Multi-modal Mapping of the Face Selective Ventral Temporal Cortex–A Group Study With Clinical Implications for ECS, ECoG, and fMRI

Abstract

Face recognition is impaired in patients with prosopagnosia, which may occur as a side effect of neurosurgical procedures. Face selective regions on the ventral temporal cortex have been localized with electrical cortical stimulation (ECS), electrocorticography (ECoG), and functional magnetic resonance imagining (fMRI). This is the first group study using within-patient comparisons to validate face selective regions mapping, utilizing the aforementioned modalities. Five patients underwent surgical treatment of intractable epilepsy and joined the study. Subdural grid electrodes were implanted on their ventral temporal cortices to localize seizure foci and face selective regions as part of the functional mapping protocol. Face selective regions were identified in all patients with fMRI, four patients with ECoG, and two patients with ECS. From 177 tested electrode locations in the region of interest (ROI), which is defined by the fusiform gyrus and the inferior temporal gyrus, 54 face locations were identified by at least one modality in all patients. fMRI mapping showed the highest detection rate, revealing 70.4% for face selective locations, whereas ECoG and ECS identified 64.8 and 31.5%, respectively. Thus, 28 face locations were co-localized by at least two modalities, with detection rates of 89.3% for fMRI, 85.7% for ECoG and 53.6 % for ECS. All five patients had no face recognition deficits after surgery, even though five of the face selective locations, one obtained by ECoG and the other four by fMRI, were within 10 mm to the resected volumes. Moreover, fMRI included a quite large volume artifact on the ventral temporal cortex in the ROI from the anatomical structures of the temporal base. In conclusion, ECS was not sensitive in several patients, whereas ECoG and fMRI even showed activation within 10 mm to the resected volumes. Considering the potential signal drop-out in fMRI makes ECoG the most reliable tool to identify face selective locations in this study. A multimodal approach can improve the specificity of ECoG and fMRI, while simultaneously minimizing the number of required ECS sessions. Hence, all modalities should be considered in a clinical mapping protocol entailing combined results of co-localized face selective locations.

Intracerebral electrical stimulation to understand the neural basis of human face identity recognition

“…Stimulating the posterior face-selective regions with SEEG (IOG and LatMidFG) often evoked perceptual changes (facial elements in disarray, seeing the different faces as being the same, facial palinopsia, Table 1). This observation is in agreement with ECOG DES studies consistently reporting facial perceptual changes (usually a perceptual distortion) when stimulating the right LatMidFG (Parvizi et al, 2012;Rangaranjan et al, 2014;Schalk et al, 2017;Schrouff et al, 2020;Sanada et al, 2021; see also Mundel et al, 2003). In contrast, as noted above, DES inside the right AntFG did not evoke perceptual effects (case 3, CD, Table 1).…”

“…First, with the exception of early studies (Allison et al, 1994 andPuce et al, 1999) and the case reported by Parvizi et al, (2012) who was not impaired at naming famous face pictures, ECOG DES studies with face stimuli essentially required subjects to passively look at faces (Mundel et al, 2003;Rangarajan et al, 2014;Rangarajan & Parvizi, 2016;Sanada et al, 2021;Schalk et al, 2017;Schrouff et al, 2020) or to perform face detection tasks (Chong et al, 2013;Keller et al, 2017), without specifically testing for FIR impairment.…”

“…Given the high and consistent face‐selective responses found in the right LatMidFG, that is, the FFA, it is not surprising that this region has been the focus of most ECOG DES studies investigating the processing of faces (Mundel et al., 2003; Parvizi et al., 2012; Rangaranjan et al., 2014; Sanada et al., 2021; Schalk et al., 2017; Schrouff et al., 2020). While SEEG studies performed in large populations of subjects have also identified the largest face‐selective neural responses in this region (Hagen et al., 2020; Jonas et al., 2016), only one case of intracerebral stimulation has been reported so far: subject MB who, during stimulation inside the right LatMidFG (Figure 3a, Table 1) experienced facial palinopsia , that is, hallucinations of facial elements appropriately incorporated in the face identity in front of her (Video 2) (Jonas et al., 2018).…”

“…In the early ECOG studies focusing on intracranial potentials in response to face stimuli (e.g., N200), facial hallucinations and transient disruption of famous face naming were noted in several individuals following DES to various VOTC sites (Allison et al., 1994; Puce et al., 1999). More recently, ECOG studies focusing on DES (of the LatMidFG) have reported face‐related perceptual changes (i.e., changes in the phenomenological experience of the face stimulus, usually a distortion of the experimenter's face in front of the subject or a presented picture; Parvizi et al., 2012; Rangaranjan et al., 2014; Schalk et al., 2017; Schrouff et al., 2020; Sanada et al., 2021; see also Mundel et al., 2003). However, there was no FIR impairment during DES at a face naming task in the case study reported by Parvizi and colleagues (2012) and, to our knowledge, none of the other recent studies evaluated FIR.…”

“…From the point of view of fundamental research, each technique has its own advantages: while ECOG offers a more extensive spatial coverage, more homogenous across individual brains, SEEG provides recordings directly inside the grey matter, allowing the specific exploration of cortical sulci and medial temporal lobe structures (e.g., amygdala, hippocampus). These respective advantages of ECOG and SEEG apply to electrophysiological recordings (Rossion et al, 2018;George et al, 2020), but also to DES: while the wider coverage of ECOG electrodes allows more common sites to be stimulated across individuals and may even promote (small) group studies (e.g., Sanada et al, 2021;Schrouff et al, 2020), the electrodes are not inserted inside the cerebral matter, preventing to stimulate cortical sulci and medial temporal lobe structures, but also requiring higher current intensity to elicit potentially less specific behavioural effects than with depth electrodes (SEEG).…”