Confidence in Memories: Behavioral and Neural Approaches

The brain computes and uses uncertainty to guide decision-making. While this is well established for information sensed externally in the form of perceptions, it is less established whether information retrieved from internal storage, in the form of episodic memory, is also treated probabilistically. To test this question, we developed a spatial episodic memory task in which rats gamble their time on a memory choice in each trial, indicating their confidence in its accuracy. We found that rats express higher confidence on correct trials than errors, indicating a degree of self-reflective consciousness thought previously to exist only in humans. We introduce a generative model for episodic memory confidence that predicts the observed patterns of memory confidence. To investigate the neural correlates of memory confidence, we implanted four rats with triple-site, local field potential (LFP) and single-unit recording devices targeting the orbitofrontal cortex (OFC), nucleus accumbens (NAc), and dorsal hippocampus. To perform these surgeries, we developed a novel method for the implantation of thin-film polymer electrode arrays through the dura mater. We demonstrate that this technology can yield long-term, high quality single unit and LFP recordings. To investigate the neural activity in these three regions as it may relate to memory confidence, we took as a starting point the decades-old observation that the hippocampus is required for memory, and the more recent finding that hippocampal neurons store and send information about past experience to the rest of the brain. In particular, a hippocampal neural activity pattern known as the sharp wave-ripple (SWR) is an LFP event associated with highly synchronous neural firing in the hippocampus and modulation of neural activity in distributed brain regions. A growing body of evidence indicates that SWRs support both memory consolidation and memory retrieval. This work is summarized in a synthetic review that introduces the perspective that the SWR may mediate the retrieval of stored representations that can be utilized immediately by downstream circuits in decision-making, planning, recollection, or a confidence evaluation, while simultaneously initiating memory consolidation processes. Finally, a proof-of-concept study of SWR function in the episodic memory task is presented