The Extralemniscal System Modulates Early Somatosensory Cortical Processing

Sudden and surprising sensory changes signal environmental events that may require immediate behavioral reactions. In mammals, these changes engage nonspecific "extralemniscal" thalamocortical pathways and evoke large and widespread cortical vertex potentials (VPs). Extralemniscal activity modulates cortical motor output in a variety of tasks and facilitates purposeful and immediate behavioral responses. In contrast, whether the extralemniscal system also affects cortical processing of sensory input transmitted through canonical "lemniscal" thalamocortical pathways remains unknown. Here we tested this hypothesis. In 23 healthy human participants (11 females) we continuously probed lemniscal processing in the primary somatosensory cortex (S1) by measuring the early-latency evoked potentials elicited by a stream of high-frequency (9.5 Hz) somatosensory electrical stimuli. We concurrently recorded extralemniscal activity by measuring the large VPs elicited by fast-rising and infrequent (∼0.1 Hz) auditory pure tones. We observed that the amplitude of S1 responses changes as a function of the phase of the VP, an effect consequent to a modulation of lemniscal input at the cortical rather than subcortical level. These findings demonstrate that a transient activation of the extralemniscal system interferes with ongoing cortical functions across different brain systems-i.e., not only at the level of the motor output but already at the sensory input-and thereby influences global brain dynamics.