The neuron mixer and its impact on human brain dynamics
Charlotte E. Luff,
Robert Peach,
Emma-Jane Mallas,
Edward Rhodes,
Felix Laumann,
Edward S. Boyden,
David J. Sharp,
Mauricio Barahona,
Nir Grossman
Affiliations
Charlotte E. Luff
Department of Brain Sciences, Imperial College London, London, UK; UK Dementia Research Institute, Imperial College London, London, UK
Robert Peach
Department of Brain Sciences, Imperial College London, London, UK; UK Dementia Research Institute, Imperial College London, London, UK; Department of Neurology, University Hospital Würzburg, Würzburg, Germany
Emma-Jane Mallas
Department of Brain Sciences, Imperial College London, London, UK; UK Dementia Research Institute, Care Research & Technology Centre, London, UK
Edward Rhodes
Department of Brain Sciences, Imperial College London, London, UK; UK Dementia Research Institute, Imperial College London, London, UK
Felix Laumann
Department of Mathematics, Imperial College London, London, UK
Edward S. Boyden
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA; Howard Hughes Medical Institute, Chevy Chase, MD, USA
David J. Sharp
Department of Brain Sciences, Imperial College London, London, UK; UK Dementia Research Institute, Care Research & Technology Centre, London, UK; Centre for Injury Studies, Imperial College London, London, UK
Mauricio Barahona
Department of Mathematics, Imperial College London, London, UK
Nir Grossman
Department of Brain Sciences, Imperial College London, London, UK; UK Dementia Research Institute, Imperial College London, London, UK; Corresponding author
Summary: A signal mixer facilitates rich computation, which has been the building block of modern telecommunication. This frequency mixing produces new signals at the sum and difference frequencies of input signals, enabling powerful operations such as heterodyning and multiplexing. Here, we report that a neuron is a signal mixer. We found through ex vivo and in vivo whole-cell measurements that neurons mix exogenous (controlled) and endogenous (spontaneous) subthreshold membrane potential oscillations, producing new oscillation frequencies, and that neural mixing originates in voltage-gated ion channels. Furthermore, we demonstrate that mixing is evident in human brain activity and is associated with cognitive functions. We found that the human electroencephalogram displays distinct clusters of local and inter-region mixing and that conversion of the salient posterior alpha-beta oscillations into gamma-band oscillations regulates visual attention. Signal mixing may enable individual neurons to sculpt the spectrum of neural circuit oscillations and utilize them for computational operations.
