Selective Activation of the Deep Layers of the Human Primary Visual Cortex by Top-Down Feedback

Abstract

In addition to bottom-up input, the visual cortex receives large amounts of feedback from other cortical areas [1-3]. One compelling example of feedback activation of early visual neurons in the absence of bottom-up input occurs during the famous Kanizsa illusion, where a triangular shape is perceived, even in regions of the image where there is no bottom-up visual evidence for it. This illusion increases the firing activity of neurons in the primary visual cortex with a receptive field on the illusory contour [4]. Feedback signals are largely segregated from feedforward signals within each cortical area, with feedforward signals arriving in the middle layer, while top-down feedback avoids the middle layers and predominantly targets deep and superficial layers [1, 2, 5, 6]. Therefore, the feedback-mediated activity increase in V1 during the perception of illusory shapes should lead to a specific laminar activity profile that is distinct from the activity elicited by bottom-up stimulation. Here, we used fMRI at high field (7 T) to empirically test this hypothesis, by probing the cortical response to illusory figures in human V1 at different cortical depths [7-14]. We found that, whereas bottom-up stimulation activated all cortical layers, feedback activity induced by illusory figures led to a selective activation of the deep layers of V1. These results demonstrate the potential for non-invasive recordings of neural activity with laminar specificity in humans and elucidate the role of top-down signals during perceptual processing.

The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

“…This finding is supported by laminar recordings in animals reporting both supraand infragranular sources (9,12) and relating α-activity to feedback projections that target both supra-and infragranular layers (4). Consistently, laminar fMRI work has linked feedback processes to both superficial (17) and deep layers (18). Interestingly, the attention modulation in the α-band is coupled to BOLD only in superficial layers.…”

“…Although a recent study explored the feasibility of measuring laminar-specific activity with magnetoencephalography (MEG) (13), most recent advances in measuring laminar activity in humans have been made using high-resolution functional MRI (fMRI) (14)(15)(16)(17)(18). In this study, we make use of these recent developments to investigate the relationship between electrophysiology and the laminar-specific blood oxygen level-dependent (BOLD) signal.…”

Prospective motion correction improves the sensitivity of fMRI pattern decoding

“…Across two fMRI resolutions, we found evidence that PMC application improves data quality at higher resolutions (1.5 mm). Given the increasing interest in laminar structures and fine scale functional specialization that are only visible at submillimeter resolution (Gilbert, Henson, & Simons, 2010; Kok, Bains, Van Mourik, Norris, & De Lange, 2016; Xing, Yeh, Burns, & Shapley, 2012; Yacoub, Harel, & Ugurbil, 2008), it is likely that PMC will become crucial for advancement in these endeavors.…”

Cortical feedback signals generalise across different spatial frequencies of feedforward inputs

“…The occlusion paradigm is therefore different to paradigms using 477 Kanizsa figures (e.g. Kok et al, 2016) or neon colour spreading where the non-stimulated region is 478 perceptually filled-in. Our paradigm relates to amodal completion where the subjects do not directly 479 perceive, but rather infer a presence of the continued stimulus behind the occluder, from knowledge about 480 natural objects and scenes.…”