Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Alex Gonzalez, J. Benjamin Hutchinson, Melina R. Uncapher, Janice Chen, Karen F. LaRocque, Brett L. Foster, Vinitha Rangarajan, Josef Parvizi, Anthony D. Wagner
2015 Proceedings of the National Academy of Sciences of the United States of America  
Theories of the neurobiology of episodic memory predominantly focus on the contributions of medial temporal lobe structures, based on extensive lesion, electrophysiological, and imaging evidence. Against this backdrop, functional neuroimaging data have unexpectedly implicated left posterior parietal cortex (PPC) in episodic retrieval, revealing distinct activation patterns in PPC subregions as humans make memory-related decisions. To date, theorizing about the functional contributions of PPC
more » ... been hampered by the absence of information about the temporal dynamics of PPC activity as retrieval unfolds. Here, we leveraged electrocorticography to examine the temporal profile of high gamma power (HGP) in dorsal PPC subregions as participants made old/new recognition memory decisions. A double dissociation in memory-related HGP was observed, with activity in left intraparietal sulcus (IPS) and left superior parietal lobule (SPL) differing in time and sign for recognized old items (Hits) and correctly rejected novel items (CRs). Specifically, HGP in left IPS increased for Hits 300-700 ms poststimulus onset, and decayed to baseline ∼200 ms preresponse. By contrast, HGP in left SPL increased for CRs early after stimulus onset (200−300 ms) and late in the memory decision (from 700 ms to response). These memory-related effects were unique to left PPC, as they were not observed in right PPC. Finally, memory-related HGP in left IPS and SPL was sufficiently reliable to enable brain-based decoding of the participant's memory state at the single-trial level, using multivariate pattern classification. Collectively, these data provide insights into left PPC temporal dynamics as humans make recognition memory decisions. intracranial EEG | declarative memory | decision making | multivariate pattern analysis | ECoG T he ability to remember past events-episodic memory-is known to critically depend on medial temporal lobe (MTL) structures (1, 2) and their interaction with prefrontal cortex (3) . Neuroimaging studies of humans making memory-based decisions, although advancing understanding of MTL and prefrontal mnemonic function (4-8), consistently and unexpectedly demonstrate that activity in left lateral posterior parietal cortex (PPC) also varies with episodic memory outcomes (9-14). In particular, functional MRI (fMRI) data reveal dissociable effects of memory on activity in left intraparietal sulcus (IPS), superior parietal lobule (SPL), and angular gyrus (AG), wherein activity tracks perceived memory strength, retrieval decision uncertainty, and episodic recollection, respectively (9-14). For example, during recognition memory decisions, activity in left lateral IPS is greater during higher confidence hits and monotonically decreases across lower confidence hits to lower confidence correct rejections (CRs) to higher confidence CRs (15-17). By contrast, activity in left SPL is greater during lower confidence recognition decisions (for both hits and correct rejections) relative to higher confidence decisions (11, 16, 17) . Studies of patients with PPC lesions demonstrate a complex pattern of effects on memory, with performance spared on some measures of episodic memory, but impaired as measured by retrieval confidence, memory for source details, and cued recall (18-23). For example, a recent study of two patients with bilateral IPS lesions revealed unimpaired recognition memory accuracy, but a reduction in high confidence hits and false alarms relative to matched controls (22). Importantly, this decline in high confidence recognition decisions was only observed for items perceived as old, and not for items perceived as novel. As with fMRI measures of left lateral IPS activity, these lesion data suggest that the role of IPS in memory varies as a function of whether the test probe is perceived as old or new. The role of lateral PPC in episodic retrieval is posited to relate to broader (i.e., nonmnemonic) functions. Extant evidence indicates that dorsal PPC is involved in other cognitive domains, such as perceptual decision making (24-28). For example, human fMRI studies of two-choice perceptual decisions have demonstrated that IPS activity tracks the strength of perceptual evidence (24, 25), independent of response modality (25). A mechanistic interpretation of such activity is that IPS neurons act as evidence accumulators, with a distinct population of IPS neurons accumulating evidence toward each of the two decision bounds. When the evidence reaches one of the bounds, a perceptual decision it thought to be reached. Such results motivated the hypothesis that left IPS might serve as a mnemonic accumulator during old/new recognition decisions (9, 16). Significance Over the past decade, human posterior parietal cortex (PPC) has been unexpectedly implicated in remembering and memory-related decision making. Functional neuroimaging indicates that memory-related responses differ across PPC, and patients with PPC lesions show subtle to significant changes in memory behavior. These surprising observations have motivated novel theorizing, yet current understanding of PPC contributions to memory is limited by the absence of temporal information about activity in PPC subregions as retrieval decisions unfold. In this study, recordings from the human brain show for the first time that distinct temporal and functional profiles of activity are present in PPC subregions as participants make recognition memory decisions. These new findings inform theories of parietal functional contributions to memory, decision making, and attention.
doi:10.1073/pnas.1510749112 pmid:26283375 pmcid:PMC4568245 fatcat:6awibfdfv5c2vpadwcml4a5npe