Relating layer fMRI signals to acoustics and intracranial neuronal activity in the human auditory cortex in a naturalistic design

How neuronal activity across cortical depths relates to fMRI signals during naturalistic perception has been difficult to verify noninvasively in humans. Here, we examine depth-dependent coupling between neuronal activity and fMRI signals during passive music listening. Depth-specific fMRI responses were modeled using envelopes of neural power in different frequencies elicited by the same naturalistic stimuli from a separate group of patients under intracranial EEG monitoring. From deep toward superficial depths, the relationship between neural power in different frequencies and fMRI signals systematically changed: alpha/beta activity (8-30 Hz) was increasingly associated with negative fMRI signals, while gamma-band (>30 Hz) activity showed increasingly positive associations. Gamma-band activity, including broadband high-frequency activity (>70 Hz), a proxy for neuronal firing, predicted fMRI signals beyond acoustic features, with coupling peaking at mid-to-superficial depths. Our findings reveal a systematic, depth-dependent pattern of neurovascular coupling in the human auditory cortex — a noninvasive link between neuronal frequency content and fMRI signals not previously shown in humans.