From Malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants

Norman Pecoraro, Mary F. Dallman, James P. Warne, Abigail B. Ginsberg, Kevin D. Laugero, Susanne E. la Fleur, Hani Houshyar, Francisca Gomez, Aditi Bhargava, Susan F. Akana

Research output: Contribution to journalArticle

98 Citations (Scopus)

Abstract

The hypothalamo-pituitary-adrenal (HPA) axis is the critical mediator of the vertebrate stress response system, responding to environmental stressors by maintaining internal homeostasis and coupling the needs of the body to the wants of the mind. The HPA axis has numerous complex drivers and highly flexible operating characterisitics. Major drivers include two circadian drivers, two extra-hypothalamic networks controlling top-down (psychogenic) and bottom-up (systemic) threats, and two intra-hypothalamic networks coordinating behavioral, autonomic, and neuroendocrine outflows. These various networks jointly and flexibly control HPA axis output of periodic (oscillatory) functions and a range of adventitious systemic or psychological threats, including predictable daily cycles of energy flow, actual metabolic deficits over many time scales, predicted metabolic deficits, and the state-dependent management of post-prandial responses to feeding. Evidence is provided that reparation of metabolic derangement by either food or glucocorticoids results in a metabolic signal that inhibits HPA activity. In short, the HPA axis is intimately involved in managing and remodeling peripheral energy fluxes, which appear to provide an unidentified metabolic inhibitory feedback signal to the HPA axis via glucocorticoids. In a complementary and perhaps a less appreciated role, adrenocortical hormones also act on brain to provide not only feedback, but feedforward control over the HPA axis itself and its various drivers, as well as coordinating behavioral and autonomic outflows, and mounting central incentive and memorial networks that are adaptive in both appetitive and aversive motivational modes. By centrally remodeling the phenotype, the HPA axis provides ballistic and predictive control over motor outflows relevant to the type of stressor. Evidence is examined concerning the global hypothesis that the HPA axis comprehensively induces integrative phenotypic plasticity, thus remodeling the body and its governor, the brain, to yoke the needs of the body to the wants of the mind. Adverse side effects of this yoking under conditions of glucocorticoid excess are discussed.

Original languageEnglish (US)
Pages (from-to)247-340
Number of pages94
JournalProgress in Neurobiology
Volume79
Issue number5-6
DOIs
StatePublished - Aug 2006
Externally publishedYes

Fingerprint

Glucocorticoids
Phenotype
Brain
Meals
Vertebrates
Motivation
Homeostasis
Hormones
Psychology
Food

Keywords

  • Energy balance
  • Hypothalamo-pituitary-adrenal axis
  • Motivation
  • Phenotypic plasticity
  • Stress

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Pecoraro, N., Dallman, M. F., Warne, J. P., Ginsberg, A. B., Laugero, K. D., la Fleur, S. E., ... Akana, S. F. (2006). From Malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants. Progress in Neurobiology, 79(5-6), 247-340. https://doi.org/10.1016/j.pneurobio.2006.07.004

From Malthus to motive : How the HPA axis engineers the phenotype, yoking needs to wants. / Pecoraro, Norman; Dallman, Mary F.; Warne, James P.; Ginsberg, Abigail B.; Laugero, Kevin D.; la Fleur, Susanne E.; Houshyar, Hani; Gomez, Francisca; Bhargava, Aditi; Akana, Susan F.

In: Progress in Neurobiology, Vol. 79, No. 5-6, 08.2006, p. 247-340.

Research output: Contribution to journalArticle

Pecoraro, N, Dallman, MF, Warne, JP, Ginsberg, AB, Laugero, KD, la Fleur, SE, Houshyar, H, Gomez, F, Bhargava, A & Akana, SF 2006, 'From Malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants', Progress in Neurobiology, vol. 79, no. 5-6, pp. 247-340. https://doi.org/10.1016/j.pneurobio.2006.07.004
Pecoraro N, Dallman MF, Warne JP, Ginsberg AB, Laugero KD, la Fleur SE et al. From Malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants. Progress in Neurobiology. 2006 Aug;79(5-6):247-340. https://doi.org/10.1016/j.pneurobio.2006.07.004
Pecoraro, Norman ; Dallman, Mary F. ; Warne, James P. ; Ginsberg, Abigail B. ; Laugero, Kevin D. ; la Fleur, Susanne E. ; Houshyar, Hani ; Gomez, Francisca ; Bhargava, Aditi ; Akana, Susan F. / From Malthus to motive : How the HPA axis engineers the phenotype, yoking needs to wants. In: Progress in Neurobiology. 2006 ; Vol. 79, No. 5-6. pp. 247-340.
@article{3f60628af4124792aad64c7ebe4ea011,
title = "From Malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants",
abstract = "The hypothalamo-pituitary-adrenal (HPA) axis is the critical mediator of the vertebrate stress response system, responding to environmental stressors by maintaining internal homeostasis and coupling the needs of the body to the wants of the mind. The HPA axis has numerous complex drivers and highly flexible operating characterisitics. Major drivers include two circadian drivers, two extra-hypothalamic networks controlling top-down (psychogenic) and bottom-up (systemic) threats, and two intra-hypothalamic networks coordinating behavioral, autonomic, and neuroendocrine outflows. These various networks jointly and flexibly control HPA axis output of periodic (oscillatory) functions and a range of adventitious systemic or psychological threats, including predictable daily cycles of energy flow, actual metabolic deficits over many time scales, predicted metabolic deficits, and the state-dependent management of post-prandial responses to feeding. Evidence is provided that reparation of metabolic derangement by either food or glucocorticoids results in a metabolic signal that inhibits HPA activity. In short, the HPA axis is intimately involved in managing and remodeling peripheral energy fluxes, which appear to provide an unidentified metabolic inhibitory feedback signal to the HPA axis via glucocorticoids. In a complementary and perhaps a less appreciated role, adrenocortical hormones also act on brain to provide not only feedback, but feedforward control over the HPA axis itself and its various drivers, as well as coordinating behavioral and autonomic outflows, and mounting central incentive and memorial networks that are adaptive in both appetitive and aversive motivational modes. By centrally remodeling the phenotype, the HPA axis provides ballistic and predictive control over motor outflows relevant to the type of stressor. Evidence is examined concerning the global hypothesis that the HPA axis comprehensively induces integrative phenotypic plasticity, thus remodeling the body and its governor, the brain, to yoke the needs of the body to the wants of the mind. Adverse side effects of this yoking under conditions of glucocorticoid excess are discussed.",
keywords = "Energy balance, Hypothalamo-pituitary-adrenal axis, Motivation, Phenotypic plasticity, Stress",
author = "Norman Pecoraro and Dallman, {Mary F.} and Warne, {James P.} and Ginsberg, {Abigail B.} and Laugero, {Kevin D.} and {la Fleur}, {Susanne E.} and Hani Houshyar and Francisca Gomez and Aditi Bhargava and Akana, {Susan F.}",
year = "2006",
month = "8",
doi = "10.1016/j.pneurobio.2006.07.004",
language = "English (US)",
volume = "79",
pages = "247--340",
journal = "Progress in Neurobiology",
issn = "0301-0082",
publisher = "Elsevier Limited",
number = "5-6",

}

TY - JOUR

T1 - From Malthus to motive

T2 - How the HPA axis engineers the phenotype, yoking needs to wants

AU - Pecoraro, Norman

AU - Dallman, Mary F.

AU - Warne, James P.

AU - Ginsberg, Abigail B.

AU - Laugero, Kevin D.

AU - la Fleur, Susanne E.

AU - Houshyar, Hani

AU - Gomez, Francisca

AU - Bhargava, Aditi

AU - Akana, Susan F.

PY - 2006/8

Y1 - 2006/8

N2 - The hypothalamo-pituitary-adrenal (HPA) axis is the critical mediator of the vertebrate stress response system, responding to environmental stressors by maintaining internal homeostasis and coupling the needs of the body to the wants of the mind. The HPA axis has numerous complex drivers and highly flexible operating characterisitics. Major drivers include two circadian drivers, two extra-hypothalamic networks controlling top-down (psychogenic) and bottom-up (systemic) threats, and two intra-hypothalamic networks coordinating behavioral, autonomic, and neuroendocrine outflows. These various networks jointly and flexibly control HPA axis output of periodic (oscillatory) functions and a range of adventitious systemic or psychological threats, including predictable daily cycles of energy flow, actual metabolic deficits over many time scales, predicted metabolic deficits, and the state-dependent management of post-prandial responses to feeding. Evidence is provided that reparation of metabolic derangement by either food or glucocorticoids results in a metabolic signal that inhibits HPA activity. In short, the HPA axis is intimately involved in managing and remodeling peripheral energy fluxes, which appear to provide an unidentified metabolic inhibitory feedback signal to the HPA axis via glucocorticoids. In a complementary and perhaps a less appreciated role, adrenocortical hormones also act on brain to provide not only feedback, but feedforward control over the HPA axis itself and its various drivers, as well as coordinating behavioral and autonomic outflows, and mounting central incentive and memorial networks that are adaptive in both appetitive and aversive motivational modes. By centrally remodeling the phenotype, the HPA axis provides ballistic and predictive control over motor outflows relevant to the type of stressor. Evidence is examined concerning the global hypothesis that the HPA axis comprehensively induces integrative phenotypic plasticity, thus remodeling the body and its governor, the brain, to yoke the needs of the body to the wants of the mind. Adverse side effects of this yoking under conditions of glucocorticoid excess are discussed.

AB - The hypothalamo-pituitary-adrenal (HPA) axis is the critical mediator of the vertebrate stress response system, responding to environmental stressors by maintaining internal homeostasis and coupling the needs of the body to the wants of the mind. The HPA axis has numerous complex drivers and highly flexible operating characterisitics. Major drivers include two circadian drivers, two extra-hypothalamic networks controlling top-down (psychogenic) and bottom-up (systemic) threats, and two intra-hypothalamic networks coordinating behavioral, autonomic, and neuroendocrine outflows. These various networks jointly and flexibly control HPA axis output of periodic (oscillatory) functions and a range of adventitious systemic or psychological threats, including predictable daily cycles of energy flow, actual metabolic deficits over many time scales, predicted metabolic deficits, and the state-dependent management of post-prandial responses to feeding. Evidence is provided that reparation of metabolic derangement by either food or glucocorticoids results in a metabolic signal that inhibits HPA activity. In short, the HPA axis is intimately involved in managing and remodeling peripheral energy fluxes, which appear to provide an unidentified metabolic inhibitory feedback signal to the HPA axis via glucocorticoids. In a complementary and perhaps a less appreciated role, adrenocortical hormones also act on brain to provide not only feedback, but feedforward control over the HPA axis itself and its various drivers, as well as coordinating behavioral and autonomic outflows, and mounting central incentive and memorial networks that are adaptive in both appetitive and aversive motivational modes. By centrally remodeling the phenotype, the HPA axis provides ballistic and predictive control over motor outflows relevant to the type of stressor. Evidence is examined concerning the global hypothesis that the HPA axis comprehensively induces integrative phenotypic plasticity, thus remodeling the body and its governor, the brain, to yoke the needs of the body to the wants of the mind. Adverse side effects of this yoking under conditions of glucocorticoid excess are discussed.

KW - Energy balance

KW - Hypothalamo-pituitary-adrenal axis

KW - Motivation

KW - Phenotypic plasticity

KW - Stress

UR - http://www.scopus.com/inward/record.url?scp=33748893078&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33748893078&partnerID=8YFLogxK

U2 - 10.1016/j.pneurobio.2006.07.004

DO - 10.1016/j.pneurobio.2006.07.004

M3 - Article

C2 - 16982128

AN - SCOPUS:33748893078

VL - 79

SP - 247

EP - 340

JO - Progress in Neurobiology

JF - Progress in Neurobiology

SN - 0301-0082

IS - 5-6

ER -