Working Memory 2.0
Open accessAbstract
Working memory is the fundamental function by which we break free from reflexive input-output reactions to gain control over our own thoughts. It has two types of mechanisms: online maintenance of information and its volitional or executive control. Classic models proposed persistent spiking for maintenance but have not explicitly addressed executive control. We review recent theoretical and empirical studies that suggest updates and additions to the classic model. Synaptic weight changes between sparse bursts of spiking strengthen working memory maintenance. Executive control acts via interplay between network oscillations in gamma (30-100 Hz) in superficial cortical layers (layers 2 and 3) and alpha and beta (10-30 Hz) in deep cortical layers (layers 5 and 6). Deep-layer alpha and beta are associated with top-down information and inhibition. It regulates the flow of bottom-up sensory information associated with superficial layer gamma. We propose that interactions between different rhythms in distinct cortical layers underlie working memory maintenance and its volitional control.
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All across cortex, gamma power (>35 Hz)/spiking is higher during bottom-up sensory inputs.
“A key observation is that, all across cortex, gamma power (>35 Hz)/spiking is higher during bottom-up sensory inputs.”
From Layer and rhythm specificity for predictive routing (2020) · cites this paper as [29]
The section “Beta in deep-layer cortex interacts with gamma in superficial-layer cortex” (page unavailable) says bottom-up gamma and informative spiking in sensory areas are typically elevated during sensory stimulation. But “Mechanisms of gamma/beta interplay” (page unavailable) distinguishes prefrontal cortex, where sensory drive has less impact and gamma can occur without a stimulus. The copy therefore supports the sensory-area pattern, not the unqualified claim that it holds all across cortex; the cited passages also do not establish the >35 Hz cutoff. (LLM, conf=0.85)
Experimental — accuracy not yet measuredGamma power/spiking is anticorrelated with alpha/beta (8 to 30 Hz) power, which is higher under conditions of top-down control (e.g., attention and response inhibition).
“They are anticorrelated with alpha/beta (8 to 30 Hz) power (26–29), which is higher under conditions of top-down control (e.g., attention and response inhibition) (30–34).”
From Layer and rhythm specificity for predictive routing (2020) · cites this paper as [29]
The Introduction and “What is the alternative?” state that alpha/beta and gamma activity are anticorrelated; “What about alpha/beta?” links alpha/beta to top-down information and inhibition. But that section says attention increases gamma for attended inputs, while alpha/beta increases for unattended locations or modalities. It does not establish the claim’s unqualified assertion that alpha/beta power is higher during attention or its specific example of response inhibition. (LLM, conf=0.84)
Experimental — accuracy not yet measured
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A Connectomic Hypothesis for the Hominization of the Brain
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Exercise types and working memory components during development
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Stable maintenance of multiple representational formats in human visual short-term memory
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Working memory control dynamics follow principles of spatial computing
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Age-Related Differences in Resting-State EEG and Allocentric Spatial Working Memory Performance
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Visual mental imagery: Evidence for a heterarchical neural architecture
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Prefrontal pyramidal neurons are critical for all phases of working memory
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Perspectives on adaptive dynamical systems
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In vivo ephaptic coupling allows memory network formation
Pinotsis, D. A., & Miller, E. K. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad251 · Cited by 62 · see citing works
Self-citationGonzález‐Burgos, G., Miyamae, T., Krimer, Y., Gulchina, Y., Pafundo, D. E., Krimer, O. L., Bazmi, H. H., Arion, D., Enwright, J. F., Fish, K. N., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1210-19.2019 · Cited by 60 · see citing works
The role of executive function in shaping reinforcement learning
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Cytoelectric coupling: Electric fields sculpt neural activity and “tune” the brain’s infrastructure
Pinotsis, D. A., Fridman, G. Y., & Miller, E. K. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2023.102465 · Cited by 64 · see citing works
Self-citationHannah, R., Muralidharan, V., Sundby, K. K., & Aron, A. R. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117222 · Cited by 60 · see citing works
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The neuroscience of active learning and direct instruction
Dubinsky, J. M., & Hamid, A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105737 · Cited by 101 · see citing works
Auditory cortical connectivity in humans
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Long-term learning transforms prefrontal cortex representations during working memory
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Working Memory Is Complex and Dynamic, Like Your Thoughts
Buschman, T. J., & Miller, E. K. (2022) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01940 · Cited by 55 · see citing works
Self-citationOlaru, M., Cernera, S., Hahn, A., Wozny, T. A., Ansó, J., de Hemptinne, C., Little, S. J., Neumann, W., Abbasi-Asl, R., & Starr, P. A. (2024) · Brain · doi:10.1093/brain/awae004 · Cited by 55 · see citing works
Exact neural mass model for synaptic-based working memory
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Bistability of prefrontal states gates access to consciousness
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Movement-related beta ERD and ERS abnormalities in neuropsychiatric disorders
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Human connectome topology directs cortical traveling waves and shapes frequency gradients
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Tracking Selective Rehearsal and Active Inhibition of Memory Traces in Directed Forgetting
Fellner, M.-C., Waldhauser, G. T., & Axmacher, N. (2020) · Current Biology · doi:10.1016/j.cub.2020.04.091 · Cited by 52 · see citing works
A Hierarchy of Functional States in Working Memory
Muhle-Karbe, P. S., Myers, N. E., & Stokes, M. G. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.3104-20.2021 · Cited by 51 · see citing works
Corticostriatal beta oscillation changes associated with cognitive function in Parkinson’s disease
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Robust and brain-like working memory through short-term synaptic plasticity
Kozachkov, L., Tauber, J., Lundqvist, M., Brincat, S. L., Slotine, J.-J. E., & Miller, E. K. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010776 · Cited by 49 · see citing works
Self-citationNeuronal Correlates of Spatial Working Memory in the Endbrain of Crows.
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Predictive Coding: A more cognitive process than we thought?
Gabhart, K. M., Xiong, Y. (., & Bastos, A. M. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2025.01.012 · Cited by 54 · see citing works
Self-citationBilingual Language Experience Shapes Resting-State Brain Rhythms
Bice, K., Yamasaki, B. L., & Prat, C. S. (2020) · Neurobiology of Language · doi:10.1162/nol_a_00014 · Cited by 46 · see citing works
Dissecting the neurobiology of linguistic disorganisation and impoverishment in schizophrenia
Palaniyappan, L. K. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.08.015 · Cited by 47 · see citing works
Anterior–Posterior Hippocampal Dynamics Support Working Memory Processing
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Sanchez-Todo, R., Bastos, A. M., Lopez-Sola, E., Mercadal, B., Santarnecchi, E., Miller, E. K., Deco, G., & Ruffini, G. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.119938 · Cited by 46 · see citing works
Self-citationReframing the debate: The distributed systems view of working memory
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Disentangling the flow of signals between populations of neurons
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A model of working memory for latent representations
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Human amygdala compared to orbitofrontal cortex connectivity, and emotion
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Mental programming of spatial sequences in working memory in the macaque frontal cortex
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Targeting Cognition and Networks Through Neural Oscillations
Widge, A. S., & Miller, E. K. (2019) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2019.0740 · Cited by 39 · see citing works
Self-citationWorking memory capacity of crows and monkeys arises from similar neuronal computations
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When the time is right: Temporal dynamics of brain activity in healthy aging and dementia
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Distinct functions for beta and alpha bursts in gating of human working memory
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A Thalamic Orphan Receptor Drives Variability in Short-Term Memory
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Multivariate Lesion-Behavior Mapping of General Cognitive Ability and Its Psychometric Constituents
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Anterior-Posterior Hippocampal Dynamics Support Working Memory Processing
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Dependence of Working Memory on Coordinated Activity Across Brain Areas
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Decoding distributed oscillatory signals driven by memory and perception in the prefrontal cortex
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The role of recollection, familiarity, and the hippocampus in episodic and working memory
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Synaptic Variability and Cortical Gamma Oscillation Power in Schizophrenia
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- Authors
- Miller, E. K., Lundqvist, M., & Bastos, A. M.
- Affiliations
- Massachusetts Institute of Technology (US)
- Corresponding author
- Miller, Earl K.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2018-10
- Volume
- 100
- Issue
- 2
- Pages
- 463-475
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC8112390
- OpenAlex
- W2898524098
- Cited by
- 797
- References
- 165
- Citations by year
- 2026: 100 · 2025: 130 · 2024: 134 · 2023: 143 · 2022: 116 · 2021: 87 · 2020: 63 · 2019: 22 · 2018: 1
- FWCI
- 5.77
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIMH (R37MH087027)
- ONR (MURI N00014-16-1-2832)
- The Picower Fellows Program
- MIT Picower Institute
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- working memory, working memory maintenance, executive function, synaptic plasticity, gamma oscillations, alpha oscillations, beta oscillations, cortical layers, top-down control, neural oscillations
- MeSH terms
- Animals, Brain, Humans, Memory, Short-Term, Models, Neurological
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