A Flexible Model of Working Memory

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2019 May 20

PMID 31103359

Citations 58

Authors

Flora Bouchacourt

Timothy J Buschman

Affiliations

Soon will be listed here.

Abstract

Working memory is fundamental to cognition, allowing one to hold information "in mind." A defining characteristic of working memory is its flexibility: we can hold anything in mind. However, typical models of working memory rely on finely tuned, content-specific attractors to persistently maintain neural activity and therefore do not allow for the flexibility observed in behavior. Here, we present a flexible model of working memory that maintains representations through random recurrent connections between two layers of neurons: a structured "sensory" layer and a randomly connected, unstructured layer. As the interactions are untuned with respect to the content being stored, the network maintains any arbitrary input. However, in our model, this flexibility comes at a cost: the random connections overlap, leading to interference between representations and limiting the memory capacity of the network. Additionally, our model captures several other key behavioral and neurophysiological characteristics of working memory.

Citing Articles

Redundant, weakly connected prefrontal hemispheres balance precision and capacity in spatial working memory.

Tschiersch M, Umakantha A, Williamson R, Smith M, Barbosa J, Compte A bioRxiv. 2025; .

PMID: 39868323 PMC: 11760753. DOI: 10.1101/2025.01.15.633176.

Sensory-memory interactions via modular structure explain errors in visual working memory.

Yang J, Zhang H, Lim S Elife. 2024; 13.

PMID: 39388221 PMC: 11466453. DOI: 10.7554/eLife.95160.

A transient high-dimensional geometry affords stable conjunctive subspaces for efficient action selection.

Kikumoto A, Bhandari A, Shibata K, Badre D Nat Commun. 2024; 15(1):8513.

PMID: 39353961 PMC: 11445473. DOI: 10.1038/s41467-024-52777-6.

Cortically Disparate Visual Features Evoke Content-Independent Load Signals during Storage in Working Memory.

Jones H, Thyer W, Suplica D, Awh E J Neurosci. 2024; 44(44).

PMID: 39327004 PMC: 11529812. DOI: 10.1523/JNEUROSCI.0448-24.2024.

Maintenance and transformation of representational formats during working memory prioritization.

Pacheco-Estefan D, Fellner M, Kunz L, Zhang H, Reinacher P, Roy C Nat Commun. 2024; 15(1):8234.

PMID: 39300141 PMC: 11412997. DOI: 10.1038/s41467-024-52541-w.

References

Kostadinov D, Sanes J . Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function. Elife. 2015; 4. PMC: 4548410. DOI: 10.7554/eLife.08964. View

Harris K, Mrsic-Flogel T . Cortical connectivity and sensory coding. Nature. 2013; 503(7474):51-8. DOI: 10.1038/nature12654. View

Kiorpes L . Visual development in primates: Neural mechanisms and critical periods. Dev Neurobiol. 2015; 75(10):1080-90. PMC: 4523497. DOI: 10.1002/dneu.22276. View

Zaksas D, Pasternak T . Directional signals in the prefrontal cortex and in area MT during a working memory for visual motion task. J Neurosci. 2006; 26(45):11726-42. PMC: 6674769. DOI: 10.1523/JNEUROSCI.3420-06.2006. View

Bays P, Catalao R, Husain M . The precision of visual working memory is set by allocation of a shared resource. J Vis. 2009; 9(10):7.1-11. PMC: 3118422. DOI: 10.1167/9.10.7. View

Mckenzie S, Frank A, Kinsky N, Porter B, Riviere P, Eichenbaum H . Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron. 2014; 83(1):202-15. PMC: 4082468. DOI: 10.1016/j.neuron.2014.05.019. View

Kiyonaga A, Scimeca J, Bliss D, Whitney D . Serial Dependence across Perception, Attention, and Memory. Trends Cogn Sci. 2017; 21(7):493-497. PMC: 5516910. DOI: 10.1016/j.tics.2017.04.011. View

Klingberg T . Development of a superior frontal-intraparietal network for visuo-spatial working memory. Neuropsychologia. 2006; 44(11):2171-7. DOI: 10.1016/j.neuropsychologia.2005.11.019. View

Pouget A, Dayan P, Zemel R . Information processing with population codes. Nat Rev Neurosci. 2001; 1(2):125-32. DOI: 10.1038/35039062. View

10.

Spaak E, Watanabe K, Funahashi S, Stokes M . Stable and Dynamic Coding for Working Memory in Primate Prefrontal Cortex. J Neurosci. 2017; 37(27):6503-6516. PMC: 5511881. DOI: 10.1523/JNEUROSCI.3364-16.2017. View

11.

Lin P, Luck S . The Influence of Similarity on Visual Working Memory Representations. Vis cogn. 2009; 17(3):356-372. PMC: 2678681. DOI: 10.1080/13506280701766313. View

12.

Bays P, Husain M . Dynamic shifts of limited working memory resources in human vision. Science. 2008; 321(5890):851-4. PMC: 2532743. DOI: 10.1126/science.1158023. View

13.

Heeger D, Simoncelli E, Movshon J . Computational models of cortical visual processing. Proc Natl Acad Sci U S A. 1996; 93(2):623-7. PMC: 40101. DOI: 10.1073/pnas.93.2.623. View

14.

Pasupathy A, Miller E . Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature. 2005; 433(7028):873-6. DOI: 10.1038/nature03287. View

15.

Buschman T, Siegel M, Roy J, Miller E . Neural substrates of cognitive capacity limitations. Proc Natl Acad Sci U S A. 2011; 108(27):11252-5. PMC: 3131328. DOI: 10.1073/pnas.1104666108. View

16.

Duncan J . An adaptive coding model of neural function in prefrontal cortex. Nat Rev Neurosci. 2001; 2(11):820-9. DOI: 10.1038/35097575. View

17.

Wang X . Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci. 2001; 24(8):455-63. DOI: 10.1016/s0166-2236(00)01868-3. View

18.

Song S, Sjostrom P, Reigl M, Nelson S, Chklovskii D . Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 2005; 3(3):e68. PMC: 1054880. DOI: 10.1371/journal.pbio.0030068. View

19.

Romo R, Hernandez A, Zainos A, Lemus L, Brody C . Neuronal correlates of decision-making in secondary somatosensory cortex. Nat Neurosci. 2002; 5(11):1217-25. DOI: 10.1038/nn950. View

20.

Fuster J . Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol. 1973; 36(1):61-78. DOI: 10.1152/jn.1973.36.1.61. View