Download Central Control of the Cardiovascular and Respiratory Systems

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July 1999
motoneurons. The respiratory system in birds resembles
that of mammals, except that they lack a diaphragm and
the lungs are ventilated by volume changes in the air sacs.
The cardiovascular system is undivided in a typical
fish, with the heart delivering blood into the branchial
vasculature and an arterioarterial respiratory route conducting blood directly from the gills to the systemic circuit. A parallel arteriovenous route through the branchial
circulation is probably nutritive, rather than constituting a
functional shunt past the respiratory route. In contrast,
mammals and birds have a completely divided circulatory
system, with separate pulmonary and systemic circuits.
Air-breathing fish, amphibians, and most reptiles have
more or less incompletely divided circulatory systems,
allowing differential perfusion of the pulmonary circuit.
This ability may be an essential component of their intermittent patterns of ventilation, often associated with periods of submersion. Amphibians may, in addition, utilize
bimodal respiration. Larval amphibians possess gills, often in combination with developing lungs, while adult
amphibians can switch between cutaneous and lung
breathing (e.g., during graded hypoxia or submersion) so
that the distributing effect of vascular mechanisms are of
paramount importance.
Despite these major differences in the construction
and mode of operation of their respiratory and cardiovascular systems, evidence is accumulating that the vertebrates share some important similarities in the mechanisms of central generation of the respiratory rhythm,
control of the cardiovascular system and, more specifically in the present context, in the central nervous and
reflex generation of cardiorespiratory interactions. The
central theme of this review is the evolution of the mechanisms of integration and coordination that match blood
flow to ventilatory movements, a relationship probably
fundamental to the success of vertebrates. Accordingly,
we address such questions as the origin and nature of
tonic nervous activity to the heart, to blood vessels, and to
the airways. It may be that our review of the evolutionary
relationships between cardiorespiratory control systems
in vertebrates will illuminate our current inadequate understanding of the fundamental mechanisms underlying
the observed interrelationships between respiratory control and cardiac control.
Knowledge of this complex area is of course dominated by the results of medically oriented research on
mammals. To thoroughly review the mammalian literature is beyond the scope and length constraints of the
current account. Instead, reference will be made in the
relevant sections to recent extensive reviews. Readers
requiring a more detailed account of the mammalian literature thus have points of access to that debate, without
unduly lengthening the current review, or unbalancing it
in relation to the available information from “lower” vertebrates. Each aspect of the review, therefore, begins with
a summary of our current understanding of the extensive
mammalian literature. This then underpins the subsequent comparative survey of the other vertebrate groups,
considered in turn from fish, through amphibians and
reptiles to birds, in relation to our more thorough understanding of the mammalian pattern. The treatment of each
group is necessarily uneven because of the limitations on
our knowledge so that the sections on “fish” are sometimes divided between elasmobranchs and teleosts and
sometimes not. It must be emphasized here that, unlike
the mammals and birds, the so-called “lower vertebrate”
groups have a complex phylogeny; that is to say that fish,
amphibian, or reptile is an umbrella term describing very
diverse groups of animals, some relatively little studied.
Because the respiratory and cardiovascular systems and
their innervation in the lower vertebrates are less well
known than those of mammals, some brief descriptions of
selected examples are included to illuminate the account
of the mechanisms of their control.
Some consideration of the mechanisms of ventilation
and of the generation of the respiratory rhythm in the CNS
is a necessary prelude to a review of the control of
cardiorespiratory interactions. Consequently, a very brief
overview of this area in mammals leads to a comparative
account of our more limited understanding of the mechanisms in lower vertebrates, which includes descriptions
of their patterns of ventilation and their origins in the
brain stem, plus a consideration of the factors determining the onset and frequency of bouts of intermittent
breathing in air-breathing fish, amphibians, and reptiles.
We then describe the innervation of the reflexogenic
areas supplying the cardiovascular and respiratory systems and implicated in the generation of cardiorespiratory interactions, including central and peripheral chemoreceptors, arterial baroreceptors, and mechanoreceptors
supplying the respiratory system. There follows a review
of the evidence for functional chemoreceptors and mechanoreceptors in fish, including air-breathing fish, and in
amphibians, which considers the developing roles for
central chemoreceptors, lung stretch receptors, and arterial baroreceptors as the vertebrates evolved from primarily water-breathing to facultative and then to obligate
air-breathing forms.
A review of the efferent innervation of the cardiovascular and respiratory systems is initiated by consideration
of the cranial autonomic outflow. Beginning with a detailed description of the central locations of vagal preganglionic neurons (VPN) in mammals, which emphasizes the
importance of the nucleus ambiguus (nA), a comparative
account of the central origins of vagal efferents innervating the cardiovascular and respiratory systems in lower
vertebrates follows. This considers evidence of a developing role in the control of cardiorespiratory interactions
for neurons relocated from the dorsal motor nucleus of
the vagus (DVN) into the nA. Description of the sympa-
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