Parietal Representations of Stimulus Features Are Amplified during Memory Retrieval and Flexibly Aligned with Top-Down Goals

Abstract

In studies of human episodic memory, the phenomenon of reactivation has traditionally been observed in regions of occipitotemporal cortex (OTC) involved in visual perception. However, reactivation also occurs in lateral parietal cortex (LPC), and recent evidence suggests that stimulus-specific reactivation may be stronger in LPC than in OTC. These observations raise important questions about the nature of memory representations in LPC and their relationship to representations in OTC. Here, we report two fMRI experiments that quantified stimulus feature information (color and object category) within LPC and OTC, separately during perception and memory retrieval, in male and female human subjects. Across both experiments, we observed a clear dissociation between OTC and LPC: while feature information in OTC was relatively stronger during perception than memory, feature information in LPC was relatively stronger during memory than perception. Thus, while OTC and LPC represented common stimulus features in our experiments, they preferentially represented this information during different stages. In LPC, this bias toward mnemonic information co-occurred with stimulus-level reinstatement during memory retrieval. In Experiment 2, we considered whether mnemonic feature information in LPC was flexibly and dynamically shaped by top-down retrieval goals. Indeed, we found that dorsal LPC preferentially represented retrieved feature information that addressed the current goal. In contrast, ventral LPC represented retrieved features independent of the current goal. Collectively, these findings provide insight into the nature and significance of mnemonic representations in LPC and constitute an important bridge between putative mnemonic and control functions of parietal cortex. When humans remember an event from the past, patterns of sensory activity that were present during the initial event are thought to be reactivated. Here, we investigated the role of lateral parietal cortex (LPC), a high-level region of association cortex, in representing prior visual experiences. We find that LPC contained stronger information about stimulus features during memory retrieval than during perception. We also found that current task goals influenced the strength of stimulus feature information in LPC during memory. These findings suggest that, in addition to early sensory areas, high-level areas of cortex, such as LPC, represent visual information during memory retrieval, and that these areas may play a special role in flexibly aligning memories with current goals.

Perception and memory have distinct spatial tuning properties in human visual cortex

“…Here, we confirm prior findings of reactivation by showing spatially precise retinotopic activation in multiple visual areas, as well as reduced SNR during memory. We also show clear evidence that perception and memory responses are most similar in higher level visual areas as proposed by Pearson et al (2015) and paralleling prior findings (Favila et al, 2018;Breedlove et al, 2018). However, we also found systematic differences that could not be explained by lower SNR.…”

“…Pylyshyn, 2002). More recently, memory researchers have favored decoding and pattern similarity approaches over univariate activation analyses to examine the content of retrieved memories (Polyn et al, 2005;Kuhl et al, 2011;Favila et al, 2018). While these approaches are powerful, they do not explicitly specify the form mnemonic activity should take, and many activation schemes can lead to successful decoding.…”

Progression from feature-specific brain activity to hippocampal binding during episodic encoding

“…Our findings of feature-specific encoding effects demonstrate that multimodal details of complex episodes can be decomposed in the brain, even when encoded simultaneously. The specific pattern of our results converges with univariate and multivariate decoding studies previously using these types of features, including color (Uncapher et al, 2006;Favila et al, 2018), sounds (Gottlieb et al, 2012), and scenes (Park and Chun, 2009;Morgan et al, 2011;Staresina et al, 2011) to study perception and encoding. We additionally showed that these visuo-perceptual neural correlates were only present early on in encoding, which is consistent with relatively earlier subsequent memory effects in ventral visual areas shown using intracranial EEG (Long and Kahana, 2015).…”

Visual and semantic representations predict subsequent memory in perceptual and conceptual memory tests

“…The systems consolidation view (Winocur and Moscovitch 2011) purports that such transfer of episodic (from hippocampus to cortex) or working memory traces (from visual to parietal and frontal regions, see Xu 2017). Further evidence from studies scanning both encoding and retrieval blocks, and find that memory representations during retrieval may be found in separate regions from encoding (Xiao et al 2017;Favila et al 2018) also support this transfer-based view. Furthermore, regions coding for 2 nd -order similarity between brain and model similarity (i.e., our IRAF regressors) with values below a statistical threshold (and therefore not visible in the IRAF maps in Fig.…”

“…The nature of visual representations has been examined in at least three different domains of cognitive neuroscience: vision, semantic cognition, and episodic memory. Vision researchers have examined the representations of visual properties Rajalingham et al 2018), semantic cognition researchers, the representations of semantic features and categories (Konkle and Oliva 2012;Clarke et al 2013;Martin et al 2018), and episodic memory researchers, the representations that are reactivated during episodic memory tests (Kuhl et al 2012;Favila et al 2018).…”