Magnetoencephalography in Twins Reveals a Strong Genetic Determination of the Peak Frequency of Visually Induced Gamma-Band Synchronization

Many aspects of brain processing are intimately linked to brain rhythms. Essentially all classical brain rhythms, i.e., delta, theta, alpha, beta, and sleep waves, are highly heritable. This renders brain rhythms an interesting intermediate phenotype for cognitive and behavioral traits. One brain rhythm that has been particularly strongly linked to cognition is the gamma rhythm: it is involved in attention, short- and long-term memory, and conscious awareness. It has been described in sensory and motor cortices, association and control structures, and the hippocampus. In contrast to most other brain rhythms, the gamma frequency highly depends on stimulus and task conditions, suggesting a low heritability. However, the heritability of gamma has not been assessed. Here, we show that visually induced gamma-band synchronization in humans is strongly genetically determined. Eighty twin subjects (20 monozygotic and 20 dizygotic twin pairs) viewed a moving sinusoidal grating while their brain activity was recorded using magnetoencephalography. The stimulus induced spectrally confined gamma-band activity in sensors over visual cortex in all subjects, with individual peak frequencies ranging from 45 to 85 Hz. Gamma-band peak frequencies were highly correlated across monozygotic twins (r = 0.88), but not across dizygotic twins (r = 0.32) or unrelated subjects (r = 0.02). This implies a heritability of the gamma-band frequency of 91%. This strong genetic determination suggests that gamma-related cognitive functions are under close genetic control.

[1]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .

[2]  M H Lader,et al.  A twin study of the genetic influences on the electroencephalogram. , 1972, Journal of medical genetics.

[3]  Rowland Lp Presidential address, 1981. , 1981 .

[4]  Presidential address, 1981. Research with twins: the concept of emergenesis. , 1982, Psychophysiology.

[5]  David T. Lykken,et al.  Research with twins: The concept of emergenesis. , 1982 .

[6]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[7]  F. L. D. Silva,et al.  Basic mechanisms of cerebral rhythmic activities , 1990 .

[8]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  D I Boomsma,et al.  Heritability of human brain functioning as assessed by electroencephalography. , 1996, American journal of human genetics.

[10]  W. Klimesch,et al.  Alpha frequency, reaction time, and the speed of processing information. , 1996, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[11]  Linkowski,et al.  EEG sleep patterns in twins , 1999, Journal of sleep research.

[12]  M. Hasselmo,et al.  Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. , 1999, Archives of general psychiatry.

[13]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[14]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[15]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[16]  M. Neale,et al.  Are Smarter Brains Running Faster? Heritability of Alpha Peak Frequency, IQ, and Their Interrelation , 2001, Behavior genetics.

[17]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[18]  H. Scheich,et al.  Stimulus-related gamma oscillations in primate auditory cortex. , 2002, Journal of neurophysiology.

[19]  W. Singer,et al.  Oscillatory Neuronal Synchronization in Primary Visual Cortex as a Correlate of Stimulus Selection , 2002, The Journal of Neuroscience.

[20]  G. Baal,et al.  Twin and family studies of the human electroencephalogram: a review and a meta-analysis , 2002, Biological Psychology.

[21]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[22]  Fiona E. N. LeBeau,et al.  GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Marc W Howard,et al.  Gamma oscillations correlate with working memory load in humans. , 2003, Cerebral cortex.

[24]  B. Ermentrout,et al.  Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  F. Vogel,et al.  The genetic basis of the normal human electroencephalogram (EEG) , 1970, Humangenetik.

[26]  D. Lewis,et al.  Cortical inhibitory neurons and schizophrenia , 2005, Nature Reviews Neuroscience.

[27]  W. Freiwald,et al.  Coherent oscillatory activity in monkey area v4 predicts successful allocation of attention. , 2005, Cerebral cortex.

[28]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[29]  Danielle Posthuma,et al.  Netherlands Twin Register: From Twins to Twin Families , 2006, Twin Research and Human Genetics.

[30]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

[31]  Nicholas G Martin,et al.  Genetic variation of individual alpha frequency (IAF) and alpha power in a large adolescent twin sample. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[32]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[33]  E. Miller,et al.  Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices , 2007, Science.

[34]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[35]  Arjen van Ooyen,et al.  Genetic Contributions to Long-Range Temporal Correlations in Ongoing Oscillations , 2007, The Journal of Neuroscience.

[36]  Adam E. Green,et al.  Using genetic data in cognitive neuroscience: from growing pains to genuine insights , 2008, Nature Reviews Neuroscience.

[37]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[38]  C. Tallon-Baudry,et al.  Neural Dissociation between Visual Awareness and Spatial Attention , 2008, The Journal of Neuroscience.

[39]  Rainer Goebel,et al.  Genetic Contribution to Variation in Cognitive Function: An fMRI Study in Twins , 2009, Science.

[40]  Derek K. Jones,et al.  Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans , 2009, Proceedings of the National Academy of Sciences.

[41]  T. Sejnowski,et al.  Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING? , 2009, Neuron.

[42]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[43]  K. D. Singh,et al.  Spectral properties of induced and evoked gamma oscillations in human early visual cortex to moving and stationary stimuli. , 2009, Journal of neurophysiology.

[44]  Catherine Tallon-Baudry,et al.  The roles of gamma-band oscillatory synchrony in human visual cognition. , 2009, Frontiers in bioscience.

[45]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[46]  Derek K. Jones,et al.  Visual gamma oscillations and evoked responses: Variability, repeatability and structural MRI correlates , 2010, NeuroImage.

[47]  W. Singer,et al.  Gamma-Phase Shifting in Awake Monkey Visual Cortex , 2010, The Journal of Neuroscience.

[48]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[49]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[50]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[51]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.