Medial prefrontal activity during delay period contributes to learning of a working memory task

Liu, Ding; Gu, Xiaowei; Zhu, Jia; Zhang, Xiaoxing; Han, Zhe; Yan, Wenjun; Cheng, Qi; Jiang, Hao; Fan, Hongmei; Hou, Ronghui; Chen, Zhaoqin; Chen, Yulei; Li, C.

doi:10.1126/science.1256573

Cited by 190 publications

(222 citation statements)

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“…Preparatory activity is thus distributed in a redundant fashion across functional modules that can both operate independently and correct each other. The cortical networks involved in working memory could be organized in a similar manner [7][8][9][10] . It is likely that modularity and redundancy operate in circuits contained in one hemisphere, perhaps even spatially interdigitated.…”

Section: Discussionmentioning

confidence: 99%

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Robust neuronal dynamics in premotor cortex during motor planning

Li¹,

Daie²,

Svoboda³

et al. 2016

Nature

421

473

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Neural activity maintains representations that bridge past and future events, often over many seconds. Network models can produce persistent and ramping activity, but the positive feedback that is critical for these slow dynamics can cause sensitivity to perturbations. Here we use electrophysiology and optogenetic perturbations in mouse premotor cortex to probe robustness of persistent neural representations during motor planning. Preparatory activity is remarkably robust to large-scale unilateral silencing: detailed neural dynamics that drive specific future movements were quickly and selectively restored by the network. Selectivity did not recover after bilateral silencing of premotor cortex. Perturbations to one hemisphere are thus corrected by information from the other hemisphere. Corpus callosum bisections demonstrated that premotor cortex hemispheres can maintain preparatory activity independently. Redundancy across selectively coupled modules, as we observed in premotor cortex, is a hallmark of robust control systems. Network models incorporating these principles show robustness that is consistent with data.

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Section: Discussionmentioning

confidence: 99%

“…Neurons in frontal and parietal cortex show slow dynamics, including persistent and ramping activity, related to motor planning [1][2][3][4] , action timing 5,6 , working memory [7][8][9][10] and decision making [11][12][13] . Neurons have intrinsic time constants on the order often milliseconds 14 .…”

Section: Introductionmentioning

confidence: 99%

Robust neuronal dynamics in premotor cortex during motor planning

Li¹,

Daie²,

Svoboda³

et al. 2016

Nature

421

473

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“…In a recent study [12] , using head-fixed mice, Liu et al developed an olfactory delayed-nonmatch-to-sample paradigm (DNMS), a standard working memory task that had only been used in primates before (Fig. 1).…”

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confidence: 99%

Learning to memorize: Shedding new light on prefrontal functions

2015

Neurosci. Bull.

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·Research Highlight·Working memory is one of the essential higher cognitive functions that actively holds behaviorally-relevant information essential for guiding subsequent actions. It includes subsystems that store and manipulate singlemode or multi-modal sensory information, e.g., spatial information, visual images, auditory scenes, olfactory objects, or any combination of these. In addition to merely holding a certain amount of information for a short period of time, as is generally believed, the cognitive processes involved are far more complex, including the executive and attentional control of short-term memory, permitting interim integration, and the processing, disposal, and retrieval of information. Evolution-wise, working memory is essential for the behavioral fl exibility that allows humans and animals to quickly adapt to rapidly changing environments.A wealth of studies have been conducted in attempts to understand the neuronal process underlying working memory, and have identified a number of brain regions as crucial, including the prefrontal cortex (PFC), posterior parietal cortex, anterior cingulate, and parts of the basal ganglia. Among these regions, the PFC has drawn most attention due to the striking finding that individual neurons show persistent activity during the memory-retention period [1][2][3] (termed the delay period, a hallmark of working memory tasks): elevated activity persists after the sensory stimuli have been removed until the holding period is over (from seconds to tens of seconds) and the behavioral choice has been made. This raises the immediate question of whether the persistent activity in the PFC during the delay period encodes the contents of working memory (memory storage). This has been under debate for the last two decades [4] .Some studies find that PFC activity increases when the number of items to be memorized increases. This seems to support the hypothesis that the PFC plays an important role in memory storage, as a straightforward explanation would be that increasing the demands of storage would be expected to increase the activity level in a region where representations are being actively stored. However, an equally plausible explanation would be that if PFC activity refl ects top-down signals to control more posterior regions where the actual representations are stored, maintaining higher loads of information might require increased PFC input in order for retained information to survive delay and distraction. Therefore, it is not yet clear that the PFC is the site where the representations are stored. The fact that the PFC has been found to play important roles in executive functions [4] implies that its role in working memory might be controlling attention, selecting strategies, and manipulating information, rather than information storage [2,5] .To resolve this debate, it is therefore necessary to achieve a deeper understanding of the causal role of the PFC in working memory tasks. This would require temporally precise perturbation of neuronal activity in spec...

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“…They found that behavioral performance was impaired during the learning stage of the working memory task (olfactory delayed-nonmatch-to-sample go/no-go task), but not after the mice were well-trained, indicating that the delay-period medial PFC activity is involved in learning the task, but not in the maintenance of working memory information. They conclude that properly-regulated delay-period medial PFC activity is critical for information retention when mice are learning the working memory task, but not for working memory maintenance after the animals are well-trained [17] .…”

mentioning

confidence: 99%

“…Chinese Academy of Sciences [17] . As noted above, working memory involves a short-term interval of retention termed the 'delay period'.…”

mentioning

confidence: 99%

A step forward in the understanding of prefrontal cortical functions

Funahashi

2015

Neurosci. Bull.

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·Editorial·The prefrontal cortex (PFC) is an integrative area that guides behaviors and thoughts [1][2][3] . During the past century, a great many studies have been performed on PFC functions, using a variety of technical approaches such as anatomy, lesion, neuropsychology, electrophysiology, and functional imaging [2,3] . It is well known that the PFC plays an essential role in inhibitory control of behavior, regulation of attention, working memory, decision-making, and behavioral organization [1][2][3][4][5][6] .In October 2013, the 4 th International Conference on Prefrontal Cortex was held in Nanchang University (Nanchang, China), co-organized by Bao-Ming Li (Nanchang University, China), Shintaro Funahashi (Kyoto University, Japan), Yong-Di Zhou (East China Normal University, China), and Satoru Otani (Ryotokuji University, Japan). A group of scientists from China, Japan, the USA, Germany, and Brazil comprehensively introduced their studies and extensively discussed progress in the understanding of PFC functions. This special issue covers the reviews and reports by the speakers at the conference.Evolutionarily, the PFC is the last-emerged structure of the brain. It is unknown how it has evolved into such a complex system in humans. The mesocortical dopamine projection into the PFC is essential for its cognitive functions. Lee and Goto propose a hypothesis that the mesocortical dopamine projection is one of the biological substrates involved in PFC evolution, and that this evolutionary process may result in the emergence of psychiatric disorders such as schizophrenia [7] .Working memory refers to the cognitive process of maintaining information for seconds for subsequent goaldirected actions. Persistent neuronal firing in the sensory cortex and the PFC during the delay period in a working memory task has been considered to be the neuronal substrate for working memory maintenance. However, the role of the delay activity in the sensory cortex is thought to differ from that in the PFC. Ku et al. propose that the delay activities in the sensory cortex and the PFC reflect the quality and quantity of representations in working memory, respectively [8] .In addition to maintaining working memory information, the PFC is thought to store memory traces for "rules"or "strategies" that determine the temporal structure of behavior, and this kind of memory might be served by synaptic plasticity in the PFC. Otani et al. review the induction of long-term synaptic plasticity in the medial PFC of rats, with special emphasis on the regulation of synaptic plasticity by dopamine. They conclude that synaptic plasticity in the PFC is powerfully modulated by dopamine in an inverted-U-shaped, dose-dependent manner [9]

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Medial prefrontal activity during delay period contributes to learning of a working memory task

Cited by 190 publications

References 42 publications

Robust neuronal dynamics in premotor cortex during motor planning

Robust neuronal dynamics in premotor cortex during motor planning

Learning to memorize: Shedding new light on prefrontal functions

A step forward in the understanding of prefrontal cortical functions

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