Spike firing allometry in avian intrapulmonary chemoreceptors: matching neural code to body size

Author:

Hempleman S. C.1,Kilgore D. L.2,Colby C.3,Bavis R. W.4,Powell F. L.5

Affiliation:

1. Department of Biological Sciences, Northern Arizona University, Flagstaff,AZ 86011-5640 USA

2. Division of Biological Sciences, The University of Montana, Missoula, MT 59812 USA

3. Department of Respiratory Care, Boise State University, Boise, ID 83725 USA

4. Department of Biology, Bates College, Lewiston, ME 04240 USA

5. Division of Physiology, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0623 USA

Abstract

SUMMARY Biological rates in small animals are usually higher than those in large animals, yet the maximal rate of action potential (spike) generation in sensory neurons encoding rate functions is similar in all animals, due to the conserved genetics of voltage-gated ion channels. Therefore, sensory signals that vary at rates approaching maximal spike generation rate, as might occur in animals of diminished body size, may require specialized spike coding to convey this information. To test whether spike coding scales allometrically in sensory neurons monitoring signals that change frequency with body size, we recorded action potentials from 70 avian intrapulmonary chemoreceptors (IPC),respiratory neurons that detect lung CO2 changes during breathing,in five different avian species ranging in size from body mass Mb = 0.045 kg (lovebirds) to 5.23 kg (geese). Since breathing frequency scales approximately to Mb–1/4 (higher in small birds, lower in large birds), we reasoned that IPC discharge frequencies may also scale to maintain spike information transmission within each breath. We found that phasic action potential discharge pattern, as quantified by the peak discharge rate and the magnitude of spike frequency adaptation, scaled between Mb–0.22 and Mb–0.26, like breathing rate(P<0.05). Previously published values of peak discharge rate in IPC also fit this allometric relationship. We suggest that mass-dependent scaling of neural coding may be necessary for preserving information transmission with decreasing body size.

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

Reference24 articles.

1. Berger, P. J., Tallman, R. D. and Kunz, A. L.(1980). Discharge of intrapulmonary chemoreceptors and its modulation by rapid FICO2 changes in decerebrate ducks Respir. Physiol.42,123-130.

2. Brown, J. H. and West, G. B. (2000). Scaling in Biology. New York: Oxford University Press.

3. Burger, R. E., Coleridge, J. C. G., Coleridge, H. M., Nye, P. C. G., Powell, F. L., Ehlers, C. and Banzett, R. B.(1976). Chemoreceptors in the paleopulmonic lung of the emu:discharge patterns during cyclic ventilation. Respir. Physiol.28,249-259.

4. Calder, W. A. (1996). Size,Function, and Life History. Mineola, NY: Dover.

5. Fedde, M. R. and Scheid, P. (1976). Intrapulmonary CO2 receptors in the duck: IV Discharge pattern of the population during a respiratory cycle. Respir. Physiol.26,223-227.

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