Episodic memory involves consciously remembering past events often with an impressive degree of perceptual detail. How is the brain able to recreate prior perceptual states without the necessary sensory inputs? A long- held view is that consciously remembering a stimulus requires reactivation of activity patterns associated with the perception of that stimulus. This process of neocortical `sensory reinstatement' is thought to be dependent on the hippocampus, a region critical for episodic memory. Consequently, there has been an overwhelming empirical focus on studying reinstatement activities within the hippocampus. However, if sensory reinstatement in neocortex is a critical part of episodic memory retrieval, it must be empirically shown to be a spatially and temporally precise recapitulation of sensory processing, and to causally contribute to memory behavior. To date, the best evidence of sensory reinstatement in human neocortex has come from neuroimaging studies reporting spatial overlap or similarity of brain responses for perceiving and retrieving stimuli. While informative, such data: i) do not consistently show overlap in expected sensory cortices; ii) cannot measure the reinstatement of temporal response features; iii) are correlational in nature. To address these limitations and provide critical data on sensory reinstatement in human neocortex we will use intracranial recording and stimulation to study the precise anatomical (Aim 1), temporal (Aim 2) and causal (Aim 3) properties of visual reinstatement. Human electrocorticography (ECoG) provides the needed spatial and temporal precision for capturing and perturbing neural population activity at spatio-temporal scales undetectable with non-invasive methods. In Aim 1, we will use high-density ECoG recordings to quantify the spatial precision of reinstatement dynamics in higher order visual cortices, and quantify how stimulus selectivity relates to stimulus reinstatement. In Aim 2, we will test the temporal precision of reinstatement dynamics by inducing and manipulating oscillatory activities in primary visual cortex to test the fidelity of their reinstatement during retrieval. In Aim 3, we will use targeted electrical brain stimulation to test the causal role of sensory reinstatement in neocortex. Together, the Aims of this proposal will direct needed empirical attention towards the neural properties of neocortical reinstatement and causally test its role in human episodic memory retrieval. These advances will help elucidate how reinstatement like processes are exacerbated for conditions involving the intrusion of vivid mental content like post-traumatic stress disorder and schizophrenia.

This project will quantify how the human visual system is activated during the retrieval of visual memories. We will use electrical recording and stimulation of the human brain to understand how these memory `reactivations' influence the content, vividness and accuracy of memory behavior. These findings will improve our understanding of how the brain creates visual imagery without visual input, a process exacerbated for memories in post-traumatic stress disorder and hallucinations in schizophrenia.