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Articles, Behavioral/Cognitive

Age-Related Changes in 1/f Neural Electrophysiological Noise

Bradley Voytek, Mark A. Kramer, John Case, Kyle Q. Lepage, Zechari R. Tempesta, Robert T. Knight and Adam Gazzaley
Journal of Neuroscience 23 September 2015, 35 (38) 13257-13265; DOI: https://doi.org/10.1523/JNEUROSCI.2332-14.2015
Bradley Voytek
1Departments of Neurology and
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Mark A. Kramer
3Department of Mathematics and Statistics, Boston University, Boston, Massachusetts 02215, and
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John Case
4Helen Wills Neuroscience Institute and
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Kyle Q. Lepage
3Department of Mathematics and Statistics, Boston University, Boston, Massachusetts 02215, and
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Zechari R. Tempesta
1Departments of Neurology and
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Robert T. Knight
4Helen Wills Neuroscience Institute and
5Department of Psychology, University of California, Berkeley, California 94720
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Adam Gazzaley
1Departments of Neurology and
2Physiology and Psychiatry and UCSF Center for Integrative Neuroscience, University of California, San Francisco, California 94158,
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Abstract

Aging is associated with performance decrements across multiple cognitive domains. The neural noise hypothesis, a dominant view of the basis of this decline, posits that aging is accompanied by an increase in spontaneous, noisy baseline neural activity. Here we analyze data from two different groups of human subjects: intracranial electrocorticography from 15 participants over a 38 year age range (15–53 years) and scalp EEG data from healthy younger (20–30 years) and older (60–70 years) adults to test the neural noise hypothesis from a 1/f noise perspective. Many natural phenomena, including electrophysiology, are characterized by 1/f noise. The defining characteristic of 1/f is that the power of the signal frequency content decreases rapidly as a function of the frequency (f) itself. The slope of this decay, the noise exponent (χ), is often <−1 for electrophysiological data and has been shown to approach white noise (defined as χ = 0) with increasing task difficulty. We observed, in both electrophysiological datasets, that aging is associated with a flatter (more noisy) 1/f power spectral density, even at rest, and that visual cortical 1/f noise statistically mediates age-related impairments in visual working memory. These results provide electrophysiological support for the neural noise hypothesis of aging.

SIGNIFICANCE STATEMENT Understanding the neurobiological origins of age-related cognitive decline is of critical scientific, medical, and public health importance, especially considering the rapid aging of the world's population. We find, in two separate human studies, that 1/f electrophysiological noise increases with aging. In addition, we observe that this age-related 1/f noise statistically mediates age-related working memory decline. These results significantly add to this understanding and contextualize a long-standing problem in cognition by encapsulating age-related cognitive decline within a neurocomputational model of 1/f noise-induced deficits in neural communication.

  • 1/f
  • electrocorticography
  • EEG
  • neural noise
  • phase/amplitude coupling
  • working memory
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The Journal of Neuroscience: 35 (38)
Journal of Neuroscience
Vol. 35, Issue 38
23 Sep 2015
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Age-Related Changes in 1/f Neural Electrophysiological Noise
Bradley Voytek, Mark A. Kramer, John Case, Kyle Q. Lepage, Zechari R. Tempesta, Robert T. Knight, Adam Gazzaley
Journal of Neuroscience 23 September 2015, 35 (38) 13257-13265; DOI: 10.1523/JNEUROSCI.2332-14.2015

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Age-Related Changes in 1/f Neural Electrophysiological Noise
Bradley Voytek, Mark A. Kramer, John Case, Kyle Q. Lepage, Zechari R. Tempesta, Robert T. Knight, Adam Gazzaley
Journal of Neuroscience 23 September 2015, 35 (38) 13257-13265; DOI: 10.1523/JNEUROSCI.2332-14.2015
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Keywords

  • 1/f
  • electrocorticography
  • EEG
  • neural noise
  • phase/amplitude coupling
  • working memory

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