Elsevier

NeuroImage

Volume 141, 1 November 2016, Pages 250-261
NeuroImage

Lamina-dependent calibrated BOLD response in human primary motor cortex

https://doi.org/10.1016/j.neuroimage.2016.06.030Get rights and content

Abstract

Disentangling neural activity at different cortical depths during a functional task has recently generated growing interest, since this would allow to separate feedforward and feedback activity. The majority of layer-dependent studies have, so far, relied on gradient-recalled echo (GRE) blood-oxygenation-level dependent (BOLD) acquisitions, which are weighted towards the large draining veins at the cortical surface. The current study aims to obtain quantitative brain activity responses in the primary motor cortex on a laminar scale without the contamination due to accompanying secondary vascular effects.

Evoked oxidative metabolism was evaluated using the Davis model, to investigate its applicability, advantages, and limits in lamina-dependent fMRI. Average values for the calibration parameter, M, and for changes in the cerebral metabolic rate of oxygen consumption (CMRO2) during a unilateral finger-tapping task were (11 ± 2)% and (30 ± 7)%, respectively, with distinct variation features across the cortical depth. The results presented here showed an uncoupling between BOLD-based functional magnetic resonance imaging (fMRI) and metabolic changes across cortical depth, while the tight coupling between CMRO2 and CBV was conserved across cortical layers.

We conclude that the Davis model can help to obtain estimates of lamina-dependent metabolic changes without contamination from large draining veins, with high consistency and reproducibility across participants.

Section snippets

Mathematical symbols

    [X]:

    concentration of compound X;

    .0:

    index indicating a baseline (‘rest’) level;

    .t:

    index indicating the total blood compartment;

    .v:

    index indicating the venous compartment;

    CBF:

    cerebral blood flow;

    CBV:

    cerebral blood volume;

    CMRO2:

    cerebral metabolic rate of oxygen consumption;

    f:

    relative CBF;

    M:

    calibration constant, i.e., maximal BOLD signal change;

    n:

    metabolic-vascular coupling factor;

    R2:

    (irreversible) transverse relaxation rate;

    R2′:

    effective transverse relaxation rate induced by external fields;

    r:

Calculation of CMRO2 and scaled profiles

The Davis model assumes the following relationship (Davis et al., 1998, Hoge et al., 1999):δSact=M1vvfβrβ,

where δSact = (Sact  S0)/S0 is the relative BOLD signal change (induced either by a task or a gas manipulation) from the baseline value, S0, and β is a constant describing the coupling between the effective transverse relaxation rate induced by external fields, R2′, and the dHb concentration according to.R2'=κCBVdHbβ.

κ is a proportionality constant that varies with magnetic field

Results

Robust BOLD and VASO activations were found in all participants within the hand-knob area (Fig. 4).

The average temporal SNR (tSNR) was (20.7 ± 2.2) for BOLD and (15.2 ± 2.4) for VASO. The functional CNR (defined as (∆ S/S)  tSNR) for the finger-tapping contrast was (0.9 ± 0.3) for BOLD and (− 0.4 ± 0.2) for VASO; the functional CNR for the pure hypercapnia challenge (i.e., without concomitant tapping) was (1.1 ± 0.2) for BOLD and (− 0.4 ± 0.1) for VASO. The statistical activation maps show the responses under

Discussion

The data from our study suggest that sufficient CNR was obtained to investigate simultaneously recorded BOLD and CBV responses during finger tapping and hypercapnia, as well as for high-resolution estimation of CMRO2. Fig. 3 demonstrates that significant changes in BOLD and VASO signals are consistently detected across participants. Independent of this consistent detectability, however, there is relatively large variability in the amplitude of the functional responses across participants,

Conclusion

We have demonstrated that it is possible to measure CBV and BOLD signal changes during finger tapping and hypercapnia on a submillimeter laminar level. By application of a modified Davis model, this data can be used to estimate changes of CMRO2 and the value of the calibration parameter M across the cortical thickness on this laminar scale. We have shown that there are differences in depth-dependent activation profiles of the BOLD signal and CBV and that these features are consistent across

Acknowledgements

This study was supported by the Initial Training Network, HiMR, funded by the FP7 Marie Curie Actions of the European Commission (FP7-PEOPLE-2012-ITN-316716). We thank Enrico Reimer for IT support regarding MRI data conversion and developing a 3D MRI data projection viewer for planning slice orientation. We also thank Riccardo Metere for fruitful discussions and Domenica Wilfling and Elisabeth Wladimirow for radiographic assistance. Parts of the this work have been presented at the 23rd Annual

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    1

    Present address: Laurentius Huber, Ph.D. Section on Functional Imaging Methods Laboratory of Brain and Cognition, National Institute of Mental Health, Building 10, Room 1D80 10, Center Dr. MSC 1148 Bethesda, MD 20892-1148, USA.

    2

    Present address: Claudine J. Gauthier, Ph.D., Richard J. Renaud Science Complex, 7141 Sherbrooke W. Concordia University, Montréal, Québec, Canada.

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