The inferior occipital gyrus is a major cortical source of the face‐evoked N170: Evidence from simultaneous scalp and intracerebral human recordings

Abstract

The sudden onset of a face image leads to a prominent face-selective response in human scalp electroencephalographic (EEG) recordings, peaking 170 ms after stimulus onset at occipitotemporal (OT) scalp sites: the N170 (or M170 in magnetoencephalography). According to a widely held view, the main cortical source of the N170 lies in the fusiform gyrus (FG), whereas the posteriorly located inferior occipital gyrus (IOG) would rather generate earlier face-selective responses. Here, we report neural responses to upright and inverted faces recorded in a unique patient using multicontact intracerebral electrodes implanted in the right IOG and in the OT sulcus above the right lateral FG (LFG). Simultaneous EEG recordings on the scalp identified the N170 over the right OT scalp region. The latency and amplitude of this scalp N170 were correlated at the single-trial level with the N170 recorded in the lateral IOG, close to the scalp lateral occipital surface. In addition, a positive component maximal around the latency of the N170 (a P170) was prominent above the internal LFG, whereas this region typically generates an N170 (or "N200") over its external/ventral surface. This suggests that electrophysiological responses in the LFG manifest as an equivalent dipole oriented mostly along the vertical axis with likely minimal projection to the lateral OT scalp region. Altogether, these observations provide evidence that the IOG is a major cortical generator of the face-selective scalp N170, qualifying the potential contribution of the FG and questioning a strict serial spatiotemporal organization of the human cortical face network.

Memory influences visual cognition across multiple functional states of interactive cortical dynamics

“…Neural processes underlying VPP/N170 have been implicated in learning and representing knowledge for expert object categorization (Curran, Tanaka, & Weiskopf, 2002;Rossion, Curran, & Gauthier, 2002;Rossion, Kung, & Tarr, 2004;Scott, Tanaka, Sheinberg, & Curran, 2006; J. W. Tanaka & Curran, 2001). Convergent evidence localizes the brain sources to occipitotemporal cortex for objects and to face-specific areas in posterior fusiform gyrus, inferior occipital gyrus, and superior temporal sulcus for faces (Bötzel, Schulze, & Stodieck, 1995;Corrigan et al, 2009;Horovitz, Rossion, Skudlarski, & Gore, 2004;Itier & Taylor, 2004c;Jacques et al, 2019;Miki, Watanabe, Kakigi, & Puce, 2004;Puce et al, 1999;Rossion et al, 1999;Schendan et al, 1998;Schweinberger, Pickering, Jentzsch, Burton, & Kaufmann, 2002;Watanabe, Kakigi, & Puce, 2003). Computational modelling indicates that feedforward processing from V1 to higher areas along the ventral visual pathway explains the category-specificity of the VPP/N170 (David et al, 2006).…”

Fast periodic visual stimulation to highlight the relationship between human intracerebral recordings and scalp electroencephalography

“…The epileptic patient, as well as the recording settings, are identical to those reported in Jacques et al (). The patient has also been described in Jonas et al ().…”

“…The few studies which investigated the relationship between simultaneously recorded scalp EEG and SEEG signals relied on event‐related potential (ERP) approaches, in which brain activity is recorded to the sudden occurrence of an event (external or internal such as epileptic spikes) and then averaged in the time domain (Dubarry et al, ; Jacques et al, ; Koessler et al, ; Merlet et al, ; Rosburg et al, ). At least two main factors make it difficult to perform these studies and therefore seriously limit their availability.…”

Event-related network changes unfold the dynamics of cortical integration during face processing

“…Several models of the face-processing network posit that its core regions are the inferior occipital gyrus, the fusiform gyrus and the superior temporal sulcus (Haxby & Gobbini, 2012;Haxby et al, 2000;Ishai, 2008;Rossion et al, 2003), which are regions dedicated to the analysis of the visual features that define a face as an holistic percept (Haxby & Gobbini, 2012). Furthermore, these regions have been consistently found as the source of the N170 potential observed with EEG (Eimer, 2012;Jacques et al, 2019;Tadel et al, 2019). The present results bolster the claim for a distributed processing mechanism for faces (Haxby & Gobbini, 2012) that is centered around these regions, providing a quantitative measure of their involvement within the whole brain network.…”

“…Rather it results from the disruption of this segregation, which allows the emergence of a collective activity within the nodes comprising the network (Behrmann & Plaut, 2013). These need to be arranged in a small-world topology that maximizes the information exchange (Bassett & Bullmore, 2006;Telesford et al, 2011), with few highly connected hubs, likely corresponding to the core part of the face-perception network (Ishai, 2008;Jacques et al, 2019), whose influence dynamically increases as the computation progress.…”