Independent Activity Subspaces for Working Memory and Motor Preparation in the Lateral Prefrontal Cortex

AbstractThe lateral prefrontal cortex is involved in the integration of multiple types of information, including working memory and motor preparation. However, it is not known how downstream regions can extract one type of information without interference from the others present in the network. Here we show that the lateral prefrontal cortex contains two independent low-dimensional subspaces: one that encodes working memory information, and another that encodes motor preparation information. These subspaces capture all the information about the target in the delay periods, and the information in both subspaces is reduced in error trials. A single population of neurons with mixed selectivity forms both subspaces, but the information is kept largely independent from each other. A bump attractor model with divisive normalization replicates the properties of the neural data. These results have implications for the neural mechanisms of cognitive flexibility and capacity limitations.

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Minimally dependent activity subspaces for working memory and motor preparation in the lateral prefrontal cortex

eLife ◽

10.7554/elife.58154 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 2

Author(s):

Cheng Tang ◽

Roger Herikstad ◽

Aishwarya Parthasarathy ◽

Camilo Libedinsky ◽

Shih-Cheng Yen

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Motor Preparation ◽

Lateral Prefrontal Cortex ◽

Neural Data ◽

Divisive Normalization ◽

Dependent Activity ◽

Attractor Model ◽

Low Dimensional ◽

Types Of Information

The lateral prefrontal cortex is involved in the integration of multiple types of information, including working memory and motor preparation. However, it is not known how downstream regions can extract one type of information without interference from the others present in the network. Here, we show that the lateral prefrontal cortex of non-human primates contains two minimally dependent low-dimensional subspaces: one that encodes working memory information, and another that encodes motor preparation information. These subspaces capture all the information about the target in the delay periods, and the information in both subspaces is reduced in error trials. A single population of neurons with mixed selectivity forms both subspaces, but the information is kept largely independent from each other. A bump attractor model with divisive normalization replicates the properties of the neural data. These results provide new insights into neural processing in prefrontal regions.

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Time-invariant working memory representations in the presence of code-morphing in the lateral prefrontal cortex

Nature Communications ◽

10.1038/s41467-019-12841-y ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 5

Author(s):

Aishwarya Parthasarathy ◽

Cheng Tang ◽

Roger Herikstad ◽

Loong Fah Cheong ◽

Shih-Cheng Yen ◽

...

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Dimensional Subspace ◽

Neural Data ◽

Neuronal Populations ◽

Attractor Model ◽

Memory Representations ◽

Low Dimensional ◽

Types Of Information ◽

Time Invariant

Abstract Maintenance of working memory is thought to involve the activity of prefrontal neuronal populations with strong recurrent connections. However, it was recently shown that distractors evoke a morphing of the prefrontal population code, even when memories are maintained throughout the delay. How can a morphing code maintain time-invariant memory information? We hypothesized that dynamic prefrontal activity contains time-invariant memory information within a subspace of neural activity. Using an optimization algorithm, we found a low-dimensional subspace that contains time-invariant memory information. This information was reduced in trials where the animals made errors in the task, and was also found in periods of the trial not used to find the subspace. A bump attractor model replicated these properties, and provided predictions that were confirmed in the neural data. Our results suggest that the high-dimensional responses of prefrontal cortex contain subspaces where different types of information can be simultaneously encoded with minimal interference.

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Decision letter: Minimally dependent activity subspaces for working memory and motor preparation in the lateral prefrontal cortex

10.7554/elife.58154.sa1 ◽

2020 ◽

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Motor Preparation ◽

Lateral Prefrontal Cortex ◽

Dependent Activity

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Author response: Minimally dependent activity subspaces for working memory and motor preparation in the lateral prefrontal cortex

10.7554/elife.58154.sa2 ◽

2020 ◽

Author(s):

Cheng Tang ◽

Roger Herikstad ◽

Aishwarya Parthasarathy ◽

Camilo Libedinsky ◽

Shih-Cheng Yen

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Motor Preparation ◽

Author Response ◽

Lateral Prefrontal Cortex ◽

Dependent Activity

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Cannabinoid-Mediated Disinhibition and Working Memory: Dynamical Interplay of Multiple Feedback Mechanisms in a Continuous Attractor Model of Prefrontal Cortex

Cerebral Cortex ◽

10.1093/cercor/bhm103 ◽

2007 ◽

Vol 17 (suppl 1) ◽

pp. i16-i26 ◽

Cited By ~ 40

Author(s):

E. Carter ◽

X.-J. Wang

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Feedback Mechanisms ◽

Attractor Model

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Compressed Timeline of Recent Experience in Monkey Lateral Prefrontal Cortex

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01273 ◽

2018 ◽

Vol 30 (7) ◽

pp. 935-950 ◽

Cited By ~ 26

Author(s):

Zoran Tiganj ◽

Jason A. Cromer ◽

Jefferson E. Roy ◽

Earl K. Miller ◽

Marc W. Howard

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Sample Stimulus ◽

Human Memory ◽

Recent Experience ◽

Lateral Prefrontal Cortex ◽

Elapsed Time ◽

Cognitive Theories ◽

Stimulus Identity ◽

Neural Underpinnings

Cognitive theories suggest that working memory maintains not only the identity of recently presented stimuli but also a sense of the elapsed time since the stimuli were presented. Previous studies of the neural underpinnings of working memory have focused on sustained firing, which can account for maintenance of the stimulus identity, but not for representation of the elapsed time. We analyzed single-unit recordings from the lateral prefrontal cortex of macaque monkeys during performance of a delayed match-to-category task. Each sample stimulus triggered a consistent sequence of neurons, with each neuron in the sequence firing during a circumscribed period. These sequences of neurons encoded both stimulus identity and elapsed time. The encoding of elapsed time became less precise as the sample stimulus receded into the past. These findings suggest that working memory includes a compressed timeline of what happened when, consistent with long-standing cognitive theories of human memory.

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