Prefrontal gamma power and LFP tuning in working memory decrease during monkey adolescent development

AbstractWorking memory ability continues to mature into adulthood in both humans and non-human primates. At the single neuron level, adolescent development is characterized by increased prefrontal firing rate in the delay period, but less is known about how coordinated activity between neurons is altered. Local field potentials (LFP) provide a window into the computation carried out by the local network. To address the effects of adolescent development on LFP activity, three male rhesus monkeys were trained to perform an oculomotor delayed response task and tested at both the adolescent and adult stage. Simultaneous single-unit and LFP signals were recorded from areas 8a and 46 of the dorsolateral prefrontal cortex (dlPFC). In both the cue and delay period, power relative to baseline increased in the gamma frequency range (32 - 128 Hz). In the adult stage, high-firing neurons were also more likely to reside at sites with strong gamma power increase from baseline. For both stages, the gamma power increase in the delay was selective for sites with neuron encoding stimulus information in their spiking. Gamma power and neuronal firing did not show stronger temporal correlations. Our results establish gamma power decrease to be a feature of prefrontal cortical maturation.Significance StatementGamma-frequency oscillations in extracellular field recordings (such as LFP or EEG) are a marker of normal interactions between excitatory and inhibitory neurons in neural circuits. Abnormally low gamma power during working memory is seen in conditions such as schizophrenia. We sought to examine whether the immature prefrontal cortex similarly exhibits lower power in the gamma frequency range during working memory, in a non-human primate model of adolescence. Contrary to this expectation, the adolescent PFC exhibited stronger gamma power during the maintenance of working memory. Our findings reveal an unknown developmental maturation trajectory of gamma band oscillations and raise the possibility that schizophrenia represent an excessive state of prefrontal maturation.

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GSK3β inhibition restores cortical gamma oscillation and cognitive behavior in a mouse model of NMDA receptor hypofunction relevant to schizophrenia

Neuropsychopharmacology ◽

10.1038/s41386-020-00819-0 ◽

2020 ◽

Vol 45 (13) ◽

pp. 2207-2218

Author(s):

Kazuhito Nakao ◽

Mahendra Singh ◽

Kiran Sapkota ◽

Bailey C. Hagler ◽

Robert N. Hunter ◽

...

Keyword(s):

Working Memory ◽

Mouse Model ◽

Spatial Working Memory ◽

Gamma Oscillations ◽

Gamma Oscillation ◽

Mutant Mice ◽

Patch Clamp Recording ◽

Behavioral Deficits ◽

Gamma Power ◽

Sensory Evoked

Abstract Cortical gamma oscillations are believed to be involved in mental processes which are disturbed in schizophrenia. For example, the magnitudes of sensory-evoked oscillations, as measured by auditory steady-state responses (ASSRs) at 40 Hz, are robustly diminished, whereas the baseline gamma power is enhanced in schizophrenia. Such dual gamma oscillation abnormalities are also present in a mouse model of N-methyl-D-aspartate receptor hypofunction (Ppp1r2cre/Grin1 knockout mice). However, it is unclear whether the abnormal gamma oscillations are associated with dysfunction in schizophrenia. We found that glycogen synthase kinase-3 (GSK3) is overactivated in corticolimbic parvalbumin-positive GABAergic interneurons in Grin1 mutant mice. Here we addressed whether GSK3β inhibition reverses both abnormal gamma oscillations and behavioral deficits with high correlation by pharmacological and genetic approach. We demonstrated that the paralog selective-GSK3β inhibitor, but not GSK3α inhibitor, normalizes the diminished ASSRs, excessive baseline gamma power, and deficits in spatial working memory and prepulse inhibition (PPI) of acoustic startle in Grin1 mutant mice. Cell-type specific GSK3B knockdown, but not GSK3A knockdown, also reversed abnormal gamma oscillations and behavioral deficits. Moreover, GSK3B knockdown, but not GSK3A knockdown, reverses the mutants’ in vivo spike synchrony deficits. Finally, ex vivo patch-clamp recording from pairs of neighboring cortical pyramidal neurons showed a reduction of synchronous spontaneous inhibitory-postsynaptic-current events in mutants, which was reversed by GSK3β inhibition genetically and pharmacologically. Together, GSK3β inhibition in corticolimbic interneurons ameliorates the deficits in spatial working memory and PPI, presumably by restoration of synchronous GABA release, synchronous spike firing, and evoked-gamma power increase with lowered baseline power.

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The Preliminary Investigation of Multi-Level Working Memory in Predicting Anxiety/Depressive Symptomatology in Childhood/Adolescence

10.31234/osf.io/qvedc ◽

2019 ◽

Author(s):

Brian Kavanaugh ◽

Alexa Fryc ◽

Simona Temereanca Ibanescu ◽

Eric Tirrell ◽

Lindsay Oberman ◽

...

Keyword(s):

Working Memory ◽

Depressive Symptomatology ◽

Preliminary Investigation ◽

Gamma Oscillations ◽

Composite Score ◽

Clinical Markers ◽

Measurement Variability ◽

Parent Questionnaire ◽

Gamma Power ◽

Multi Level

Prior research in working memory (WM) has been hampered by measurement variability and a lack of integration of neural and clinical markers. This study sought to examine whether a multi-level composite of WM with neural, cognitive, and behavioral levels could predict childhood affective symptomatology in seventeen children and adolescents receiving outpatient mental health services. WM-related theta/gamma oscillations at the F3 electrode were measured via electroencephalography (EEG) recording during a spatial WM task. Other measures included a neuropsychological measure of WM, parent questionnaire assessing WM, and self-reported affective symptoms. Gamma power and theta-gamma coupling, but not theta power, predicted high WM demands performance (i.e., 16-19% of variance). Two composite scores were created consisting of gamma power or theta-gamma coupling, clinical WM measure performance, and parent-reported WM symptoms. These multi-level composite score predicted self-reported depressive (22-32% of variance) symptoms, while only the gamma-version of the composite predicted anxious symptoms (39% of variance compared to 12% of variance). A WM composite score consisting of neural, cognitive, and behavioral levels predicted the severity of childhood affective symptomatology. WM, like other EFs, is highly complex and may be most appropriately measured in clinical and research settings with a combination of neural, cognitive, and behavioral measures.

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Compromised Behavior and Gamma Power During Working Memory in Cognitively Healthy Individuals With Abnormal CSF Amyloid/Tau

Frontiers in Aging Neuroscience ◽

10.3389/fnagi.2020.574214 ◽

2020 ◽

Vol 12 ◽

Author(s):

Roger Rochart ◽

Quanying Liu ◽

Alfred N. Fonteh ◽

Michael G. Harrington ◽

Xianghong Arakaki

Keyword(s):

Working Memory ◽

Healthy Individuals ◽

Gamma Power

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Gamma Power during Working Memory in Pre‐symptomatic Alzheimer’s Disease Differs from Normal Healthy Aging

The FASEB Journal ◽

10.1096/fasebj.2020.34.s1.04743 ◽

2020 ◽

Vol 34 (S1) ◽

pp. 1-1

Author(s):

Xianghong Arakaki ◽

Quanying Liu ◽

Alfred N Fonteh ◽

Michael G Harrington

Keyword(s):

Alzheimer’S Disease ◽

Alzheimer's Disease ◽

Working Memory ◽

Healthy Aging ◽

Gamma Power

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Dorsal Root Ganglion Stimulation Modulates Cortical Gamma Activity in the Cognitive Dimension of Chronic Pain

Brain Sciences ◽

10.3390/brainsci10020095 ◽

2020 ◽

Vol 10 (2) ◽

pp. 95 ◽

Cited By ~ 1

Author(s):

Tariq Parker ◽

Yongzhi Huang ◽

Ashley L.B. Raghu ◽

James J. FitzGerald ◽

Alexander L. Green ◽

...

Keyword(s):

Chronic Pain ◽

Working Memory ◽

Pain Relief ◽

Dorsal Root Ganglion ◽

Task Performance ◽

Dorsal Root ◽

Oscillatory Activity ◽

Cognitive Dimension ◽

Gamma Power ◽

Back Task

A cognitive task, the n-back task, was used to interrogate the cognitive dimension of pain in patients with implanted dorsal root ganglion stimulators (DRGS). Magnetoencephalography (MEG) signals from thirteen patients with implanted DRGS were recorded at rest and while performing the n-back task at three increasing working memory loads with DRGS-OFF and the task repeated with DRGS-ON. MEG recordings were pre-processed, then power spectral analysis and source localization were conducted. DRGS resulted in a significant reduction in reported pain scores (mean 23%, p = 0.001) and gamma oscillatory activity (p = 0.036) during task performance. DRGS-induced pain relief also resulted in a significantly reduced reaction time during high working memory load (p = 0.011). A significant increase in average gamma power was observed during task performance compared to the resting state. However, patients who reported exacerbations of pain demonstrated a significantly elevated gamma power (F(3,80) = 65.011612, p < 0.001, adjusted p-value = 0.01), compared to those who reported pain relief during the task. Our findings demonstrate that gamma oscillatory activity is differentially modulated by cognitive load in the presence of pain, and this activity is predominantly localized to the prefrontal and anterior cingulate cortices in a chronic pain cohort.

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Neural Correlates of Visual Short-term Memory Dissociate between Fragile and Working Memory Representations

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00870 ◽

2015 ◽

Vol 27 (12) ◽

pp. 2477-2490 ◽

Cited By ~ 18

Author(s):

Annelinde R. E. Vandenbroucke ◽

Ilja G. Sligte ◽

Jade G. de Vries ◽

Michael X. Cohen ◽

Victor A. F. Lamme

Keyword(s):

Working Memory ◽

Visual Working Memory ◽

Visual Processing ◽

Short Term Memory ◽

Iconic Memory ◽

Partial Report ◽

Time Frequency ◽

Gamma Power ◽

Eeg Recordings ◽

Memory Stage

Evidence is accumulating that the classic two-stage model of visual STM (VSTM), comprising iconic memory (IM) and visual working memory (WM), is incomplete. A third memory stage, termed fragile VSTM (FM), seems to exist in between IM and WM [Vandenbroucke, A. R. E., Sligte, I. G., & Lamme, V. A. F. Manipulations of attention dissociate fragile visual STM from visual working memory. Neuropsychologia, 49, 1559–1568, 2011; Sligte, I. G., Scholte, H. S., & Lamme, V. A. F. Are there multiple visual STM stores? PLoS One, 3, e1699, 2008]. Although FM can be distinguished from IM using behavioral and fMRI methods, the question remains whether FM is a weak expression of WM or a separate form of memory with its own neural signature. Here, we tested whether FM and WM in humans are supported by dissociable time–frequency features of EEG recordings. Participants performed a partial-report change detection task, from which individual differences in FM and WM capacity were estimated. These individual FM and WM capacities were correlated with time–frequency characteristics of the EEG signal before and during encoding and maintenance of the memory display. FM capacity showed negative alpha correlations over peri-occipital electrodes, whereas WM capacity was positively related, suggesting increased visual processing (lower alpha) to be related to FM capacity. Furthermore, FM capacity correlated with an increase in theta power over central electrodes during preparation and processing of the memory display, whereas WM did not. In addition to a difference in visual processing characteristics, a positive relation between gamma power and FM capacity was observed during both preparation and maintenance periods of the task. On the other hand, we observed that theta–gamma coupling was negatively correlated with FM capacity, whereas it was slightly positively correlated with WM. These data show clear differences in the neural substrates of FM versus WM and suggest that FM depends more on visual processing mechanisms compared with WM. This study thus provides novel evidence for a dissociation between different stages in VSTM.

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Reward-Sensitive Basal Ganglia Stabilize the Maintenance of Goal-Relevant Neural Patterns in Adolescents

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01572 ◽

2020 ◽

Vol 32 (8) ◽

pp. 1508-1524

Author(s):

Nicholas A. Hubbard ◽

Rachel R. Romeo ◽

Hannah Grotzinger ◽

Melissa Giebler ◽

Andrea Imhof ◽

...

Keyword(s):

Working Memory ◽

Basal Ganglia ◽

Functional Connectivity ◽

Adolescent Development ◽

Delayed Response ◽

Functional Connections ◽

Pattern Stability ◽

Connectivity Patterns ◽

The Stability ◽

Putative Mechanism

Maturation of basal ganglia (BG) and frontoparietal circuitry parallels developmental gains in working memory (WM). Neurobiological models posit that adult WM performance is enhanced by communication between reward-sensitive BG and frontoparietal regions, via increased stability in the maintenance of goal-relevant neural patterns. It is not known whether this reward-driven pattern stability mechanism may have a role in WM development. In 34 young adolescents (12.16–14.72 years old) undergoing fMRI, reward-sensitive BG regions were localized using an incentive processing task. WM-sensitive regions were localized using a delayed-response WM task. Functional connectivity analyses were used to examine the stability of goal-relevant functional connectivity patterns during WM delay periods between and within reward-sensitive BG and WM-sensitive frontoparietal regions. Analyses revealed that more stable goal-relevant connectivity patterns between reward-sensitive BG and WM-sensitive frontoparietal regions were associated with both greater adolescent age and WM ability. Computational lesion models also revealed that functional connections to WM-sensitive frontoparietal regions from reward-sensitive BG uniquely increased the stability of goal-relevant functional connectivity patterns within frontoparietal regions. Findings suggested (1) the extent to which goal-relevant communication patterns within reward-frontoparietal circuitry are maintained increases with adolescent development and WM ability and (2) communication from reward-sensitive BG to frontoparietal regions enhances the maintenance of goal-relevant neural patterns in adolescents' WM. The maturation of reward-driven stability of goal-relevant neural patterns may provide a putative mechanism for understanding the developmental enhancement of WM.

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Theta and Gamma Power Increases and Alpha/Beta Power Decreases with Memory Load in an Attractor Network Model

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00029 ◽

2011 ◽

Vol 23 (10) ◽

pp. 3008-3020 ◽

Cited By ~ 88

Author(s):

Mikael Lundqvist ◽

Pawel Herman ◽

Anders Lansner

Keyword(s):

Working Memory ◽

Single Cell ◽

Network Model ◽

Memory Load ◽

Cell Activity ◽

Gamma Oscillations ◽

Attractor Network ◽

Beta Power ◽

Gamma Power ◽

Alpha Beta

Changes in oscillatory brain activity are strongly correlated with performance in cognitive tasks and modulations in specific frequency bands are associated with working memory tasks. Mesoscale network models allow the study of oscillations as an emergent feature of neuronal activity. Here we extend a previously developed attractor network model, shown to faithfully reproduce single-cell activity during retention and memory recall, with synaptic augmentation. This enables the network to function as a multi-item working memory by cyclic reactivation of up to six items. The reactivation happens at theta frequency, consistently with recent experimental findings, with increasing theta power for each additional item loaded in the network's memory. Furthermore, each memory reactivation is associated with gamma oscillations. Thus, single-cell spike trains as well as gamma oscillations in local groups are nested in the theta cycle. The network also exhibits an idling rhythm in the alpha/beta band associated with a noncoding global attractor. Put together, the resulting effect is increasing theta and gamma power and decreasing alpha/beta power with growing working memory load, rendering the network mechanisms involved a plausible explanation for this often reported behavior.

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Conceptual short-term memory (CSTM) supports core claims of Christiansen and Chater

Behavioral and Brain Sciences ◽

10.1017/s0140525x15000928 ◽

2016 ◽

Vol 39 ◽

Author(s):

Mary C. Potter

Keyword(s):

Working Memory ◽

Rapid Serial Visual Presentation ◽

Language Comprehension ◽

Short Term Memory ◽

Visual Presentation ◽

Long Term Memory ◽

Short Term ◽

Term Memory ◽

Use Of Knowledge

AbstractRapid serial visual presentation (RSVP) of words or pictured scenes provides evidence for a large-capacity conceptual short-term memory (CSTM) that momentarily provides rich associated material from long-term memory, permitting rapid chunking (Potter 1993; 2009; 2012). In perception of scenes as well as language comprehension, we make use of knowledge that briefly exceeds the supposed limits of working memory.

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