Mental chronometry of target detection: human thalamus leads cortex

Attentive monitoring of environmental stimuli is most fundamental for rapid target detection. The aim of this study was to assess the timing of thalamic versus cortical processes involved in this cognitive operation. To this end, simultaneous depth and scalp EEG was recorded in eight patients with essential tremor, undergoing thalamic deep brain stimulation (DBS), when the DBS electrodes could be accessed via their temporarily externalized leads. The patients performed an oddball task consisting of 300 presentations of one frequent and two rare visual cues, appearing in randomized order. One of the rare cues was defined as a target, the occurrences of which had to be indicated by a button press (motor condition) or silently counted (non-motor condition). At the scalp and the thalamus, event-related potentials (ERP) were largest upon target presentation, with peak latencies in the time domain of classical P300 responses. Remarkably, target-specific thalamic ERP emerged significantly prior to scalp P300. Furthermore, whereas scalp ERP had a higher amplitude upon rare than upon frequent non-target signals, thalamic ERP were independent of stimulus probability. This pattern was identified during motor and non-motor task execution. We conclude that the human thalamus specifically supports the early recognition of target events and can widely distribute this label through its divergent cortical projections.