The fundamental organization of cardiac mitochondria as a network of coupled oscillators

Miguel Antonio Aon, Sonia Cortassa, Brian O'Rourke

Research output: Contribution to journalArticle

Abstract

Mitochondria can behave as individual oscillators whose dynamics may obey collective, network properties. We have shown that cardiomyocytes exhibit high-amplitude, self-sustained, and synchronous oscillations of bioenergetic parameters when the mitochondrial network is stressed to a critical state. Computational studies suggested that additional low-amplitude, high-frequency oscillations were also possible. Herein, employing power spectral analysis, we show that the temporal behavior of mitochondrial membrane potential (ΔΨm) in cardiomyocytes under physiological conditions is oscillatory and characterized by a broad frequency distribution that obeys a homogeneous power law (1/fβ) with a spectral exponent, β = 1.74. Additionally, relative dispersional analysis shows that mitochondrial oscillatory dynamics exhibits long-term memory, characterized by an inverse power law that scales with a fractal dimension (Df) of 1.008, distinct from random behavior (Df = 1.5), over at least three orders of magnitude. Analysis of a computational model of the mitochondrial oscillator suggests that the mechanistic origin of the power law behavior is based on the inverse dependence of amplitude versus frequency of oscillation related to the balance between reactive oxygen species production and scavenging. The results demonstrate that cardiac mitochondria behave as a network of coupled oscillators under both physiological and pathophysiological conditions.

Original languageEnglish (US)
Pages (from-to)4317-4327
Number of pages11
JournalBiophysical Journal
Volume91
Issue number11
DOIs
StatePublished - Dec 2006

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Mitochondria
Cardiac Myocytes
Mitochondrial Dynamics
Fractals
Long-Term Memory
Mitochondrial Membrane Potential
Energy Metabolism
Reactive Oxygen Species
Power (Psychology)

ASJC Scopus subject areas

  • Biophysics

Cite this

The fundamental organization of cardiac mitochondria as a network of coupled oscillators. / Aon, Miguel Antonio; Cortassa, Sonia; O'Rourke, Brian.

In: Biophysical Journal, Vol. 91, No. 11, 12.2006, p. 4317-4327.

Research output: Contribution to journalArticle

Aon, Miguel Antonio ; Cortassa, Sonia ; O'Rourke, Brian. / The fundamental organization of cardiac mitochondria as a network of coupled oscillators. In: Biophysical Journal. 2006 ; Vol. 91, No. 11. pp. 4317-4327.
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