Spatially Dissociated Intracerebral Maps for Face- and House-Selective Activity in the Human Ventral Occipito-Temporal Cortex

Abstract

We report a comprehensive mapping of the human ventral occipito-temporal cortex (VOTC) for selective responses to frequency-tagged faces or landmarks (houses) presented in rapid periodic trains of objects, with intracerebral recordings in a large sample (N = 75). Face-selective contacts are three times more numerous than house-selective contacts and show a larger amplitude, with a right hemisphere advantage for faces. Most importantly, these category-selective contacts are spatially dissociated along the lateral-to-medial VOTC axis, respectively, consistent with neuroimaging evidence. At the minority of “overlap” contacts responding selectively to both faces and houses, response amplitude to the two categories is not correlated, suggesting a contribution of distinct populations of neurons responding selectively to each category. The medio-lateral dissociation also extends into the underexplored anterior temporal lobe (ATL). In this region, a relatively high number of intracerebral recording contacts show category-exclusive responses (i.e., without any response to baseline visual objects) to faces but rarely to houses, in line with the proposed role of this region in processing people-related semantic information. Altogether, these observations shed novel insight on the neural basis of human visual recognition and strengthen the validity of the frequency-tagging approach coupled with intracerebral recordings in epileptic patients to understand human brain function.

Dissociated face- and word-selective intracerebral responses in the human ventral occipito-temporal cortex

“…Across all recorded contacts, contacts showing significant selective responses to both faces and houses were classified as face-house-overlap contacts (irrespective of how they responded to words). Note that a full description of face-house intracerebral responses, as measured with FPVS-SEEG, has been reported elsewhere (Hagen et al, 2020), and that here we use the overlap between faces and houses strictly as a comparison to face-word-overlap.…”

“…Patients were included in the study if they had at least one intracerebral electrode implanted in the VOTC (Figure 1B). The SEEG data for word stimulation from 36 patients were included in Lochy et al (2018), while the data for face stimulation from all patients were included in Hagen et al (2020). All patients gave written consent to participate to the study, which was part of a protocol approved by the Ethics committee of the University Hospital of Nancy.…”

“…Intracerebral EEG was sampled at a 512 Hz with a 256-channel amplifier and referenced to either a midline prefrontal scalp electrode (FPz, in 32 participants) or, when scalp electrodes were not available, an intracerebral contact in the white matter (6 participants). Similar to previous intracranial reports, the data in subsequent analysis were not re-referenced (e.g., Allison, McCarthy, 2002; Hagen et al, 2020; Jonas et al 2016; Kadipasaogly et al 2016; Lochy et al, 2018; Matsuo et al, 2015; Nobre, McCarthy, 1995). However, a separate analysis using a bipolar re-reference yielded the same data pattern.…”

“…In a control condition with houses, participants viewed continuous sequences of natural images of objects presented periodically at 6 Hz through sinusoidal contrast modulation, with randomly selected house images inserted every fifth item, so that the frequency of house presentation was 1.2 Hz (i.e. 6 Hz/5) (see Figure 1 in Hagen et al, 2020). Thus, the procedure was identical to faces with the exception that variable natural house images was interspersed at the fifth cycle rather than images of faces.…”

“…All images were randomly selected from their respective categories. Note that a full report of face-house intracerebral responses, as measured with FPVS-SEEG, have been reported elsewhere (Hagen et al, 2020), and that here we use the overlap between faces and houses strictly as a control comparison to face-word-overlap.…”