Contextual Feedback to Superficial Layers of V1

Abstract

SummaryNeuronal cortical circuitry comprises feedforward, lateral, and feedback projections, each of which terminates in distinct cortical layers [1–3]. In sensory systems, feedforward processing transmits signals from the external world into the cortex, whereas feedback pathways signal the brain’s inference of the world [4–11]. However, the integration of feedforward, lateral, and feedback inputs within each cortical area impedes the investigation of feedback, and to date, no technique has isolated the feedback of visual scene information in distinct layers of healthy human cortex. We masked feedforward input to a region of V1 cortex and studied the remaining internal processing. Using high-resolution functional brain imaging (0.8 mm3) and multivoxel pattern information techniques, we demonstrate that during normal visual stimulation scene information peaks in mid-layers. Conversely, we found that contextual feedback information peaks in outer, superficial layers. Further, we found that shifting the position of the visual scene surrounding the mask parametrically modulates feedback in superficial layers of V1. Our results reveal the layered cortical organization of external versus internal visual processing streams during perception in healthy human subjects. We provide empirical support for theoretical feedback models such as predictive coding [10, 12] and coherent infomax [13] and reveal the potential of high-resolution fMRI to access internal processing in sub-millimeter human cortex.

Laminar fMRI: Applications for cognitive neuroscience

“…Therefore, studies using laminar fMRI have typically divided gray matter into several evenly spaced bins, as an approximation of the underlying cortical laminae ( Figure 1A and B). Consistent with the known functional architecture of the cortical column, these studies find feedback responses in deep and superficial, but not middle, cortical bins Kok et al, 2016;Muckli et al, 2015;Scheeringa et al, 2016). …”

Cortical feedback signals generalise across different spatial frequencies of feedforward inputs

“…To test feedback signals in the absence of feedforward stimulation, we used an occlusion paradigm 96 previously employed by Smith and Muckli (2010), Muckli et al (2015) and Morgan et al (2016). For the 97 feedback conditions, we occluded the lower right image quadrant with a white rectangle.…”

“…We can study feedback signals by isolating them from the feedforward inputs by partially 78 occluding the image. The V1 representation of occluded regions of the visual field contains contextual 79 information (Ban et al, 2013;Shushruth, 2011;Smith and Muckli, 2010;Sugita, 1999) fed back to the 80 superficial layers (Muckli et al, 2015). Using a partial occlusion paradigm (Smith and Muckli, 2010 …”

“…However, large surround receptive fields of these voxels capture feedforward information from the 104 stimulated surround (Smith and Muckli, 2010;Muckli et al, 2015). Thus, voxels in the occluded region 105 receive information fed back from higher areas; we refer to this condition as 'feedback'.…”

“…This suggests that our SF cut-offs were not wide enough to lead to completely separate brain 430 activity patterns in the feedforward regions. Since feedback signals are likely to be even coarser than 431 feedforward signals (Muckli et al, 2015), it is unsurprising we could generalise across SF in feedback 432 conditions as well. As noted before, feedforward conditions had bottom-up stimulation which still includes 433 some feedback.…”