Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled

PLoS Comput Biol. 2016 Oct 14;12(10):e1005162. doi: 10.1371/journal.pcbi.1005162. eCollection 2016 Oct.

Abstract

Several theories have been advanced to explain how cross-frequency coupling, the interaction of neuronal oscillations at different frequencies, could enable item multiplexing in neural systems. The communication-through-coherence theory proposes that phase-matching of gamma oscillations between areas enables selective processing of a single item at a time, and a later refinement of the theory includes a theta-frequency oscillation that provides a periodic reset of the system. Alternatively, the theta-gamma neural code theory proposes that a sequence of items is processed, one per gamma cycle, and that this sequence is repeated or updated across theta cycles. In short, both theories serve to segregate representations via the temporal domain, but differ on the number of objects concurrently represented. In this study, we set out to test whether each of these theories is actually physiologically plausible, by implementing them within a single model inspired by physiological data. Using a spiking network model of visual processing, we show that each of these theories is physiologically plausible and computationally useful. Both theories were implemented within a single network architecture, with two areas connected in a feedforward manner, and gamma oscillations generated by feedback inhibition within areas. Simply increasing the amplitude of global inhibition in the lower area, equivalent to an increase in the spatial scope of the gamma oscillation, yielded a switch from one mode to the other. Thus, these different processing modes may co-exist in the brain, enabling dynamic switching between exploratory and selective modes of attention.

MeSH terms

  • Animals
  • Attention / physiology
  • Biological Clocks / physiology*
  • Computer Simulation
  • Feedback, Physiological / physiology
  • Gamma Rhythm / physiology*
  • Humans
  • Models, Neurological*
  • Neurons / physiology*
  • Theta Rhythm / physiology*
  • Visual Cortex / physiology*
  • Visual Perception / physiology

Grants and funding

This work was supported by a EURYI award to RV (European Science Foundation, http://www.esf.org/coordinating-research/euryi.html), by the European Commission (Spacecog, FP7-FET proactive, NBIS, Grant Agreement No. 600785, http://cordis.europa.eu/project/rcn/106239_en.html), and by an ERC Consolidator grant P-CYCLES 614244 to RV. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.