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

Johannes D Veldhuis, M. Straume, A. Iranmanesh, T. Mulligan, C. Jaffe, A. Barkan, M. L. Johnson, S. Pincus

Research output: Contribution to journalArticle

120 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume280
Issue number3 49-3
StatePublished - 2001
Externally publishedYes

Fingerprint

Secretory Pathway
Entropy
Insulin-Like Growth Factor I
Testosterone
Hormones
Growth Hormone-Releasing Hormone
Neurosecretory Systems
Luteinizing Hormone
Gonadotropin-Releasing Hormone
Growth Hormone

Keywords

  • ACTH
  • Cortisol
  • Growth hormone
  • Hormone
  • Insulin -like growth factor type I
  • Luteinizing hormone
  • Neuroregulation
  • Testosterone
  • Thyrotropin
  • Thyroxine

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Secretory process regularity monitors neuroendocrine feedback and feedforward signaling strength in humans. / Veldhuis, Johannes D; Straume, M.; Iranmanesh, A.; Mulligan, T.; Jaffe, C.; Barkan, A.; Johnson, M. L.; Pincus, S.

In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology, Vol. 280, No. 3 49-3, 2001.

Research output: Contribution to journalArticle

Veldhuis, JD, Straume, M, Iranmanesh, A, Mulligan, T, Jaffe, C, Barkan, A, Johnson, ML & Pincus, S 2001, 'Secretory process regularity monitors neuroendocrine feedback and feedforward signaling strength in humans', American Journal of Physiology - Regulatory Integrative and Comparative Physiology, vol. 280, no. 3 49-3.
Veldhuis, Johannes D ; Straume, M. ; Iranmanesh, A. ; Mulligan, T. ; Jaffe, C. ; Barkan, A. ; Johnson, M. L. ; Pincus, S. / Secretory process regularity monitors neuroendocrine feedback and feedforward signaling strength in humans. In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology. 2001 ; Vol. 280, No. 3 49-3.
@article{1ee4036da51d4901803bd4baf1de4ddc,
title = "Secretory process regularity monitors neuroendocrine feedback and feedforward signaling strength in humans",
abstract = "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.",
keywords = "ACTH, Cortisol, Growth hormone, Hormone, Insulin -like growth factor type I, Luteinizing hormone, Neuroregulation, Testosterone, Thyrotropin, Thyroxine",
author = "Veldhuis, {Johannes D} and M. Straume and A. Iranmanesh and T. Mulligan and C. Jaffe and A. Barkan and Johnson, {M. L.} and S. Pincus",
year = "2001",
language = "English (US)",
volume = "280",
journal = "American Journal of Physiology - Renal Fluid and Electrolyte Physiology",
issn = "1931-857X",
publisher = "American Physiological Society",
number = "3 49-3",

}

TY - JOUR

T1 - Secretory process regularity monitors neuroendocrine feedback and feedforward signaling strength in humans

AU - Veldhuis, Johannes D

AU - Straume, M.

AU - Iranmanesh, A.

AU - Mulligan, T.

AU - Jaffe, C.

AU - Barkan, A.

AU - Johnson, M. L.

AU - Pincus, S.

PY - 2001

Y1 - 2001

N2 - 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.

AB - 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.

KW - ACTH

KW - Cortisol

KW - Growth hormone

KW - Hormone

KW - Insulin -like growth factor type I

KW - Luteinizing hormone

KW - Neuroregulation

KW - Testosterone

KW - Thyrotropin

KW - Thyroxine

UR - http://www.scopus.com/inward/record.url?scp=0035003193&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0035003193&partnerID=8YFLogxK

M3 - Article

C2 - 11171650

AN - SCOPUS:0035003193

VL - 280

JO - American Journal of Physiology - Renal Fluid and Electrolyte Physiology

JF - American Journal of Physiology - Renal Fluid and Electrolyte Physiology

SN - 1931-857X

IS - 3 49-3

ER -