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Detecting imminent collisions is essential for our survival and is likely supported by evolutionarily conserved mechanisms in the brain. Using high-resolution 7T fMRI, we investigated subcortical pathways for detecting collision trajectories in healthy human subjects and hemianopic patients. When healthy participants focused their attention on a central fixation task, their superior colliculus (SC), ventromedial pulvinar (vmPul) and ventral tegmental area (VTA) elicited stronger responses to a peripheral object approaching on head-collision courses compared to near-miss trajectories. Correlation and path analyses of collision-sensitive responses revealed collision sensitivity in the SC-vmPul and SC-VTA pathways without attention and cortical influence. Both behavioral performance and SC responses showed higher sensitivity to looming stimuli from the upper visual field. For hemianopic patients with unilateral lesions of the geniculostriate pathway, the ipsilesional SC, vmPul and VTA showed collision sensitivity to looming stimuli in their blind visual field, in the absence of their awareness. Stronger responses in the SC were also associated with better detection performance of the collision events. These findings clearly demonstrate that human tectofugal pathways, without attention and awareness, automatically detects approaching objects on a collision course, supporting blindsight to impending visual threats.HighlightsSC-vmPul and SC-VTA pathways show collision sensitivity without attention and cortical influence in healthy participants.Both behavioral performance and SC responses show higher sensitivity to looming stimuli from the upper visual field.The ipsilesional SC, vmPul and VTA of hemianopic patients automatically detects collision trajectories in their blind visual field without awareness.SC response is associated with “blindsight” detection of impending collisions.

Laminar fMRI based on BOLD and CBV contrast at ultrahigh magnetic fields has been applied for studying the dynamics of mesoscopic brain networks. However, the quantitative interpretations of BOLD/CBV fMRI results are confounded by different baseline physiology across cortical layers. Here we introduce a novel 3D zoomed pseudo-continuous arterial spin labeling technique at 7T that offers the unique capability for quantitative measurements of laminar cerebral blood flow (CBF) both at rest and during task activation with high spatial specificity and sensitivity. We found arterial transit time in superficial layers is ∼100 msec shorter than in middle/deep layers revealing the dynamics of labeled blood flowing from pial arteries to downstream microvasculature. Resting state CBF peaked in the middle layers which is highly consistent with microvascular density measured from human cortex specimens. Finger tapping induced a robust two-peak laminar profile of CBF increases in the superficial (somatosensory and premotor input) and deep (spinal output) layers of M1, while finger brushing task induced a weaker CBF increase in superficial layers (somatosensory input). We further demonstrated that top-down attention induced a predominant CBF increase in deep layers and a smaller CBF increase on top of the lower baseline CBF in superficial layers of V1 (feedback cortical input), while bottom-up stimulus driven activity peaked in the middle layers (feedforward thalamic input). These quantitative laminar profiles of perfusion activity suggest an important role of M1 superficial layers for the computation of finger movements, and that visual attention may amplify deep layer output to the subcortex.Significance StatementCBF or microvascular perfusion measured by arterial spin labeling (ASL) is a key parameter for in vivo assessment of neurovascular function. Compared to BOLD or VASO fMRI, ASL perfusion contrast offers the unique capability for quantitative CBF measurements both at baseline and during task activation, which is critical for quantitative estimation of metabolic activities tightly related to neuronal activation. We proposed a zoomed 3D ASL technique at 7T for laminar perfusion imaging with high spatial specificity and sensitivity. This technique is able to differentiate and quantify the input/output and feedforward/feedback activities of human motor and visual cortex, thereby providing an important tool for quantitative assessment of neurovascular function and metabolic activities of neural circuits across cortical layers.

Attention mechanisms at different cortical layers of human visual cortex remain poorly understood. Using submillimeter-resolution fMRI at 7T, we investigated the effects of top-down spatial attention on the contrast responses across different cortical depths in human early visual cortex. Gradient echo (GE) T2* weighted BOLD signal showed an additive effect of attention on contrast responses across cortical depths. Compared to the middle cortical depth, attention modulation was stronger in the superficial and deep depths of V1, and also stronger in the superficial depth of V2 and V3. Using ultra-high resolution (0.3mm in-plane) balanced steady-state free precession (bSSFP) fMRI, a multiplicative scaling effect of attention was found in the superficial and deep layers, but not in the middle layer of V1. Attention modulation of low contrast response was strongest in the middle cortical depths, indicating baseline enhancement or contrast gain of attention modulation on feedforward input. Finally, the additive effect of attention on T2* BOLD can be explained by strong nonlinearity of BOLD signals from large blood vessels, suggesting multiplicative effect of attention on neural activity. These findings support that top-down spatial attention mainly operates through feedback connections from higher order cortical areas, and a distinct mechanism of attention may also be associated with feedforward input through subcortical pathway.HighlightsResponse or activity gain of spatial attention in superficial and deep layersContrast gain or baseline shift of attention in V1 middle layerNonlinearity of large blood vessel causes additive effect of attention on T2* BOLD