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First published online March 12, 2009
Journal of Experimental Biology 212, 906-913 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.020529
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The basis of vagal efferent control of heart rate in a neotropical fish, the pacu, Piaractus mesopotamicus

E. W. Taylor1,2,*, C. A. C. Leite1, L. H. Florindo1, T. Beläo1 and F. T. Rantin1

1 Department of Physiological Sciences, Federal University of São Carlos (UFSCar), São Carlos, SP, Brazil
2 School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK


Figure 1
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  		Fig. 1. (A) The rostro-caudal distribution in the brainstem of P. mesopotamicus of cell bodies of respiratory visceral motor neurones (RVMN) supplying axons to the mandibular Vth, opercular VIIth, branchial IXth, and 1st and 4th branchial Xth, together with cardiac vagal preganglionic neurons (CVPN) supplying axons to the cardiac vagus. Data are taken from fish with the best fills (largest number of labelled cell bodies). (B) Transverse section of the brainstem 1.33 mm rostral of obex. The cell bodies of the CVPN that supply the cardiac branch of the right vagus are stained with the fluorescent tracer True Blue and the respiratory motor neurons that supply the 4th branchial branch of the left vagus are stained with Fluorogold. They are located either side of the 4th ventricle (V). Scale bar, 100 µm.

 

Figure 2
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  		Fig. 2. A trace of opercular movements together with integrated efferent activity recorded from cranial nerves V, mandibular; IX, branchial; X, 1st and 2nd branchial, and 4th cardiac. Each is aligned with simultaneous recordings of opercular movements. The vertical lines mark the estimated onset of bursts in the cardiac nerve and reveal that this is early in the sequence of activities in all nerves. The `noisy' trace recorded from the cardiac nerve reflects the occurrence of spontaneously active, non-bursting units.

 

Figure 3
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  		Fig. 3. Mean duration (±s.d.) of the interval between each onset (filled diamonds) or peak (filled squares) of the burst activity in respiratory branches of cranial nerves V, IX and X or the cardiac branch of X and the peak of the succeeding opercular movement (time=0). The cartoon at the top of the figure indicates the derivation of the points plotted below, with the upper trace being opercular movement and the lower trace a sample of activity in the Vth cranial nerve. The letters a–e denote significantly similar groups of mean values. The peaks of activity in the cardiac nerve are concurrent with activity in the Vth cranial nerve and both anticipate activity in the IXth and 1st, 2nd and 3rd respiratory branches of the Xth.

 

Figure 4
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  		Fig. 4. Effects of central electrical stimulation of the IXth, Xth, VIIth and Vth cranial nerves on heart rate, measured as arterial blood pressure (Pa, mmHg). The period of stimulation is indicated by the horizontal bar above or beneath each trace and the stimulation parameters are given below each trace. The initial, intrinsic heart rate (beats min–1), followed by the bursting rate of the electrical stimuli and the consequent heart rate are given above each trace. (A) Continuous stimulation of the IXth cranial nerve caused the heart to stop. (B) Phasic stimulation of the IXth initially inhibited then recruited the heart. (C) At a higher bursting frequency the heart slowed to one-third of the rate of stimulation of the IXth. (D) Heart recruited by phasic stimulation of the 1st respiratory branch of the Xth. (E) Heart recruited by phasic stimulation of the facial branch of the VIIth. (F) Electrical stimulation of the Vth cranial nerve was without effect on the heart.

 

Figure 5
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  		Fig. 5. Entrainment of fH by peripheral electrical stimulation of the right cardiac vagus either with continuous trains of stimuli or with trains of brief pulses (0.2–0.3 s) of impulses (1–2 ms; 20–40 Hz). Heart rate was recorded as blood pressure (Pa, mmHg). Pre-stimulation fH and the stimulus frequency plus the imposed fH are given immediately above each trace (beats min–1). The periods of stimulation are indicated by the horizontal bars at the base of the traces and the stimulus parameters are given either above or below these bars. (A) Cardiac arrest during continuous stimulation. (B) Entrainment at a rate slower than the intrinsic fH. (C) Entrainment at a rate faster than the intrinsic fH. (D) Entrainment by every 4th burst of stimuli.

 

Figure 6
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  		Fig. 6. Graphs showing the range over which heart rate (fH) of P. mesopotamicus (four fish, P1, P2, P3 and P4) was entrained by brief (0.2–0.3 s) bursts of electrical stimuli (1–2 ms pulses at 20–40 Hz) delivered down the peripheral cut end of the right cardiac vagus at rates (fS) between 40 and 180 bursts min–1. Open symbols denote the pre-stimulation fH of each fish and filled symbols the entrained rates. Points deviating from the central line denote different ratios between fH and fS, which are indicated near each point. Points labelled B, C and D are taken from the traces illustrated in Fig. 5A–D. Values for fish P1 and P2 are plotted separately from those for P3 and P4 for greater clarity.

 

Figure 7
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  		Fig. 7. Ranges of stimulation frequency over which the heartbeat was recruited by peripheral stimulation of the cardiac nerve (from the 4th branch of the Xth cranial) or by central stimulation of the opercular branch of the VIIth, branchial (respiratory) branch of the IXth or the 1st and 4th branchial branches of the Xth cranial nerves. The thick bars denote 1:1 recruitment, while the thin extensions denote recruitment to rates higher or lower than the stimulation frequency, with x being a whole number between 2 and 6. In the cardiac denervated fish (lower trace) intrinsic heart rate was 79±3 beats min–1.

 

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© The Company of Biologists Ltd 2009