Perturbation-based mapping of natural frequencies with direct intracranial stimulation of the human brain

Theoretical and experimental evidence suggest that the induction of oscillatory activity by an external rhythmic source on a specific brain area is maximally efficient if the input pattern matches its so-called natural frequency, defined as the predominant neural rhythm at which the activity of this area tends to fluctuate spontaneously. Based on this principle, single pulse Transcranial Magnetic Stimulation (TMS) coupled to scalp electroencephalography (EEG) has provided evidence of frequency-specific power increases within a unique natural frequency band, considered common to the whole lobe.\n\nIn an attempt to gain deeper insight into this phenomenon and set the basis for a finer-grained atlas of natural frequencies, here we analyzed intracranial EEG (iEEG) signals modulated by single pulses of direct electrical brain stimulation in human patients implanted with depth multielectrodes. Our analyses revealed changes in local EEG activity emerging from local oscillators and contributing to a complex distribution of frequency-specific natural rhythmic responses throughout cortical regions. Moreover, challenging the notion of natural oscillations featuring a predominant frequency band characteristic for an entire lobe, our data support a rich diversity of spectral fingerprints (narrowband, vs. broadband or multiband) with single or multiple frequency peaks, often encompassing contiguous frequency bands, operating at a very local scale.\n\nOur findings contribute novel insights on which specific brain areas could be more likely to be synchronized at a given frequencies band and their preferred coupling frequencies, features that could ultimately inform on their structural and functional organization. Our results may also increase our mechanistic understanding of invasive and noninvasive brain stimulation and promote further developments of these approaches for the manipulation of brain oscillations subtending normal and impaired cognition.