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Am J Physiol Regul Integr Comp Physiol 280: R721-R729, 2001;
0363-6119/01 $5.00
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Vol. 280, Issue 3, R721-R729, March 2001

Secretory process regularity monitors neuroendocrine feedback and feedforward signaling strength in humans

J. D. Veldhuis1, M. Straume1, A. Iranmanesh2, T. Mulligan3, C. Jaffe4, A. Barkan4, M. L. Johnson1, and S. Pincus5

1 Division of Endocrinology, Departments of Internal Medicine and Pharmacology, General Clinical Research Center, Center for Biomathematical Technology, University of Virginia School of Medicine, Charlottesville 22908-0202; 2 Endocrine Section, Medical Service, Salem Veterans Affairs Medical Center, Salem 24153; 3 Geriatrics and Extended Care Service, McGuire Veterans Affairs Medical Center, Richmond, Virginia 23249; 4 Endocrine Section, Medical Service, Veterans Affairs Medical Center, Ann Arbor, Michigan 48105; and 5 Guilford, Connecticut 06437

The present experiments examine the neuroregulatory hypothesis that the degree of sample-by-sample regularity of hormone output by an interlinked hypothalamopituitary target-organ system monitors the strength of feedback and/or feedforward signaling. To test this postulate and assess its generality, we implemented a total of nine thematically complementary perturbation experiments. In particular, we altered feedback or feedforward signaling selectively in two distinct neuroendocrine systems; namely, the growth hormone (GH) insulin-like growth factor type I (IGF-I) and the luteinizing hormone-testosterone axes. Four experimental paradigms comprised preferential reduction vs. enhancement of IGF-I or testosterone feedback signal strength; and, conversely, five others entailed selective attenuation vs. augmentation of GH-releasing hormone and gonadotropin-releasing hormone feedforward signal intensity. In these independent interventions, quantitation of subordinate (nonpulsatile) secretory pattern reproducibility via the approximate entropy statistic unmasked salient changes (P values typically <10-3) in the conditional regularity of serial hormone output with high consistency (96-100%). In particular, approximate entropy quantified degradation of secretory subpattern orderliness under either muted feedback restraint or heightened feedforward drive. Assuming valid interpretation of the biological constraints imposed, these experimental observations coincide with earlier reductionist mathematical predictions, wherein increased irregularity of coupled parameter output mirrors attenuated feedback and/or augmented feedforward coupling within an integrative system.

neuroregulation; growth hormone; luteinizing hormone; insulin-like growth factor type I; testosterone; thyrotropin; thyroxine; ACTH; cortisol; hormone


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