A two-system theory of sensory-evoked brain responses

Sudden and isolated sensory stimuli (SISS) likely signal environmental events demanding immediate behavioural responses. These stimuli-which are widely and persistently used in both basic and clinical neuroscience to explore sensory processing and perception-also trigger some of the largest and most widespread electrocortical responses in the awake mammalian brain. These responses are often interpreted as reflecting either modality-specific sensory processing mediated by high-fidelity 'lemniscal' thalamocortical pathways to primary sensory cortices, cortico-cortical connections or motor activity. Here we contend that these interpretations are unjustified. We first describe evidence that the electrocortical responses elicited by the SISS used in systems and cognitive neuroscience are strongly contributed to by non-modality-specific processes mediated by diffuse 'extralemniscal' thalamocortical projections. In human EEG, this contribution is reflected in the scalp vertex potential. We then discuss the implications of this 'two-system' theory for basic and clinical neuroscience studies, including the neural correlates of consciousness, where widespread responses to sudden, isolated or rare stimuli-often interpreted as signatures of awareness-may instead reflect extralemniscal activity. We conclude by suggesting a mechanism through which transient extralemniscal responses affect ongoing brain activity and promote swift reactions to sudden environmental changes.