Intrinsic Population Dynamics are a Neuronal Substrate for Visual Attention

Perception results from a dynamic interplay between the feedforward processing of sensory stimuli and intrinsic neural activity ¹ , which is often dismissed as noise ² . To tailor perceptual processes to the organism’s current needs on a continuous, moment-to-moment basis, intrinsic dynamics – rather than just being noise – have been suggested to reflect prior expectations ^3,4 , task demands ⁵ , and attentional focus ⁶ . Here, we identify a novel signature of attentive state in which intrinsic, collective neural activity modulates visuospatial attention by dynamically interacting with sensory input within the superior colliculus (SC), a midbrain hub that integrates bottom-up visual input with top-down signals ⁷ . We show that these intrinsic dynamics organize cell activity into structured, blob-like features that are temporally and topographically localized and that rival sensory-evoked responses in strength. These features emerge as animals learn to engage in the visual detection task, and predict behavioral outcomes on a trial-by-trial basis. Although independent of sensory input or overt behavior, the features can be recruited to enhance visual responses four-fold in the attentive state, generating a “dynamic saliency map” that aligns with reaction times and behavioral outcomes. A computational model indicates that tunable blob-like features can arise from local excitatory–inhibitory interactions within the SC, and enhance sensory-evoked responses in line with observations. Together, our results identify state-dependent intrinsic population activity that interacts with sensory input to give rise to a saliency-map-like representation linked to flexible, goal-directed behavior.