High-Resolution fMRI Reveals Laminar Differences in Neurovascular Coupling between Positive and Negative BOLD Responses

Abstract

SUMMARY The six cortical layers have distinct anatomical and physiological properties, like different energy use and different feedforward and feedback connectivity. It is not known if and how layer-specific neural processes are reflected in the fMRI signal. To address this question we used high-resolution fMRI to measure BOLD, CBV, and CBF responses to stimuli that elicit positive and negative BOLD signals in macaque primary visual cortex. We found that regions with positive BOLD responses had parallel increases in CBV and CBF, whereas areas with negative BOLD responses showed a decrease in CBF but an increase in CBV. For positive BOLD responses, CBF and CBV increased in the center of the cortex, but for negative BOLD responses, CBF decreased superficially while CBV increased in the center. Our findings suggest different mechanisms for neurovascular coupling for BOLD increases and decreases, as well as laminar differences in neurovascular coupling.

Investigation of the neurovascular coupling in positive and negative BOLD responses in human brain at 7T

“…During inhibitory tasks, NBR amplitude was larger (p < 0.05) in deeper laminae (Fig. 3B), as observed previously (Boorman et al, 2010;Goense et al, 2012).…”

“…The full field stimulation paradigm was used for comparison of the same cortical regions during different stimulation paradigms. For the sake of comparison with recently published results in monkeys, a rotating ring checkerboard (rotation 2π/3 rad/s, switching rotation direction every 1.5-6 s) was also presented (Goense et al, 2012;Shmuel et al, 2006) (Fig. 1).…”

“…magnet and RF coils) and animal preparation (e.g. anesthesia and rotating ring stimulus presentation) please refer to (Goense et al, 2012;Logothetis et al, 1999;Pfeuffer et al, 2004). The adapted SS-SI-VASO parameters were 0.6332 x 0.75 x 3 mm 3 nominal voxel size and TE/TI 1 /TI 2 /TR = 7.8/785/2285/3000 ms.…”

“…More refined layer-dependent studies of NBR in sensory motor cortex of rats and visual cortex of monkeys suggest that the NBR peaks in deeper cortical layers, while the positive gradient echo (GE) BOLD response (PBR) peaks at the cortical surface (Boorman et al, 2010;Goense et al, 2012). The role of cerebral blood volume (CBV) in NBR has remained elusive.…”

“…Measurements with OIS and monocrystalline iron oxide nanoparticles (MION) reveal vasoconstriction in regions of NBR in rat somatosensory cortex (Boorman et al, 2010;Kennerley et al, 2012b) and cat extrastriate cortex (Harel et al, 2002). Goense et al (2012), on the other hand, investigated CBV changes in regions of NBR with vascular space occupancy (VASO) (Lu et al, 2003;Yang et al, 2004) and MION in visual cortex of monkeys. They reported a significant and surprising increase of CBV in deeper layers of the cortex during inhibitory tasks (Smirnakis et al, 2007).…”