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Neural correlates of auditory stimulus selectivity encoded by the precise temporal structure of EEG oscillations

Benedict Shien Wei Ng1*, Nikos K. Logothetis1, 2, 3 and Christoph Kayser1, 3
  • 1 Max-Planck Institute for Biological Cybernetics, Germany
  • 2 University of Manchester, Division of Imaging Science and Biomedical Engineering, United Kingdom
  • 3 Bernstein Center for Computational Neuroscience, Germany

Oscillations prevail in encephalographic (EEG, MEG) signals and supposedly reflect cognitive processes such as sensory representations or the routing of sensory information [1]. Typical MEG/EEG studies focus on the relation between oscillation amplitude (power) and the sensory-cognitive variables, making power an important marker for studying the brain [2]. However, recent studies have begun to also consider the dynamic signature of EEG/MEG signals, such as characterized by the phase of slow oscillations [3]. Several studies have shown that the precise temporal structure (phase) of slow encephalographic oscillations can be informative about sensory stimuli or details of the cognitive task. Noteworthy, in some studies the phase proved to be more informative about the presented stimuli than the same signal’s power [4,5,6].
However, the neural correlates underlying the information carrying capacity of the phase of slow oscillations remain unclear. We here directly tested whether the stimulus selectivity of low frequency EEG phase patterns indeed reflects the selectivity of neuronal firing in the underlying cortical areas. We employed the same naturalistic acoustic stimuli in two experiments, one recording scalp EEG in human subjects and another recording intracortical field potentials and single neurons in macaque auditory cortex (see e.g. [7]). Using stimulus decoding techniques we found that stimulus selective patterns of neural firing imprint on the phase of slow (theta band) oscillations rather than on their amplitudes. We found that sets of stimuli (sampled from the long acoustic stimulation sequence) that can be discriminated by the oscillatory phase pattern slow oscillations can also be discriminated by neural firing rates and vice versa. Importantly, no such relation was found between oscillatory power and firing rates.
Our results demonstrate a level of interrelation between scalp EEGs and neural firing that pertains to stimulus selectivity (preference) and which goes beyond known correlations between the strength of neural firing and EEG oscillatory amplitude. Thereby our findings enhance the link between the activity of sensory cortical neurons and non-invasively measured field potentials, and improve the interpretation of EEG-based studies and their implications towards understanding the neural dynamics of sensory perception.

References

1. Donner TH, Siegel M (2011) A framework for local cortical oscillation patterns. Trends Cogn Sci 15: 191-199.
2. Engel AK, Fries P (2010) Beta-band oscillations--signalling the status quo? Curr Opin Neurobiol 20: 156-165.
3. Vanrullen R, Busch NA, Drewes J, Dubois J (2011) Ongoing EEG Phase as a Trial-by-Trial Predictor of Perceptual and Attentional Variability. Front Psychol 2: 60.
4. Luo H, Poeppel D (2007) Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron 54: 1001-1010.
5. Howard MF, Poeppel D (2010) Discrimination of speech stimuli based on neuronal response phase patterns depends on acoustics but not comprehension. J Neurophysiol 104: 2500-2511.
6. Schyns PG, Thut G, Gross J (2011) Cracking the code of oscillatory activity. PLoS Biol 9: e1001064.
7. Kayser C, Montemurro MA, Logothetis N, Panzeri S (2009) Spike-phase coding boosts and stabilizes the information carried by spatial and temporal spike patterns. Neuron 61: 597-608.

Keywords: Auditory Cortex, Electroencephalography, Electrophysiology, entrainment, human, macaque, Neural coding

Conference: BC11 : Computational Neuroscience & Neurotechnology Bernstein Conference & Neurex Annual Meeting 2011, Freiburg, Germany, 4 Oct - 6 Oct, 2011.

Presentation Type: Poster

Topic: sensory processing (please use "sensory processing" as keyword)

Citation: Ng B, Logothetis NK and Kayser C (2011). Neural correlates of auditory stimulus selectivity encoded by the precise temporal structure of EEG oscillations. Front. Comput. Neurosci. Conference Abstract: BC11 : Computational Neuroscience & Neurotechnology Bernstein Conference & Neurex Annual Meeting 2011. doi: 10.3389/conf.fncom.2011.53.00204

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Received: 21 Aug 2011; Published Online: 04 Oct 2011.

* Correspondence: Dr. Benedict Shien Wei Ng, Max-Planck Institute for Biological Cybernetics, Tuebingen, Germany, benedict.ng@tuebingen.mpg.de