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First published online July 20, 2007
Journal of Experimental Biology 210, 2627-2636 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001644
Hemodynamics in the leech: blood flow in two hearts switching between two constriction patterns
1 Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA
30322, USA
2 Institute of Zoology, University of Zürich, CH-8057 Zürich,
Switzerland
* Author for correspondence (e-mail: awennin{at}emory.edu)
Accepted 15 May 2007
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Summary |
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Key words: invertebrate, circulation, cardiac cycle, leech, hemodynamics, blood flow
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Segmented animals with a closed circulatory system such as annelids face yet a
different challenge. Oxygenated and nutrient-rich blood needs to be
distributed to multiple, parallel segmental capillary beds (integument,
musculature, inner organs) and to serial vascular beds (nerve cord, intestine)
with little wiggle room for redistribution to specific vascular beds. In the
giant earthworm Megascolides, which has up to 1000 segments,
circulation time increases from anterior to posterior, effectively dividing
the animal into different circulation zones along the body axis, with the
shortest turnover times in the region of the brain and reproductive organs
(Jones et al., 1994).
In jawed leeches such as Hirudo, the focus of our study, the two
lateral longitudinal vessels serve as hearts. They reflect the segmental body
plan and are made of similar `modules', with each heart segment having up to
two contractile afferent vessels and one efferent vessel
(Fig. 1)
(Boroffka and Hamp, 1969). At
any given time, the hearts on the two sides are coordinated differently along
the body axis, with regular and precipitous switches between two modes of
coordination (Thompson and Stent,
1976a). Our recent quantitative analysis of the constriction
pattern on a segment-by-segment basis showed that the heart segments on the
peristaltic side (termed the `peristaltic heart') constrict rear-to-front
while the heart segments of the contralateral, synchronous side (termed the
`synchronous heart') constrict front-to-rear with shorter intersegmental
delays (Wenning et al.,
2004a). Switches occur every 20–40 beats
(Krahl and Zerbst-Boroffka,
1983; Thompson and Stent,
1976a; Wenning et al.,
2004b). Intravascular systolic/diastolic pressures are about
6.7/0.5 kPa for the peristaltic heart and 3.3/0.5 kPa for the synchronous
heart (Hildebrandt, 1988;
Krahl and Zerbst-Boroffka,
1983). Although myogenic in nature, leech hearts are de
facto neurogenic and require phasic input from 16 pairs of segmental
heart motor neurons for coordination, timing and switching between the
peristaltic and the synchronous mode
(Maranto and Calabrese, 1984a;
Maranto and Calabrese, 1984b).
The heart motor neurons are in turn driven by a well-studied heartbeat central
pattern generator (for reviews, see
Calabrese et al., 1995;
Kristan et al., 2005).
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The apparent flow reversal when switching from the peristaltic into the
synchronous mode (Wenning et al.,
2004a) prompted us to re-visit the hemodynamic properties of the
leech's hearts with respect to the flow into and out of the segmental
`modules' and to longitudinal flow along the body axis. We measured vessel
capacity using corrosion casts of the circulatory system. Measurements of
vessel diameters in situ yielded information about blood volume in
individual heart segments along the body axis. We used optical recordings in
intact animals to avoid dissection, which causes ballooning and cessation of
contractions of exposed blood vessels. We used juvenile leeches because their
weak pigmentation provided good contrast for the flow of red blood. Except for
shorter heartbeat periods than those of adult leeches (juveniles,
4.7±0.7 s; adults, 10.0±3.5 s), the constriction pattern as well
as the switch dynamics are very similar
(Wenning et al., 2004b).
Optical recordings were used to characterize the cardiac cycles of individual
heart segments and to assess volume differences between the peristaltic and
the synchronous heart. Part of the results has previously been published in
abstract form (Wenning and Calabrese,
2003).
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Materials and methods |
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)] were obtained from commercial suppliers (Leeches USA,
Westbury, NY, USA; 0.8–1.5 g) or, for the experiments carried out in
Zürich (Switzerland), from a local pharmacy (2.0–3.0 g). Unfed
juvenile leeches (2–6 months old, 100 mg) were kindly provided by W. B.
Kristan and K. A. French (UCSD, San Diego, CA, USA). Leeches were kept in
artificial pond water at 16°C. Leeches were cold anaesthetized and pinned
through both the anterior and posterior sucker in a stretched position.
Experiments were carried out at room temperature.
Corrosion casts of the vasculature
We assessed vessel capacity in corrosion casts of adult leeches using a
polyurethane resin (PU4ii; vasQtec, Zürich, Switzerland)
(Beckmann et al., 2003;
Krucker et al., 2006). The
resin was diluted with ethylmethylketone (30% w/v) to lower viscosity. Timely
polymerization and minimal shrinking yield elastic casts that retain their
original structure to facilitate post-casting tissue dissection and
pruning.
A longitudinal slit through the body wall between segments 10 and 12 exposed the dorsal vessel. The body wall was forced apart and held in place with small hooks. The dorsal vessel was opened and a flexible polyethylene catheter (o.d. 80–150 µm) forwarded into the vessel lumen. To avoid rupture of the vasculature during pressure injection with the resin, we slowly injected 0.5–1 ml paraformaldehyde [4%, diluted 1:1 with leech saline (mmol l–1): 115 NaCl, 4 KCl, 1.8 CaCl2, 10 glucose, 10 Hepes buffer; pH 7.4] until the fixative returned to the injection site (1–2 min). Resin was injected for about 5 min using a perfusion pump set at 100–200 µl min–1. In complete fills, the resin returned to the injection site and the tissue became rigid.
After polymerization (4–8 h), preparations were digested in 7.5% KOH (w/v; overnight at 55°C). Casts were thoroughly rinsed with water and freeze-dried. For inspection of inner surfaces, a segment of the cast was opened longitudinally and unfolded. Portions of the casts were processed for scanning electron microscopy (SEM) (Hitachi S4000, Naka, Japan) by sputtering with gold.
Measurements of segment length and vessel diameter in adult leeches
Segment length was measured in eight intact, moderately stretched leeches.
In 19 freshly dissected leeches, we measured the diameters of the hearts and
in some animals also the side vessels in maximal diastole and systole. To
minimize dissection time and blood loss, we measured the heart segments in the
anterior and posterior sections separately. Segment 10 was our reference with
its end-diastolic diameter set at 100%.
Video imaging of intact juvenile leeches
In juvenile leeches, we video-imaged the constrictions of, and blood flow
through, the hearts and their side vessels. The method and the analysis of the
optical signals were described previously
(Wenning et al., 2004a). In
brief, leeches were pinned through the anterior and the posterior sucker,
ventral side up, in a stretched position. Imaging an entire juvenile leech
took 10–45 min, capturing 3–6 segments at a time. Video clips were
digitized (Imaging Workbench software, vs. 4; Axon Instruments Inc., Union
City, CA, USA) for the automated analysis of vessel constrictions. Rhythmic
filling and emptying of the vessels with red blood caused light intensity
changes (`optical signals') in user-defined analysis windows drawn around
desired sections of the blood vessels. Absolute values of the digitized
signals depended on the analysis windows' size and on vessel visibility and
were therefore not comparable between different animals. Data analysis was
performed off-line using custom-made MATLAB software (Mathworks, Natick, MA,
USA). We expressed time differences as a percentage of the heartbeat period
(100% phase=heartbeat period).
To describe the cardiac cycle of an individual heart segment, we first determined the minimum (trough) and the maximum (peak) of the optical signal. The following points were then identified: start of diastole (=10% filled), maximal diastole (trough of the optical signal), the attainment of systole (here referred to as `systole'), which was estimated best by the moment in time halfway between maximum diastole and the moment in time of the maximum growth of the optical signal corresponding to emptying, and the end of systole (=90% empty). `10% filled' and `90% empty' correspond to the same value of light intensity of the optical signal but not to the same point in time.
Data are from eight juvenile leeches. Four of those were quiescent, and recordings were stable long enough to cover at least one switch, enabling us to compare the end-diastolic volume and the volume pumped per cycle between coordination modes. We measured the end-diastolic volume as the maximal amplitude of the optical signal and the total volume pumped as the area under the curve between two systolic maxima using Clampfit (Axon Instruments Inc., Molecular Devices Corporation, Sunnyvale, CA, USA).
Statistics and nomenclature
Values are expressed as means of the averages of individual experiments
± s.d. Leeches have 32 segments, some of which are fused to form the
head and tail brains. Segment #1 is assigned to the metameric body segment
innervated by the most anterior (non-cephalic) ganglion of the ventral nerve
cord, and segment #21 to the last metameric segment anterior to the tail
brain.
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). The end-diastolic diameters of the incoming and the single
outgoing vessels in midbody segments 7–14 were (as a percentage of the
corresponding diastolic heart) 60% (±17%; six animals) for the afferent
latero-lateral vessel, 74% (±23%; three animals) for the afferent
latero-dorsal vessel and 37% (±8%; five animals) for the efferent
latero-abdominal vessel. The diameter of the dorsal vessel was 83%
(±12%; four animals) of that of the heart (segment 10). To estimate total blood volume in leeches, we calculated the volume in heart segment 10 (1.2±0.12 µl) using the end-diastolic heart diameter and the segment length of leeches of the same weight class (Fig. 2D). Second, using the average vessel diameters determined for each heart segment from the same animals, we calculated the blood volume of one lateral heart tube as 11.0 µl. Third, using the blood distribution in the different vascular beds determined from the corrosion casts (Fig. 2B), we calculated the total blood volume as being about 120 µl in leeches weighing 1.4±0.3 g, which translates into about 8–9% of the body mass. This value is an estimate; on the one hand, the contractile vessels are overfilled in the casts, while on the other hand, the hearts' S-shape had not been taken into account when calculating the end-diastolic volume (see above).
Filling and emptying of a midbody heart segment
We constructed the cardiac cycles for individual heart segments.
Fig. 3 shows a typical optical
signal for midbody segment 10 and its cardiac cycle. The optical signal
yielded the information for the period, filling, maximal diastole and
emptying. The length of one cardiac cycle is set to 100%. Emptying took up
about 20%, while filling took up about 30%. After emptying, the heart appeared
about 10% filled for half of the cardiac cycle before filling started
again.
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Heart segments 4–18 have two afferent vessels (the latero-lateral and
latero-dorsal vessel, respectively), segments 2, 3 and 19 have one
(Boroffka and Hamp, 1969). The
afferent vessels deliver oxygenated blood from the integumental capillaries
into the heart, are contractile and are on the low pressure side of the
circulatory system (0–0.8 kPa)
(Hildebrandt, 1988)
(Fig. 1). Their orifices have
(passive) valves that are pushed back when the pressure in the heart overcomes
that of the afferent vessels (Hammersen et
al., 1976) (see closed valve in
Fig. 1). The non-muscular
efferent latero-abdominal vessel serves the nephridia and the ventral
musculature (Fig. 1; Fig. S1 in
supplementary material). The neural network of the heart extends to the
initial, muscular part of the latero-abdominal vessel
(Wenning and Cahill, 1986),
which serves as a sphincter (Fig.
1, inset).
The afferent vessels constrict before the hearts
(Boroffka and Hamp, 1969;
Hammersen et al., 1976;
Hildebrandt, 1988). We
quantified the difference between systole in the hearts and in the afferent
vessels (see Materials and methods for the definition of systole and
Fig. 3). Systole in the hearts
was assigned 0% phase. We determined systole in the heart and the afferent
vessels between segments 8 and 16 from six intact, restrained juvenile leeches
(5–15 heartbeat cycles per segment, 1–4 segments per animal). On
average, systole of the afferent vessels led heart systole by
–17.3±3.6% (Fig.
3; horizontal dotted bars) with no difference in the two
coordination modes.
Fig. 4A,B shows the
latero-dorsal vessel and the heart in segment 15 and their constriction
patterns. In these posterior segments, latero-dorsal vessels fuse and form the
latero-dorsal arches (Boroffka and Hamp,
1969). Images taken at four points (a–d) of the cardiac
cycle (Fig. 4C,D) illustrate
the sequence of events. The first image (a) shows a filled latero-dorsal
vessel and a partially filled heart. The latero-dorsal vessel entered systole
first, rapidly filling the heart (a–b). When the heart entered systole,
the valve closed, preventing backflow. During heart systole (c), the
latero-dorsal vessel was already filling again (c–d).
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Blood leaves the heart and enters the segmental circulation through the latero-abdominal vessels present in segments 3–18. Fig. 5 shows optical recordings from the hearts, the efferent latero-abdominal sphincters and the vessels in segment 11 on both sides. In both coordination modes, the latero-abdominal sphincter closed briefly and transiently before heart systole. Closure of the sphincter occurs at about the same time as systole in the afferent vessels (data not shown).
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Flow along the body axis in the peristaltic and the synchronous heart
The relative progression of systole between heart segments along the body
axis did not vary with period and enabled us to average between animals
(Wenning et al., 2004a). The
phase diagram in Fig. 6 shows
the intersegmental and side-to-side coordination of heart segments 3–18
for the peristaltic (magenta) and the contralateral synchronous (blue) heart.
Within one heartbeat cycle, heart segments on both sides complete their
cardiac cycles.
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). As a consequence of this flow pattern,
heart segments 3 and 4 were filled for most of their cardiac cycles while
midbody segments remained partially filled right after their systole for about
50% of the cardiac cycle (Fig.
6; compare segments 4 and 10). Posterior heart segments fill
somewhat earlier in their cardiac cycle (shown for segment 16 in
Fig. 6). Thus, with each
heartbeat, the peristaltic heart delivers the equivalent of several heart
segments into the head region (anterior sucker and head brain).
Systole in the synchronous heart (Fig.
6) traveled rearward, taking up about 30% of the heartbeat cycle
period. Constrictions started in the anterior heart segments with an average
intersegmental delay of –2.7% between heart segments 3 and 13 (range,
0.3 to –3.8%) (Wenning et al.,
2004a). Due to these short intersegmental delays of systole
between adjacent segments, rearward flow is expected to be restricted.
Importantly, the position and the role of the heart sphincter reverse
(Fig. 1). The sphincter is now
in front of the traveling blood column and effectively blocks rearward flow
when that heart segment constricts. Indeed, the prepulse in systolic pressure,
indicative of filling from the adjacent heart segment, disappears upon
switching into the synchronous coordination mode
(Krahl and Zerbst-Boroffka,
1983; Wenning et al.,
2004a). Since the synchronous heart is not filled from adjacent,
i.e. anterior, segments, it should carry less blood. We tested this hypothesis
by measuring the end-diastolic volume (i.e. the peak amplitude) and the total
pumped volume (i.e. the area from peak to peak) of the optical signal. Two
conditions had to be met for a meaningful analysis. First, animals had to be
quiescent since movements distort the optical signal and, second, recordings
needed to span at least one switch in coordination mode to determine the
relative volume change, preferably in both hearts of a given segment since the
absolute values of the optical signal depend on the analysis window size and
the visibility of the heart in that segment of that animal. Of the eight
juveniles used in this study, four met these requirements.
Optical recordings from two different animals are shown in Fig. 7 for anterior (A) and posterior (B) heart segments. Volume differences were largest in midbody segments 5–10, where the volume pumped during one cardiac cycle in an individual heart segment in the synchronous coordination mode was between 50 and 70% of that in the peristaltic mode, and the end-diastolic volume was between 80 and 50% of that in the peristaltic mode (4–15 beats per coordination mode in 2–8 segments per animal; Fig. 7C) with somewhat smaller differences in anterior and posterior segments. Heart segment 3 on the synchronous side is in diastole when the peristaltic heart constricts and may receive blood directly (i.e. not only via the afferent vessels) from the head region, decreasing the volume difference between the two modes. However, the smaller diameter of heart segments 3 and 4 makes the optical signal more susceptible to noise. In segments 17 and posterior, not much blood from adjacent posterior segments contributes to filling because of their almost simultaneous constriction and their taper (Fig. 2C, Fig. 6), and blood volume should be similar on both sides. Indeed, there is no difference in the ratio of the pumped volume (101±5%), and the end-diastolic volume in the synchronous heart is now 89±11% of that of the peristaltic heart (e.g. segment 16 in Fig. 7B,C).
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The role of the latero-dorsal arches
The latero-dorsal vessels in segments 14–18 extend and fuse,
retaining their muscular envelopes over their length, forming the so-called
latero-dorsal arches (Fig. 4A)
(Boroffka and Hamp, 1969). In
addition to receiving oxygenated blood from the integument, they collect
nutrient-rich blood from the intestine. As shown here, these arches provide a
shunt between the dorsal vessel (which gives rise to the major intestinal
vessels) and the hearts. Moreover, because the side-to-side phase differences
between heart systole progressively decrease with a small but consistent phase
advance of the synchronous heart (Fig.
6), there is a bias towards filling the peristaltic heart through
the arches on both sides. Fig.
8A shows optical recordings from both hearts in segment 14 and
from two points of each of the corresponding latero-dorsal arches across a
switch in coordination mode (analysis windows outlined in
Fig. 8B). Systole of the arch
on the synchronous side coincides with filling of the peristaltic heart,
followed by further filling from the ipsilateral, peristaltic side of the
arch. As in the side vessels of more anterior segments, the constriction of
the arches is strictly coordinated with the constriction of the ipsilateral
heart segment.
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Discussion |
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An intriguing feature of leech circulation is the asymmetry in the flow
pattern, with regular, reciprocal and precipitous switches between
rear-to-front (peristaltic) and a steeper front-to-rear (synchronous) wave of
constrictions. Reversal in blood flow has been observed in other animals such
as tunicates (Kriebel, 1968)
and, prominently, in adult holometabolous insects. Here, alternation of flow
direction in the dorsal heart is thought to facilitate the perfusion of
different vascular beds (wings, abdomen, thorax) and to be important for
temperature control (Smits et al.,
2000). In the moth Manduca, cardiac reversal relies on
the alternation of pacemaker dominance of two separate pacemakers for forward
and rearward flow (Dulcis et al.,
2001). Leech heartbeat is shaped by a single central pattern
generator. While temperature regulation is presumably unimportant in an
aquatic species, the high degree of segmentation requires a balance between
perfusion of segmental vascular beds and the distribution of nutrients along
the body axis.
Based on pressure recordings in the hearts and the latero-abdominal
vessels, Hildebrandt concluded that only the synchronous heart delivered blood
into the segmental circulation, and less significant amounts were to leave the
peristaltic heart (Hildebrandt,
1988). This division of labor suggested that the segmental
capillary beds would receive only part-time nutrient-rich blood provided by
the peristaltic heart and, importantly, would require separate neural control
of the latero-abdominal sphincters in the two modes, for which there is no
evidence (Maranto and Calabrese,
1984a; Maranto and Calabrese,
1984b). Regardless of the coordination mode, the sphincters close
briefly just before the hearts enter systole
(Fig. 5), suggesting that both
hearts serve the peripheral circulation. However, since longitudinal flow in
the synchronous heart is restricted due to the location of the heart
sphincters and the fast progression of systole, blood volume is lower in the
synchronous heart, most of which may be forced into the segmental
circulation.
The afferent vessels constrict before the hearts, ensuring their timely
filling. Like the hearts, they seem to be innervated by the segmental heart
motor neurons since intracellular recordings showed that each motor neuron
burst elicited plateau and excitatory junction potentials in the muscle cells
of the afferent vessels (Wenning and
Calabrese, 2003) (A.W., unpublished observations). Systole of the
afferent vessels is tied to that of the hearts, as seen, for example, across a
switch with its `double beat' in the left hemi-segment 14
(Fig. 8). Yet, despite
simultaneous excitation, systole in the afferent vessels precedes heart
systole (Figs 4,
8), presumably because the
ongoing diastolic filling of the hearts in conjunction with their larger
diameter delay constriction (Fig.
2C). Since the optical recordings signal `empty' or `full' –
and not contraction force – they will display this delay as a delay in
emptying.
In segments 14–18, the afferent latero-dorsal vessels form arches
that shunt blood from the dorsal vessel to the hearts
(Fig. 8). Heart systole on the
synchronous side is leading that on the peristaltic side by a decreasing but
consistent margin (Fig. 6).
These small side-to-side phase differences support unidirectional shunting
towards the peristaltic heart because systole in the arches on the peristaltic
side occurs during systole of the synchronous heart. Shunts allow blood to
return to the heart faster, enhancing central circulation, and are common in
highly segmented animals (Jones et al.,
1994). In leeches, these posterior shunts provide an additional
bonus because ingested blood is stored in a large crop spanning the entire
animal, with the intestine confined to segments 14 and posterior. Shunting
blood across the arches into the peristaltic heart facilitates the flow of
nutrient-rich blood to anterior segments yet still allows perfusion of the
posterior sucker and the tail brain.
Blood flows rearward in the dorsal and ventral vessel. A single dorsal
vessel forms in segment 3 (Boroffka and
Hamp, 1969) while the ventral vessel forms around the brain and
the subesophageal ganglion and encloses the chain of segmental ganglia
(Fig. 2A; Fig. S1 in
supplementary material). In the front segments, there are anastomoses between
the ventral and the dorsal vessel. In time-lapse videos, Hildebrandt showed
that rearward flow in the dorsal vessel is pulsatile and flow oscillates
between 
0.5 and 5 mm s–1 with the period of one cardiac
cycle (Hildebrandt, 1988).
Reasoning that the front heart segments may not discharge enough blood to fill
the dorsal and the ventral vessel and that the highest pressure in the dorsal
vessel, recorded in segment 10, coincides with the pressure peak in the
synchronous heart, recorded in segment 6, Hildebrandt concluded that the
dorsal vessel is filled mainly by the synchronous heart via the
latero-abdominal vessels and the segmental capillary beds. We find it
difficult to envision that pulsatile flow and pressure (between 0.9 and 1.9
kPa) (Hildebrandt, 1988) are
sustained after blood has passed through several capillary beds. We show that
only the peristaltic heart delivers blood to the head region
(Fig. 6) and propose that the
dorsal and the ventral vessel are filled predominantly by the peristaltic
heart. Larger phase lags and the supportive action of the heart sphincter
allow the peristaltic heart to propel and discharge an amount of blood into
the head region equivalent to the volume of multiple heart segments in one
peristaltic wave of systoles (minus the blood exiting into the segmental
circulation). From the peristaltic heart, blood flows through numerous
anastomoses into the dorsal and ventral vessel. This scenario explains the
pulsatile flow and the oscillating pressure pulses observed in the dorsal
vessel (Hildebrandt,
1988).
Regulation of leech heart performance
Any perturbations that affect the heart rate and/or switching must do so by
altering the properties of the neurons constituting the heartbeat central
pattern generator, which controls the 16 pairs of segmental heart motor
neurons (Calabrese, 1977;
Gramoll et al., 1994;
Thompson and Stent, 1976b).
Heart rate is inversely related to temperature and can be modulated by
stimulating identified neurons (Arbas,
1984; Arbas and Calabrese,
1990). Peptides (e.g. FMRFamide, myomodulin) increase the heart
rate through interaction with the pattern generator
(Kuhlman et al., 1985;
Masino and Calabrese, 2002;
Tobin and Calabrese, 2005).
Leeches recover from prolonged periods of hypoxia (72 h)
(Schmidt and Zerbst-Boroffka,
1993) and lower their heart rate in response to lower ambient
oxygen (Davis, 1986).
Phase relations are invariant across changes in burst period in the entire
system – from pattern generator to heart constrictions
(Norris et al., 2006;
Wenning et al., 2004a). Since
the contractile vessels of one hemisegment share the excitatory drive, the
sequence of events – afferent vessel constriction, sphincter closure,
heart systole – is fixed and not coordination mode-specific. So far, all
work on the circulatory system has been done in quiescent, restrained leeches.
It will be interesting to study whether and, if so, how hemodynamics are
modified to meet different metabolic demands such as in locomotion and
feeding. Sustaining flow through the capillary beds (Fig. S1 in supplementary
material) – some of them in series – as well as avoiding pooling,
and stagnant anoxia are challenges that leeches might meet using behavioral
responses by swimming a few lapses or doing a few stretches.
The leech hearts' constriction pattern is bilaterally asymmetric, but both hearts perform each task – albeit at different times. Both hearts serve the segmental circulation, but the peristaltic heart additionally provides the propulsive force for longitudinal flow, forward in the heart and rearward in the dorsal and ventral vessel. The heart segments' design and the different intersegmental coordination of constrictions rather than separate (neural) control of the sphincters allow the division of labor between the peristaltic and synchronous heart. Regular switching between coordination modes may prevent asymmetries in volume distribution and ensures flow of nutrient-rich blood from the intestinal region to anterior vascular beds on both sides.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Beckmann, N., Schuler, A., Mueggler, T., Meyer, E. P.,
Wiederhold, K. H., Staufenbiel, M. and Krucker, T. (2003).
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Boroffka, I. and Hamp, R. (1969). Topographie des Kreislaufsystems und Zirkulation bei Hirudo medicinalis. Z. Morph. Ökol. Tiere 64,59 -76.
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Hammersen, F., Staudte, H.-W. and Möhring, E. (1976). Studies of the fine structure of invertebrate blood vessels. II. The valves of the lateral sinus of the leech, Hirudo medicinalis L. Cell Tissue Res. 172,405 -423.[CrossRef][Medline]
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Jones, D. R., Bushnell, P. G., Evans, B. K. and Baldwin, J. (1994). Circulation in the Giant Gippland earthworm Megascolides australis. Physiol. Zool. 67,1383 -1401.
Krahl, B. and Zerbst-Boroffka, I. (1983). Blood
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Kriebel, M. E. (1968). Studies on
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