Ectothermic animals don't thrive in the cold: low temperature slows down the heart rate, which tends to decrease its output and makes animals slow and sluggish. However, some fish maintain an active lifestyle in the cold. Upon prolonged exposure to low temperature, these fish recruit compensatory mechanisms that bypass the depressive effect of cold temperature on heart rate, enabling the heart to continue to beat at a high rate and precluding an active lifestyle.
The fish heart beats independent of external stimulation due to the tightly regulated firing of action potentials (APs) from a specialized set of heart muscle cells called the pacemaker. This regular firing results from coordinated ion movements in the muscle cells. The cold-induced, compensatory increase in heart rate could be due to alterations in humoral and neural regulation of cardiac pacemaker activity and/or modification of the ionic currents underlying the regular AP firing in the pacemaker.
Jaako Haverinen and Matti Vornanen of the University of Joensuu, Finland,were interested in determining if and how thermal compensation of the rainbow trout (Oncorhynchus mykiss) heart occurs at the level of the primary pacemaker cells. Because the exact location of the pacemaker cells in the fish heart is not known, the researchers first located the pacemaker region of the fish heart by systematically impaling spontaneously contracting fish hearts with sharp microelectrodes to record APs. These have a specific shape depending on which heart region they are recorded from. Using this technique,and examining the heart tissue, the team discovered that the primary pacemaker in the rainbow trout heart is located in a small ring of tissue between the sinus venosus, the first chamber of a fish's heart, and the atrium.
Armed with this knowledge, the team then enzymatically isolated individual pacemaker cells to find out if cold compensation occurred at the cellular level. Using patch-clamping, the team recorded APs from isolated pacemaker cells from both 4°C (cold)- and 18°C (warm)-acclimated fish at the common temperature of 11°C and found that the duration of pacemaker APs was shorter and the intrinsic pace-making rate higher in cold-compared to warm-acclimated trout, showing that at least part of the compensatory increase in heart rate is inherent to the pacemaker cells.
Finally, to understand which ionic mechanisms were responsible for the cold-induced changes in pacemaker AP shape and frequency, the team compared APs recorded from spontaneously contracting pacemaker tissue preparations from warm- and cold-acclimated fish. They added chemical blockers specific to two systems: sarcoplasmic reticulum calcium ion (Ca2+) cycling and the movement of potassium ions (K+) through channels called delayed rectifier K+ channels. Both of these ionic mechanisms are implicated as being important for cardiac pacemaking in mammals and are enhanced in cold-acclimated trout.
The team found that blocking sarcoplasmic reticulum Ca2+ cycling did not modify pacemaker AP shape or frequency in cold-acclimated tissue. This, they argue, eliminates the possibility that this mechanism underlies the compensatory increase of heart rate. By contrast, the team discovered that the movement of K+ increased in the cold and could be important for increasing heart rate. When they blocked the K+ channel at the common temperature of 11°C, pacemaker AP frequency and duration decreased more in warm-acclimated preparations than in cold-acclimated ones. The team explains that the greater flow of K+ in pacemaker cells of cold-acclimated trout should theoretically shorten AP duration, increase AP discharge frequency and thus increase heart rate.