Spectrotemporal signatures of driving and modulatory circuits across cortical and subcortical networks

Abstract

Sensory processing depends on interactions between neural circuits that convey and regulate information across cortical and subcortical networks. Classical frameworks distinguish driving inputs, which transmit sensory content via suprathreshold activation, from modulatory inputs, which alter neuronal excitability without directly eliciting spiking. However, physiological signatures of these circuit types that generalize widely across distributed brain regions remain unclear. Here, we functionally differentiate driving and modulatory circuits in the awake macaque brain by jointly quantifying suprathreshold multiunit activity (MUA) and oscillatory phase coherence (inter-trial coherence, ITC) across eight cortical and thalamic structures during auditory, visual, and motor sampling conditions. Preferred sensory stimuli elicited broadband ITC increases accompanied by robust MUA, yielding relatively uniform spectral distributions across adjacent frequency bands, consistent with driving inputs. In contrast, non-preferred sensory and motor-related events produced narrowband, frequency-specific ITC modulation without concurrent firing, and was characterized by dominant peaks at stimulation or event rates, which is consistent with modulatory inputs. This narrowband ITC modulation is indicative of coordinated phase alignment, capable of dynamically regulating information transfer, mediated by driving inputs, across thalamocortical circuits. These response types were observed within individual regions, revealing two separable modes of neural activity. These findings identify distinct spectrotemporal signatures of driving and modulatory activity and demonstrate that subthreshold oscillatory modulation is a widespread mechanism for coordinating multisensory and motor influences on perception.