente Cassa di Risparmio Firenze, Italy.
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