Task-specific versus generalized mnemonic representations in parietal and prefrontal cortices

Sarma, Arup; Masse, Nicolas Y.; Wang, Xiao Jing; Freedman, David J.

doi:10.1038/nn.4168

Cited by 107 publications

(118 citation statements)

References 48 publications

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“…Here, we show that the enhanced response of the precuneus to the learned spatial representation is preserved between experimental days. This finding can be best explained by a representation of the static environment within the precuneus, which is stable for at least 1 d. Correspondingly, a recent study showed that working memory signatures can be traced in the PPC of monkeys during the delay period of a categorization task, but only after the corresponding task has been learned over a long-term period (21). Therefore, both short-term working memory and long-term episodic representations seem to exist in the precuneus.…”

Section: Discussionmentioning

confidence: 93%

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Rapid and independent memory formation in the parietal cortex

Brodt

Pöhlchen

Flanagin

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

133

116

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Previous evidence indicates that the brain stores memory in two complementary systems, allowing both rapid plasticity and stable representations at different sites. For memory to be established in a long-lasting neocortical store, many learning repetitions are considered necessary after initial encoding into hippocampal circuits. To elucidate the dynamics of hippocampal and neocortical contributions to the early phases of memory formation, we closely followed changes in human functional brain activity while volunteers navigated through two different, initially unknown virtual environments. In one condition, they were able to encode new information continuously about the spatial layout of the maze. In the control condition, no information could be learned because the layout changed constantly. Our results show that the posterior parietal cortex (PPC) encodes memories for spatial locations rapidly, beginning already with the first visit to a location and steadily increasing activity with each additional encounter. Hippocampal activity and connectivity between the PPC and hippocampus, on the other hand, are strongest during initial encoding, and both decline with additional encounters. Importantly, stronger PPC activity related to higher memory-based performance. Compared with the nonlearnable control condition, PPC activity in the learned environment remained elevated after a 24-h interval, indicating a stable change. Our findings reflect the rapid creation of a memory representation in the PPC, which belongs to a recently proposed parietal memory network. The emerging parietal representation is specific for individual episodes of experience, predicts behavior, and remains stable over offline periods, and must therefore hold a mnemonic function.long-term memory | posterior parietal cortex | precuneus | memory systems consolidation | virtual reality L earning enables adaptive and effective interaction with the environment based on past experience. How this essential capability of the brain to encode, store, and later retrieve new information is implemented on the systems level has been the focus of many studies. However, although there is consistent evidence that specific brain regions are involved in learning and memory, the interactions between these regions and their temporal dynamics remain unclear. For declarative memory, one influential model proposes complementary roles of the hippocampus and neocortex in supporting memory representations (1-3). It assumes that the highly plastic hippocampus serves as a fast learner, transiently storing newly encountered information. Later on, this information is gradually integrated into more stable neocortical networks (4).Many experiments in animals and humans have confirmed decreased hippocampal but increased neocortical contributions to memory retrieval with longer consolidation intervals (5-7). Concerning the time frame during which hippocampal independence of a memory is established, accounts diverge widely. In the case of patients with medial temporal lobe (MTL) dama...

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Section: Discussionmentioning

confidence: 93%

“…Furthermore, activity in the PPC is able to represent category-specific information during a delay period after category information has been learned (21). It is also one of very few regions in the brain that represents memory accuracy in human fMRI when memory confidence is held constant (22).…”

Section: Discussionmentioning

confidence: 99%

Rapid and independent memory formation in the parietal cortex

Brodt

Pöhlchen

Flanagin

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

133

116

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“…Decision and premotor signals are multiplexed and intertwined to the extent that decision-making signals may even be observed outside the central nervous system, in the motor periphery ( Joo et al 2016, Selen et al 2012, Song & Nakayama 2009, Spivey et al 2005). However, not all task variants produce this multiplexing phenomenon (Bennur & Gold 2011, Gold & Shadlen 2003), presumably because the mixed nature of decision and premotor responses may only be present once the mapping between abstract decision and appropriate motor action is predictable and has been learned (Law & Gold 2008, Sarma et al 2015). Thus, our perspective is that rather than study particular tasks in which LIP resembles a neural correlate of decisions, it will be particularly illuminating to seek and identify when and how these multiplexed signals are (and are not) present to understand how the brain computes decisions and plans corresponding actions.…”

Section: Discussionmentioning

confidence: 99%

“…The only difference between this scheme and the normalization that is better understood in earlier visual areas is that it would require broad spatial tuning of the normalization pool. This seems reasonable given the large RF sizes and messy retinotopy in LIP (Ben Hamed et al 2001, 2002; Blatt et al 1990; Janssen et al 2008; Platt & Glimcher 1997; but see Patel et al 2010) and the flexible tuning observed in LIP during learning (Sarma et al 2015), but more direct analyses are required.…”

Section: Applying the Sensorimotor Multiplexing Perspective To Other mentioning

confidence: 97%

The Role of the Lateral Intraparietal Area in (the Study of) Decision Making

Huk

Katz

Yates

2017

Annu. Rev. Neurosci.

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Over the past two decades, neurophysiological responses in the lateral intraparietal area (LIP) have received extensive study for insight into decision-making. In a parallel manner, inferred cognitive processes have enriched interpretations of LIP activity. Because of this bidirectional interplay between physiology and cognition, LIP has served as fertile ground for developing quantitative models that link neural activity with decision-making. These models stand as some of the most important frameworks for linking brain and mind, and they are now mature enough to be evaluated in finer detail and integrated with other lines of investigation of LIP function. Here, we focus on the relationship between LIP responses and known sensory and motor events in perceptual decision-making tasks, as assessed by correlative and causal methods. The resulting sensorimotor-focused approach offers an account of LIP activity as a multiplexed amalgam of sensory, cognitive, and motor-related activity, with a complex and often indirect relationship to decision processes. Our data-driven focus on multiplexing (and de-multiplexing) of various response components can complement decision-focused models and provides more detailed insight into how neural signals might relate to cognitive processes such as decision-making.

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“…Much previous work in LIP examined its role in attention (especially SBA) (Bisley and Goldberg, 2010; Herrington and Assad, 2009; Ibos et al, 2013; Saalmann et al, 2007), visual feature representation (Fanini and Assad, 2009; Toth and Assad, 2002) or encoding cognitive variables (Freedman and Assad, 2006; Sarma et al, 2015). Our previous study (Ibos and Freedman, 2014) was the first to parametrically characterize how FBA impacts feature tuning in LIP.…”

Section: Discussionmentioning

confidence: 99%

Interaction between Spatial and Feature Attention in Posterior Parietal Cortex

Ibos

Freedman

2016

Neuron

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Summary Lateral intraparietal (LIP) neurons encode a vast array of sensory and cognitive variables. Recently, we proposed that the flexibility of feature representations in LIP reflect the bottom-up integration of sensory signals, modulated by feature-based attention (FBA), from upstream feature-selective cortical neurons. Moreover, LIP activity is also strongly modulated by the position of space-based attention (SBA). However, the mechanisms by which SBA and FBA interact to facilitate the representation of task-relevant spatial and non-spatial features in LIP remain unclear. We recorded from LIP neurons during performance of a task which required monkeys to detect specific conjunctions of color, motion-direction, and stimulus position. Here we show that FBA and SBA potentiate each other’s effect in a manner consistent with attention gating the flow of visual information along the cortical visual pathway. Our results suggest that linear bottom-up integrative mechanisms allow LIP neurons to emphasize task-relevant spatial and non-spatial features.

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Task-specific versus generalized mnemonic representations in parietal and prefrontal cortices

Cited by 107 publications

References 48 publications

Rapid and independent memory formation in the parietal cortex

Rapid and independent memory formation in the parietal cortex

The Role of the Lateral Intraparietal Area in (the Study of) Decision Making

Interaction between Spatial and Feature Attention in Posterior Parietal Cortex

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