TMS reveals inhibitory extrastriate cortico-cortical feedback modulation of V1 activity in humans

Abstract

The interaction between the primary visual cortex (V1) and extrastriate visual areas provides the first building blocks in our perception of the world. V2, in particular, seems to play a crucial role in shaping contextual modulation information through feedback projections to V1. However, whether this feedback is inhibitory or excitatory is still unclear. In order to test the nature of V2 feedback to V1, we used neuronavigation-guided offline inhibitory transcranial magnetic stimulation (TMS) on V2 before testing participants on collinear facilitation, a contrast detection task with lateral masking. This contextual modulation task is thought to rely on horizontal connections in V1 and possibly extrastriate feedback. Results showed that when inhibitory TMS was delivered over V2, contrast thresholds decreased for targets presented in the contralateral hemifield, consistent with the retinotopic mapping of this area, while having no effect for targets presented in the ipsilateral hemifield or after control (CZ) stimulation. These results suggest that feedback from V2 to V1 during contextual modulation is mostly inhibitory, corroborating recent observations in monkey electrophysiology and extending this mechanism to human visual system. Moreover, we provide for the first time direct evidence of the involvement of extrastriate visual areas in collinear facilitation.Electronic supplementary materialThe online version of this article (10.1007/s00429-019-01964-z) contains supplementary material, which is available to authorized users.

Characterization of Feedback Neurons in the High-Level Visual Cortical Areas That Project Directly to the Primary Visual Cortex in the Cat

“…However, results reported by different research groups are diverse or even opposite. For example, some authors find out that top-down influence can facilitate the responses of V1 neurons and thus enhance their orientation or direction selectivity (Wang et al, 2000 , 2007 , 2010 ; Galuske et al, 2002 ; Huang et al, 2007 ; Tong et al, 2011 ; Moldakarimov et al, 2014 ; Zhang et al, 2014 ; Nurminen et al, 2018 ; Keller et al, 2020 ), whereas others report that top-down influence is suppressive and lowers neuronal response in the low-level visual cortex (Murray et al, 2002 ; Alink et al, 2010 ; Nassi et al, 2013 ; Klein et al, 2014 ; Hishida et al, 2019 ; Maniglia et al, 2019 ; Ranson et al, 2019 ). A critical way to reconcile these contradictions is to determine the cell type of feedback neurons as well as the neurotransmitter system used by the feedback circuitry.…”

“…However, the characteristics of feedback influence on the responses of V1 neurons remains in debate (Han and VanRullen, 2016 ). Some authors propose that top-down influence produces excitatory feedback inputs and facilitate neuronal response in the V1 area (Wang et al, 2000 , 2007 , 2010 ; Huang et al, 2004 ; Liang et al, 2007 ; Tong et al, 2011 ; Chen et al, 2014 ; Zhang et al, 2014 ; van Loon et al, 2015 ; Kok et al, 2016 ; Pafundo et al, 2016 ; Yang X. et al, 2016 ; Baumgartner et al, 2018 ; Huh et al, 2018 ), whereas others suggest that top-down influence exert suppressive impacts on neurons in the low-level visual areas (Roland et al, 2006 ; Chalk et al, 2010 ; Nassi et al, 2013 , 2014 ; Klein et al, 2014 ; Hishida et al, 2019 ; Maniglia et al, 2019 ). Still, others report bidirectional top-down effects of both suppression and enhancement (Gazzaley et al, 2005 ; Johnson and Johnson, 2009 ; Cox et al, 2019 ).…”

Anodal Occipital Transcranial Direct Current Stimulation Enhances Perceived Visual Size Illusions

“…For the Ponzo illusion, feedback projections from higher visual areas to V1 have been suggested (Zeng et al, 2020;He et al, 2015;Fang et al, 2008). These feedback connections have been found to boost the response of V1 neurons to a central stimulus and meanwhile suppress the response to its surrounding context (Maniglia, Trotter, & Aedo-Jury, 2019;Vangeneugden et al, 2019;Nurminen, Merlin, Bijanzadeh, Federer, & Angelucci, 2018;Chen et al, 2014;Nassi, Lomber, & Born, 2013;Wang, Huang, Bardy, FitzGibbon, & Dreher, 2010;Bardy, Huang, Wang, FitzGibbon, & Dreher, 2009;Hupé et al, 1998Hupé et al, , 2001). In the current study, anodal stimulation significantly increased the magnitude of both the Ponzo illusion and the Ebbinghaus illusion, which was dichoptic presented, suggesting that anodal stimulation primarily influences the feedback projections from higher to lower visual areas.…”

Repetitive Transcranial Magnetic Stimulation for Dysesthesia Caused by Subacute Myelo-Optico-Neuropathy: A Case Report

“…Repetitive transcranial magnetic stimulation (rTMS) is a variant of noninvasive neuromodulation, after which persistent plastic changes are believed to be induced [4, 5]. For administering TMS, the magnetic pulses from the coil travel through the skull toward the cortical area, resulting in brain network modulation.…”