Laminar recordings in frontal cortex suggest distinct layers for maintenance and control of working memory

All of the cerebral cortex has some degree of laminar organization. These different layers are composed of neurons with distinct connectivity patterns, embryonic origins, and molecular profiles. There are little data on the laminar specificity of cognitive functions in the frontal cortex, however. We recorded neuronal spiking/local field potentials (LFPs) using laminar probes in the frontal cortex (PMd, 8A, 8B, SMA/ACC, DLPFC, and VLPFC) of monkeys performing working memory (WM) tasks. LFP power in the gamma band (50–250 Hz) was strongest in superficial layers, and LFP power in the alpha/beta band (4–22 Hz) was strongest in deep layers. Memory delay activity, including spiking and stimulus-specific gamma bursting, was predominately in superficial layers. LFPs from superficial and deep layers were synchronized in the alpha/beta bands. This was primarily unidirectional, with alpha/beta bands in deep layers driving superficial layer activity. The phase of deep layer alpha/beta modulated superficial gamma bursting associated with WM encoding. Thus, alpha/beta rhythms in deep layers may regulate the superficial layer gamma bands and hence maintenance of the contents of WM.

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Layer and rhythm specificity for predictive routing

10.1101/2020.01.27.921783 ◽

2020 ◽

Cited By ~ 1

Author(s):

André M. Bastos ◽

Mikael Lundqvist ◽

Ayan S. Waite ◽

Nancy Kopell ◽

Earl K. Miller

Keyword(s):

Deep Layer ◽

Predictive Coding ◽

Superficial Layer ◽

Field Potentials ◽

Cortex Area ◽

Cortical Hierarchy ◽

Area 7A ◽

Gamma Rhythms ◽

Alpha Beta ◽

High Beta

SummaryIn predictive coding, experience generates predictions that attenuate the feeding forward of predicted stimuli while passing forward unpredicted “errors”. Different models have different neural implementations of predictive coding. We recorded spikes and local field potentials from laminar electrodes in five cortical areas (V4, LIP, area 7A, FEF, and PFC) while monkeys performed a task that modulated visual stimulus predictability. Pre-stimulus predictions were associated with increased alpha/beta (8-30 Hz) power/coherence that fed back the cortical hierarchy primarily via deep-layer cortex. Unpredictable stimuli were associated with increases in spiking and in gamma-band (40-90 Hz) power/coherence that fed forward up the cortical hierarchy via superficial-layer cortex. Area 7A uniquely showed increases in high-beta (~22-28 Hz) power/coherence to unpredicted stimuli. These results suggest that predictive coding may be implemented via lower-frequency alpha/beta rhythms that “prepare” pathways processing predicted inputs by inhibiting feedforward gamma rhythms and associated spiking.

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Relating neural oscillations to laminar fMRI connectivity

10.1101/2020.09.18.303263 ◽

2020 ◽

Author(s):

René Scheeringa ◽

Mathilde Bonnefond ◽

Tim van Mourik ◽

Ole Jensen ◽

David G. Norris ◽

...

Keyword(s):

Brain Regions ◽

Superficial Layer ◽

Gamma Band ◽

Alpha Power ◽

Beta Band ◽

Beta Power ◽

Neural Processes ◽

Complex Picture ◽

Deep Layers ◽

Strong Relation

AbstractLaminar fMRI can non-invasively study brain activation and potentially connectivity at the laminar level in humans. In a previous simultaneous laminar fMRI/EEG experiment, we observed that attention effects in alpha, beta and gamma band EEG power relate to attention effects in fMRI activation in V1/V2/V3 at distinct cortical depths: alpha and gamma band EEG attention effects related to fMRI effects in superficial layers, whereas beta attention effects related to deep layers. Here we reanalyzed these data to investigate how EEG-attention effects relate to changes in connectivity between regions. We computed the fMRI-based attention effect on laminar connectivity between regions within a hemisphere and connectivity between layers within brain regions. We observed that the beta band strongly relates to laminar specific changes in connectivity. Our results indicate that the attention-related decrease in beta power relates to an increase in deep-to-deep layer connectivity between regions and deep/middle to superficial layer connectivity within brain regions. The attention related alpha power increase predominantly relates to increases in connectivity between deep and superficial layers within brain regions. We observed no strong relation between laminar connectivity and gamma band oscillations. These results indicate that especially beta band oscillations, and to a lesser extent alpha band oscillations relate to laminar specific changes in connectivity as measured by laminar fMRI. Together, the effects for the alpha and beta bands suggest a complex picture of possibly co-occurring neural processes that can differentially affect laminar connectivity.

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Layer and rhythm specificity for predictive routing

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2014868117 ◽

2020 ◽

Vol 117 (49) ◽

pp. 31459-31469 ◽

Cited By ~ 2

Author(s):

André M. Bastos ◽

Mikael Lundqvist ◽

Ayan S. Waite ◽

Nancy Kopell ◽

Earl K. Miller

Keyword(s):

Predictive Coding ◽

Superficial Layer ◽

Frontal Eye Field ◽

Beta Power ◽

Deep Layers ◽

Eye Field ◽

Area 7A ◽

Posterior Parietal ◽

Alpha Beta ◽

High Beta

In predictive coding, experience generates predictions that attenuate the feeding forward of predicted stimuli while passing forward unpredicted “errors.” Different models have suggested distinct cortical layers, and rhythms implement predictive coding. We recorded spikes and local field potentials from laminar electrodes in five cortical areas (visual area 4 [V4], lateral intraparietal [LIP], posterior parietal area 7A, frontal eye field [FEF], and prefrontal cortex [PFC]) while monkeys performed a task that modulated visual stimulus predictability. During predictable blocks, there was enhanced alpha (8 to 14 Hz) or beta (15 to 30 Hz) power in all areas during stimulus processing and prestimulus beta (15 to 30 Hz) functional connectivity in deep layers of PFC to the other areas. Unpredictable stimuli were associated with increases in spiking and in gamma-band (40 to 90 Hz) power/connectivity that fed forward up the cortical hierarchy via superficial-layer cortex. Power and spiking modulation by predictability was stimulus specific. Alpha/beta power in LIP, FEF, and PFC inhibited spiking in deep layers of V4. Area 7A uniquely showed increases in high-beta (∼22 to 28 Hz) power/connectivity to unpredictable stimuli. These results motivate a conceptual model, predictive routing. It suggests that predictive coding may be implemented via lower-frequency alpha/beta rhythms that “prepare” pathways processing-predicted inputs by inhibiting feedforward gamma rhythms and associated spiking.

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Working memory alpha-beta band oscillatory signatures in adolescents and young adults

European Journal of Neuroscience ◽

10.1111/ejn.13897 ◽

2018 ◽

Vol 48 (7) ◽

pp. 2527-2536 ◽

Cited By ~ 5

Author(s):

Nowell Zammit ◽

Owen Falzon ◽

Kenneth Camilleri ◽

Richard Muscat

Keyword(s):

Working Memory ◽

Young Adults ◽

Adolescents And Young Adults ◽

Beta Band ◽

Alpha Beta

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Maintenance and Manipulation in Working Memory: Differential Ventral and Dorsal Frontal Cortex fMRI Activity

Acta Psychologica Sinica ◽

10.3724/sp.j.1041.2009.01054 ◽

2009 ◽

Vol 41 (11) ◽

pp. 1054-1062 ◽

Cited By ~ 1

Author(s):

Pudas Sara ◽

Persson Jonas ◽

Nilsson L-G ◽

Nyberg Lars

Keyword(s):

Working Memory ◽

Frontal Cortex

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Working memory load impairs the evaluation of behavioral errors in the medial frontal cortex

Psychophysiology ◽

10.1111/psyp.12899 ◽

2017 ◽

Vol 54 (10) ◽

pp. 1472-1482 ◽

Cited By ~ 9

Author(s):

Martin E. Maier ◽

Marco Steinhauser

Keyword(s):

Working Memory ◽

Frontal Cortex ◽

Memory Load ◽

Medial Frontal Cortex ◽

Working Memory Load

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Reading comprehension on the last grades of cicles I and II of elementary school

CoDAS ◽

10.1590/2317-1782/201420130069 ◽

2014 ◽

Vol 26 (4) ◽

pp. 276-285

Author(s):

Eliane Mi Chang ◽

Clara Regina Brandão de Avila

Keyword(s):

Working Memory ◽

Elementary School ◽

Reading Comprehension ◽

Research Groups ◽

Control Groups ◽

Short Term ◽

Good Readers ◽

Spearman Coefficient ◽

Positive Correlations ◽

And Control

PURPOSE: To characterize students' performance in Cycle I and II of the Elementary School (EF), in decoding, reading comprehension and underlying skills of reading, and investigate correlations between these variables, in the absence and presence of reading comprehension deficits, identified by their teachers.METHODS: 125 students from ES were grouped according to Cycle and presence or absence of reading comprehension impairments. Two Control (good readers from both Cycles) and two Research groups (poor readers from both Cycles) were established. Assessment involved: fluency and reading comprehension; oral comprehension; working and short-term phonological memory; grammar closure. It was compared (Mann-Whitney test): in intragroup study, both Control and Research groups; in intergroup study, Control and Research from different cycles, and Control I and Research II. Spearman coefficient investigated correlations.RESULTS: Analyzing reading comprehension, we observed better performance of Control Groups in all tasks in comparison to the respective Research Groups, and better performance of Control II in comparison to Control I. Research Groups had similar results in most tests. Positive correlations have been observed between most of the variables.CONCLUSION: Students without reading comprehension impairments showed better performance in reading in both Cycles. Working memory and oral comprehension did not differentiate students with and without complaints in Cycle I, differently from what was observed in Cycle II. Research II presented similar or better performance than Research I and similar or worse performance than Control I. Underlying skills showed different profiles of correlation with reading comprehension capacity, according to the group.

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Abnormal brain activity patterns during spatial working memory task in patients with end-stage renal disease on maintenance hemodialysis: a fMRI study

Brain Imaging and Behavior ◽

10.1007/s11682-020-00383-7 ◽

2020 ◽

Author(s):

Jinzhuang Huang ◽

Lei Xie ◽

Ruiwei Guo ◽

Jinhong Wang ◽

Jinquan Lin ◽

...

Keyword(s):

Working Memory ◽

Frontal Cortex ◽

Spatial Working Memory ◽

Brain Activity ◽

Activity Patterns ◽

Parietal Lobule ◽

Stage Renal Disease ◽

End Stage ◽

Esrd Patients ◽

Back Task

Abstract Hemodialysis (HD) is associated with cognitive impairment in patients with end-stage renal disease (ESRD). However, the neural mechanism of spatial working memory (SWM) impairment in HD-ESRD patients remains unclear. We investigated the abnormal alterations in SWM-associated brain activity patterns in HD-ESRD patients using blood oxygen level-dependent functional magnetic resonance imaging (BOLD-fMRI) technique during n-back tasks. Twenty-two HD-ESRD patients and 22 well-matched controls underwent an fMRI scan while undergoing a three-load n-back tasks with different difficulty levels. Cognitive and mental states were assessed using a battery of neuropsychologic tests. The HD-ESRD patients exhibited worse memory abilities than controls. Compared with the control group, the HD-ESRD patient group showed lower accuracy and longer response time under the n-back tasks, especially in the 2-back task. The patterns of brain activation changed under different working memory loads in the HD-ESRD patients, showing decreased activity in the right medial frontal gyrus and inferior frontal gyrus under 0-back and 1-back task, while more decreased activation in the bilateral frontal cortex, parietal lobule, anterior/posterior cingulate cortex and insula cortex under 2-back task. With the increase of task difficulty, the activation degree of the frontal and parietal cortex decreased. More importantly, we found that lower activation in frontal cortex and parietal lobule was associated with worse cognitive function in the HD-ESRD patients. These results demonstrate that the abnormal brain activity patterns of frontal cortex and parietal lobule may reflect the neural mediation of SWM impairment.

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GABAA and GABAC Receptors Have Contrasting Effects on Excitability in Superior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.1999.82.4.2020 ◽

1999 ◽

Vol 82 (4) ◽

pp. 2020-2023 ◽

Cited By ~ 35

Author(s):

Michael Pasternack ◽

Mathias Boller ◽

Belinda Pau ◽

Matthias Schmidt

Keyword(s):

Superior Colliculus ◽

Receptor Agonist ◽

Brain Slices ◽

Superficial Layer ◽

Field Potentials ◽

Competitive Antagonist ◽

Postsynaptic Potential ◽

Late Potential ◽

Receptor Agonists And Antagonists

We have recently found that GABAC receptor subunit transcripts are expressed in the superficial layers of rat superior colliculus (SC). In the present study we used immunocytochemistry to demonstrate the presence of GABAC receptors in rat SC at protein level. We also investigated in acute rat brain slices the effect of GABAA and GABAC receptor agonists and antagonists on stimulus-evoked extracellular field potentials in SC. Electrical stimulation of the SC optic layer induced a biphasic, early and late, potential in the adjacent superficial layer. The late component was completely inhibited by 6-cyano-7-nitroquinoxaline-2,3-dione or CoCl2, indicating that it was generated by postsynaptic activation. Muscimol, a potent GABAA and GABAC receptor agonist, strongly attenuated this postsynaptic potential at concentrations >10 μM. In contrast, the GABAC receptor agonist cis-aminocrotonic acid, as well as muscimol at lower concentrations (0.1–1 μM) increased the postsynaptic potential. This increase was blocked by (1,2,5,6-tetrahydropyridine-4-yl)methylphosphinic acid, a novel competitive antagonist of GABAC receptors. Our findings demonstrate the presence of functional GABAC receptors in SC and suggest a disinhibitory role of these receptors in SC neuronal circuitry.

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