A dynamical model of the laminar BOLD response

Abstract

High-resolution functional magnetic resonance imaging (fMRI) using blood oxygenation dependent level-dependent (BOLD) signal is an increasingly popular tool to non-invasively examine neuronal processes at the mesoscopic level. However, as the BOLD signal stems from hemodynamic changes, its temporal and spatial properties do not match those of the underlying neuronal activity. In particular, the laminar BOLD response (LBR), commonly measured with gradient-echo (GE) MRI sequence, is confounded by non-local changes in deoxygenated hemoglobin and cerebral blood volume propagated within intracortical ascending veins, leading to a unidirectional blurring of the neuronal activity distribution towards the cortical surface. Here, we present a new cortical depth-dependent model of the BOLD response based on the principle of mass conservation, which takes the effect of ascending (and pial) veins on the cortical BOLD responses explicitly into account. It can be used to dynamically model cortical depth profiles of the BOLD signal as a function of various baselineand activity-related physiological parameters for any spatiotemporal distribution of neuronal changes. We demonstrate that the commonly observed spatial increase of LBR is mainly due to baseline blood volume increase towards the surface. In contrast, an occasionally observed local maximum in the LBR (i.e. the so-called "bump") is mainly due to spatially inhomogeneous neuronal changes rather than locally higher baseline blood volume. In addition, we show that the GE-BOLD signal laminar point-spread functions, representing the signal leakage towards the surface, depend on several physiological parameters and on the level of neuronal activity. Furthermore, even in the case of simultaneous neuronal changes at each depth, inter-laminar delays of LBR transients are present due to the ascending vein. In summary, the model provides a conceptual framework for the biophysical interpretation of common experimental observations in high-resolution fMRI data. In the future, the model will allow for deconvolution of the spatiotemporal hemodynamic bias of the LBR and provide an estimate of the underlying laminar excitatory and inhibitory neuronal activity.

Linear systems analysis for laminar fMRI: Evaluating BOLD amplitude scaling for luminance contrast manipulations

“…Responses for both sessions matched almost perfectly (explained variance 99%). (2020) 10:5462 | https://doi.org/10.1038/s41598-020-62165-x www.nature.com/scientificreports www.nature.com/scientificreports/ Markuerkiaga and colleagues 83 and Marquardt and colleagues 51 , or potentially by implementing more elaborate models of BOLD responses at different cortical depths that better capture general spatiotemporal properties of the hemodynamic signal, and the dynamics of capillary, arterial, and venous effects 23,32,34,[84][85][86][87] with respect to more traditional hemodynamic models 88,89 . We observed a relative decrease in BOLD amplitude for the most superficial depth bin in several visual field maps and for several luminance contrasts.…”

TDM: a temporal decomposition method for removing venous effects from task-based fMRI

“…Finally, a biophysical model of vascular dynamics has been proposed, and this model provides a potential explanation for why temporal delays occur in veins (see Fig. 6 in Havlicek and Uludağ, 2020).…”

Cortical Depth-Dependent Modeling of Visual Hemodynamic Responses

“…This can be addressed by developing a laminar-specific hemodynamic model. Recent studies have attempted to develop this type of hemodynamic model, including Markuerkiaga et al (2016) who proposed a two-compartment BOLD model on top of a vascular model of the cortex, Heinzle et al (2016) who proposed a balloon-based model with two cortical depths, Havlicek and Uludag (2020) who proposed a multi-compartment balloon-based model, and Puckett et al (2016) who proposed distinct spatiotemporal hemodynamic response function per cortical depth. The problem with the first three models is that they only considered temporal variations in the BOLD signal across the cortical depth, disregarding any spatial effects.…”