Infragranular Sources of Sustained Local Field Potential Responses in Macaque Primary Visual Cortex

Maier, Alexander; Aura, Christopher J.; Leopold, David A.

doi:10.1523/jneurosci.5300-09.2011

Cited by 102 publications

(127 citation statements)

References 48 publications

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“…For the trialby-trial correlation, we did not observe a correlation in the same frequency range. The results for this frequency band were, however, in line with previous findings that β-band EEG power is anticorrelated to the BOLD signal (24,27) and is predominantly measured in the LFP recorded from infragranular layers in nonhuman animals (8). The deep layers are therefore also a likely source for the β-attention effect in the EEG measured here.…”

Section: Discussionsupporting

confidence: 92%

“…For the β-band, we observed a negative correlation in deep layers that is particularly strong in V1 and V2. This finding corresponds with laminar recordings in animals that find the strongest β-band synchronization in deep layers (8). Furthermore, β-activity in early visual regions has been associated with top-down streams of information from higher order regions (2,3,48,51).…”

Section: Discussionsupporting

confidence: 86%

“…Intracranial electrophysiological recordings in animals have linked neuronal oscillations in different frequency bands to the cortical feedforward and feedback information flow and to cortico-subcortical interactions (2)(3)(4)(5). In line with these findings, electrophysiological recordings in animals have also demonstrated that changes in α-, β-, and γ-bands can be localized to specific cortical layers (6)(7)(8)(9)(10)(11)(12).…”

mentioning

confidence: 73%

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The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

Scheeringa

Koopmans

Mourik

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

159

152

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Electrophysiological recordings in animals have indicated that visual cortex γ-band oscillatory activity is predominantly observed in superficial cortical layers, whereas α-and β-band activity is stronger in deep layers. These rhythms, as well as the different cortical layers, have also been closely related to feedforward and feedback streams of information. Recently, it has become possible to measure laminar activity in humans with high-resolution functional MRI (fMRI). In this study, we investigated whether these different frequency bands show a differential relation with the laminar-resolved blood-oxygen level-dependent (BOLD) signal by combining data from simultaneously recorded EEG and fMRI from the early visual cortex. Our visual attention paradigm allowed us to investigate how variations in strength over trials and variations in the attention effect over subjects relate to each other in both modalities. We demonstrate that γ-band EEG power correlates positively with the superficial layers' BOLD signal and that β-power is negatively correlated to deep layer BOLD and α-power to both deep and superficial layer BOLD. These results provide a neurophysiological basis for human laminar fMRI and link human EEG and high-resolution fMRI to systems-level neuroscience in animals.cortical layers | oscillations | high-resolution fMRI | EEG T he different cortical layers have distinct anatomical connections with subcortical, upstream, and downstream cortical regions (1). Intracranial electrophysiological recordings in animals have linked neuronal oscillations in different frequency bands to the cortical feedforward and feedback information flow and to cortico-subcortical interactions (2-5). In line with these findings, electrophysiological recordings in animals have also demonstrated that changes in α-, β-, and γ-bands can be localized to specific cortical layers (6-12).These findings are almost exclusively based on nonhuman animal research. Although a recent study explored the feasibility of measuring laminar-specific activity with magnetoencephalography (MEG) (13), most recent advances in measuring laminar activity in humans have been made using high-resolution functional MRI (fMRI) (14-18). In this study, we make use of these recent developments to investigate the relationship between electrophysiology and the laminar-specific blood oxygen level-dependent (BOLD) signal. By simultaneously measuring EEG and high-resolution fMRI in humans performing a visual attention task, we demonstrate that changes in specific frequency bands in the EEG can be related to changes in the BOLD signal measured at different cortical depths.The BOLD signal is thought to be closely related to variations in local field potentials (19-21). A wide variety of features in the local field potential (LFP) or EEG, related to several cognitive processes, have now been found to correlate with the BOLD signal (19,20,(22)(23)(24)(25)(26). Most relevant for this study, α-and β-power changes in EEG correlate negatively with the BOLD signal whereas γ-band...

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 86%

mentioning

confidence: 73%

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The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

Scheeringa

Koopmans

Mourik

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

159

152

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“…Interestingly, recent neurophysiological work has indicated that gamma-band oscillations are particularly strong in superficial layers of the cortical column (Lakatos et al, 2005;Maier et al, 2010Maier et al, , 2011. These superficial layers have dense "forward" connections to higher-order areas (Thomson and Bannister, 2003).…”

Section: Discussionmentioning

confidence: 99%

Prior Expectation Mediates Neural Adaptation to Repeated Sounds in the Auditory Cortex: An MEG Study

Todorović

Ede²,

Maris³

et al. 2011

Journal of Neuroscience

378

349

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Repetition suppression, the phenomenon that the second presentation of a stimulus attenuates neural activity, is typically viewed as an automatic consequence of repeated stimulus presentation. However, a recent neuroimaging study has suggested that repetition suppression may be driven by top-down expectations. Here we examined whether and when repetition suppression can be modulated by top-down expectation. Participants listened to auditory stimuli in blocks where tone repetitions were either expected or unexpected, while we recorded ongoing neural activity using magnetoencephalography. We found robust repetition suppression in the auditory cortex for repeated tones. Interestingly, this reduction was significantly larger for expected than unexpected repetitions, both in terms of evoked activity and gamma-band synchrony. These findings indicate a role of top-down expectation in generating repetition suppression and are in line with predictive coding models of perception, in which the difference between expected and actual input is propagated from lower to higher cortical areas.

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“…Several groups have studied V1 laminar variation (5,8,9,25,(47)(48)(49) by using spike-field coherence analysis (25), current source density analysis (5,49,50), or the BOLD signal in functional MRI (47). In this study, we used drifting gratings with spatial frequency equal to two cycles per degree, which are optimal stimuli for stimulating neurons in the V1 network (20,51).…”

Section: Dynamics Of γ-Band Power At Different Cortical Depths In V1mentioning

confidence: 99%

Laminar analysis of visually evoked activity in the primary visual cortex

Xing

Yeh

Burns

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

189

166

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Studying the laminar pattern of neural activity is crucial for understanding the processing of neural signals in the cerebral cortex. We measured neural population activity [multiunit spike activity (MUA) and local field potential, LFP] in Macaque primary visual cortex (V1) in response to drifting grating stimuli. Sustained visually driven MUA was at an approximately constant level across cortical depth in V1. However, sustained, visually driven, local field potential power, which was concentrated in the γ-band (20-60 Hz), was greatest at the cortical depth corresponding to corticocortical output layers 2, 3, and 4B. γ-band power also tends to be more sustained in the output layers. Overall, cortico-cortical output layers accounted for 67% of total γ-band activity in V1, whereas 56% of total spikes evoked by drifting gratings were from layers 2, 3, and 4B. The high-resolution layer specificity of γ-band power, the laminar distribution of MUA and γ-band activity, and their dynamics imply that neural activity in V1 is generated by laminar-specific mechanisms. In particular, visual responses of MUA and γ-band activity in cortico-cortical output layers 2, 3, and 4B seem to be strongly influenced by laminar-specific recurrent circuitry and/or feedback.B ased on anatomy and neurophysiology, our view of the cerebral cortex has changed. Instead of viewing the cortex as a single network, we now conceive of the cortical laminae as a stack of loosely interconnected but distinct neuronal networks (1-5). Each lamina has different specific inputs, projection targets, and feedback connections.The goal of this study is the determination of the spatial distribution of stimulus-driven neural activity throughout the depth of the cortex and across cortical laminae. Pursuing this goal, we chose to study Macaque primary visual cortex (V1), because V1 is a cortical area where the experimenter has control of the neuronal input by controlling visual stimulation. V1 laminar inputs, outputs, and local connections are well-known (1, 3, 6). Signals come from the thalamus [lateral geniculate nucleus (LGN)] into V1 layers 4C and 6. After intracortical processing, neuronal signals are routed to other cortical areas from cells in superficial layers 2, 3, and 4B of V1; subcortical targets receive cortical outputs from cells in layers 5 and 6. Extrastriate cortical feedback targets layers 2, 3, and 6 (1, 3, 7). The visual functional properties of cells in different layers are markedly different (2, 8-13), reflecting local circuitry that is layer-specific (1, 3, 6). Because of the similarities of laminar cortical circuitry throughout the cerebral cortex (14-16), we used V1 as a test bed to study laminar patterns of stimulus-driven responses.To sample from many neurons in each layer, we measured multiunit spike activity (MUA) and the local field potential (LFP) with multiple microelectrodes (Methods details the operational definitions of MUA and LFP). We measured the power in the LFP at frequencies < 100 Hz, because the largest changes in LFP power...

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Infragranular Sources of Sustained Local Field Potential Responses in Macaque Primary Visual Cortex

Cited by 102 publications

References 48 publications

The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

Prior Expectation Mediates Neural Adaptation to Repeated Sounds in the Auditory Cortex: An MEG Study

Laminar analysis of visually evoked activity in the primary visual cortex

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