Jaarboek no. 89. 2010/2011 - Koninklijke Maatschappij voor ...

encompassed fluid in either direction. The system is
not particularly efficient in its use of power, but has
the advantage of allowing the steady movement
of fluids and slurries without the presence of interfering
or obstructing valves and chambers. During
evolution polarity evolved in the primitive peristaltic
chordate heart. This resulted in dominant pacemaker
activity at one end of the cardiac tube transforming
this heart into a one-way pump. Retinoic
acid may be an important player in the anteroposterior
patterning. As a side issue we mention that
distinct nodal structures (sinus and atrioventricular
node) will develop in mammals only. However,
function and molecular phenotype can already be
assessed in the fish heart. During cardiac development
the nodal phenotype becomes confined to
their classic territories.
Peristaltic hearts exist but not in adult vertebrates.
All regions of such hearts possess poorly
coupled cells and intrinsic automaticity, by which
the depolarizing impulses are slowly propagated
along the tube resulting in matching peristaltic
waves of contraction. The slow contractions do not
necessitate the development of well-developed
contractile structures as are present in the myocardium
of the chambers.
Smart hearts
It is fascinating to appreciate that the basic characteristics
of the muscle cells comprising the peristaltic
heart are essentially similar to those comprising the
nodes in the chamber heart. Therefore, it is useful to
dub the peristaltic heart a nodal heart, because this
facilitates the understanding of the design of the
chamber heart that is derived from it.
A small amount of intercellular coupling is a
necessity for nodal cells, because it permits loading
of these ‘isolated’ cells to a threshold value of
electrical charge sufficiently high to depolarize the
huge mass of adjacent chamber myocardium. This
very same characteristic is responsible for the long
contraction duration (= sphincter function) in those
areas of the embryonic heart that will not, or will
develop later into chamber myocardium. Therefore,
it is not coincidental that the cardiac valves are found
Natuurkundige voordrachten I Nieuwe reeks 89
Ontwikkeling van het bouwplan van het hart
always in nodal regions. This holds true for the sinuatrial
region, atrioventricular junctional region and
also for the outflow region of the heart, provided
the myocardium would persist in this region. In the
shark heart the myocardium surrounding the semilunar
valves (conus) supports valve function and
displays conduction velocities comparable to those
measured in nodal structures. In human, outflow
tract myocardium can extend substantially downstream
from the semilunar valves, and tachycardias
originating from this area have been reported.
At this point we should look at the basic design of
the chamber heart and at the additional functional
requirements of such a heart compared to the peristaltic
heart. Chamber hearts are the more powerful
hearts that can cope with the increasing demands
imposed by the growing resistance of the microcirculation
due to the evolutionary development of liver
and kidneys. The atria became the drainage pool of
the body allowing efficient filling of the ventricles.
The ventricles became the power pumps. Like peristaltic
hearts, chamber hearts are directional because
dominant pacemaking activity remains localized at
the intake of the heart. A minimal additional requirement
of chamber hearts is the need for one-way
valves at both the inflow and the outflow of a chamber.
With relaxation a chamber has to be prevented
from refilling from the downstream compartment,
and with contraction backflow into the preceding
compartment should not occur as well.
In a broad view the vertebrate chamber heart can
be considered as a nodal tube in which at the dorsal
inflow side atria and, at the ventral outflow side,
ventricles have developed (Fig. 1a). The expression
of a number of genes (Anf, Connexin40, Connexin43
and Chisel) illustrates this process (Fig. 1b). However
the domain of expression of most cardiac genes is
broader in the embryonic heart than in the adult
heart, which is sometimes confusing if the expression
of these genes is used as chamber marker
(Fig. 1c). Back to the cardiac building plan, because
the heart tube is S-shaped it has two outer curvatures
at which the atrial and ventricular chambers
develop and two inner curvatures. The essence of
our description is that the original tube remains a
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