Elsevier

Neuroscience

Volume 146, Issue 3, 25 May 2007, Pages 1400-1412
Neuroscience

Systems neuroscience
Feedback modulates the temporal scale-free dynamics of brain electrical activity in a hypothesis testing task

https://doi.org/10.1016/j.neuroscience.2007.02.048Get rights and content

Abstract

We used the electroencephalogram (EEG) to investigate whether positive and negative performance feedbacks exert different long-lasting modulations of electrical activity in a reasoning task. Nine college students serially tested hypotheses concerning a hidden rule by judging its presence or absence in triplets of digits, and revised them on the basis of an exogenous performance feedback. The scaling properties of the transition period between feedback and triplet presentation were investigated with detrended fluctuation analysis (DFA). DFA showed temporal scale-free dynamics of EEG activity in both feedback conditions for time scales larger than 150 ms. Furthermore, DFA revealed that negative feedback elicits significantly higher scaling exponents than positive feedback. This effect covers a wide network comprising parieto-occipital and left frontal regions. We thus showed that specific task demands can modify the temporal scale-free dynamics of the ongoing brain activity. Putative neural correlates of these long-lasting feedback-specific modulations are proposed.

Section snippets

Subjects

Thirteen right-handed graduate and undergraduate students volunteered in the experiment. Subjects had normal or corrected to normal vision and no history of neurological or psychiatric disease. Three of them could not be kept for further analyses due to excessive rates of recording artifacts; while one subject was excluded because she was not naive as to the task’s manipulations. The nine remaining subjects (five women and four men; mean age=25, range 21–30 years) were all blind as to the

Testing DFA and PSA on surrogate data

We first tested on surrogate data the efficiency of DFA and PSA to estimate the correct scaling with our experimental data statistics. As will be shown in the next section, the scaling range over which scaling exponents are estimated is restricted to the interval 156–1248 ms. For every value of the scaling exponent α between 0.7 and 1.3, we generated 100 independent groups of 70 time series (corresponding to the minimum number of observations per subject and condition in the main analysis),

Discussion

The main finding of this study is that the scale-free temporal dynamics of the brain electrical activity during a HT task is modulated by performance feedback: negative feedback elicits a higher degree of temporal scaling (i.e. a higher DFA scaling exponent) than positive feedback. We thus showed that specific task demands modulate the scale-free dynamics of the associated ongoing brain activity.

The two feedback conditions significantly differed at several electrodes clustered around two main

Conclusion

In conclusion, we have shown that the scale-free dynamics of the brain electrical activity are modulated by performance feedback during the preparatory period of a HT task. This result shows that specific cognitive demands can modulate the long-range temporal scaling properties of the ongoing brain activity. We believe that investigating the modulation of long-range scale-free brain temporal dynamics by cognitive processing is a potentially valuable approach to gain new insights on many complex

Acknowledgments

We are grateful to Manuela Piazza for insightful discussions and comments on the manuscript. D.P. was supported by a Post-doctoral Fellowship of the Fondation pour la Recherche Médicale, Paris (France). This article is dedicated to the memory of one of the coauthors, Pierre-Marie Baudonnière.

References (51)

  • M. Ruchsow et al.

    Human anterior cingulate cortex is activated by negative feedback: evidence from event-related potentials in a guessing task

    Neurosci Lett

    (2002)
  • H.E. Stanley et al.

    Scale invariance and universality: organizing principles in complex systems

    Physica A

    (2000)
  • A. Takashima et al.

    Successful declarative memory formation is associated with ongoing activity during encoding in a distributed neocortical network related to working memory: An MEG study

    Neuroscience

    (2006)
  • D. Avnir et al.

    Is the geometry of nature fractal?

    Science

    (1998)
  • R. Azouz et al.

    Cellular mechanisms contributing to response variability of cortical neurons in vivo

    J Neurosci

    (1999)
  • P. Bak et al.

    Self-organized criticality: An explanation of the 1/f noise

    Phys Rev Lett

    (1987)
  • P. Bak et al.

    Self-organized criticality

    Phys Rev A

    (1988)
  • J. Bhattacharya et al.

    Universality in the brain while listening to music

    Proc R Soc Lond B

    (2001)
  • S.V. Buldyrev et al.

    Long-range correlation properties of coding and noncoding DNA sequences: GenBank analysis

    Phys Rev E

    (1995)
  • J. Davidsen et al.

    1/f(alpha) Noise from self-organized critical models with uniform driving

    Phys Rev E

    (2000)
  • W.J. Freeman et al.

    Analysis of spatial patterns of phase in neocortical gamma EEGs in rabbit

    J Neurophysiol

    (2000)
  • C. Heneghan et al.

    Establishing the relation between detrended fluctuation analysis and power spectral density analysis for stochastic processes

    Phys Rev E

    (2000)
  • C. Holroyd et al.

    The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity

    Psychological Review

    (2002)
  • J.J. Hopfield et al.

    What is a moment?Transient synchrony as a collective mechanism for spatiotemporal integration

    Proc Natl Acad Sci U S A

    (2001)
  • R.C. Hwa et al.

    Scaling properties of fluctuations in the human electroencephalogram

    Phys Rev E

    (2002)
  • Cited by (0)

    1

    M.B., D.P. made equally important contributions to this article.

    View full text