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Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing

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Highlights

  • Complex visual scenes are converted to a temporal code: a ‘to-do list’.

  • The order of the temporal code is determined by bottom-up and top-down drives.

  • Phase-coding organized by alpha oscillations coordinates competing representations.

  • Gamma activity phase-coupled to alpha oscillations segments competing representations.

Sensory systems must rely on powerful mechanisms for organizing complex information. We propose a framework in which inhibitory alpha oscillations limit and prioritize neuronal processing. At oscillatory peaks, inhibition prevents neuronal firing. As the inhibition ramps down within a cycle, a set of neuronal representations will activate sequentially according to their respective excitability. Both top-down and bottom-up drives determine excitability; in particular, spatial attention is a major top-down influence. On a shorter time scale, fast recurrent inhibition segments representations in slots 10–30 ms apart, generating gamma-band activity at the population level. The proposed mechanism serves to convert spatially distributed representations in early visual regions to a temporal phase code: that is, ‘to-do lists’ that can be processed sequentially by downstream regions.

Section snippets

Preventing information overload in the visual hierarchy

Although neuroscience research is advancing quickly in terms of data acquisition and recording techniques, there is a strong need for computational principles that can guide future empirical investigations. General neuro-computational mechanisms might have evolved to serve similar computational purposes in different regions. Information overload (see Glossary), defined as the amount of information exceeding processing capabilities, constitutes a general neuro-computational problem. One example

A mechanism transforming spatial representations into a temporal code

We propose a neuronal mechanism that serves to prevent information overload by transforming spatial representations into a temporal code. This results in short ‘to-do lists’. The mechanism is motivated by convergent evidence demonstrating that slower oscillations in the theta (5–8 Hz) and alpha band (8–13 Hz) are abundant in many brain regions, independent of species [6]. In particular, the alpha oscillations are inhibitory: that is, they rhythmically prevent firing [7]. In addition, gamma-band

Predictions and future perspectives

We have presented a general mechanism that limits and prioritizes the visual representations to be processed. The mechanism is based on an inhibitory oscillatory drive in the alpha band allowing only the most excitable representations to discharge. Further, these representations are arranged as a temporal code organized according to neuronal excitability. The population dynamics arising from this mechanism will produce oscillations in the alpha band. Gamma activity phase-locked to the alpha

Concluding remarks

In conclusion, we have presented a mechanism for how complex visual information can be represented as a temporal code. Basically, a visual scene is decomposed to a sequence, allowing processing to be prioritized. By a gradual release of inhibition in each alpha cycle, this mechanism produces ‘to-do lists’ that can be processed sequentially in downstream regions. The framework can be tested by relating single unit firing to LFP oscillations in early visual regions while various parameters, such

Acknowledgments

The authors gratefully acknowledge funding from The Netherlands Organization for Scientific Research (NWO): a VICI grant (453-09-002), an ALW Open Competition Grant (ALW2PJ/10071), an MaGW Open Competition Grant (822-02-011), and ‘The healthy brain’ funded by the Netherlands Initiative Brain and Cognition (NIHC), a part of the Organization for Scientific Research (NWO) (056-14-011).

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