Endogenous activity modulates stimulus and circuit-specific neural tuning and perception

Abstract

Perception reflects not only input from the sensory periphery, but also the endogenous neural state when sensory inputs enter the brain. Whether endogenous neural states influence perception only through global mechanisms, such as arousal, or can also perception in a neural circuit and stimulus specific manner remains largely unknown. Intracranial recordings from 30 pre-surgical epilepsy patients showed that endogenous activity independently modulated the strength of trialby-trial neural tuning of different visual category-selective neural circuits. Furthermore, the same aspect of the endogenous activity that influenced tuning in a particular neural circuit also correlated with reaction time only for trials with the category of image that circuit was selective for. These results suggest that endogenous activity may influence neural tuning and perception through circuit-specific predictive coding processes.2 Main Text: Perception depends on not only sensory input, but also the neural and cognitive state when a stimulus is presented. Traditionally, this endogenous activity has been treated as random biological noise(1). However, studies in both humans and animals demonstrate that rather than being a noise process, endogenous activity reflects fluctuations of neural activity that influence neural processing in a behaviorally relevant manner. Specifically, endogenous fluctuations in neural activity influence both coarse aspects of the neural response to sensory input(2-5) and the behavioral response to that input(5-9). Endogenous activity has rich structure, reflecting the stimulus processing properties of the local neural circuitry(10), broad scale brain network architecture(11), and may reflect statistically optimal representations of the environment(12). Fuctuations in endogenous processes such as arousal(13-15) and alertness (16,17) can influence stimulus processing and behavior. Some theoretical accounts posit that fluctuations of endogenous activity can reflect predictive processes(18) that facilitate stimulus processing in a stimulus-specific manner. However, most studies have only examined nonspecific mechanisms, such as arousal and alertness(13-17). Thus, there is a dearth of empirical evidence testing whether endogenous processes can influence neural tuning and influence behavior in a circuit and stimulus-specific manner as required by models of predictive processing.Data were acquired from 30 human neurosurgical patients with implanted intracranial electroencephalography (iEEG) while they viewed images of faces, bodies, words, hammers, houses, and scrambled non-objects and performed a 1-back, repeat detection task. Stimuli were balanced across categories and presented in a random order to reduce any potential cognitive or strategic processes that might favor one stimulus over another. This allowed us to probe the relationship between endogenous activity, visual category tuning, and behavior separately for