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Intracranial electrophysiology of mentalizing

Abstract

Functional magnetic resonance imaging (fMRI) has built the prevailing picture of the social brain. However, fMRI’s hemodynamic basis collapses two dimensions of neural activity that electrophysiology preserves: the millisecond timing of activity and its distribution across the frequency spectrum. This dissertation uses human intracranial electrophysiology (iEEG; N=34) to recover those dimensions for mentalizing – reasoning about mental states – and to reconcile the resulting picture with the fMRI literature it appears at points to contradict. Paper I, using high-frequency broadband (HFB) activity as a proxy for population spiking, shows that the default mode network's apparent simultaneity during mentalizing is in fact a posterior-to-anterior sequence, from visual cortex through temporoparietal DMN to medial prefrontal cortex. Self- and other-mentalizing engage near-identical populations distinguished by the timing – not the magnitude – of their activity, recasting the "other-selective" dmPFC of fMRI as a difference in duration mistaken for a difference in intensity. Paper II decomposes this activity across the full spectrum, revealing a dual-phase architecture shared near-identically by mentalizing and autobiographical memory and jointly distinct from arithmetic. Arithmetic is the spectral outlier: it suppresses HFB in dmPFC while driving sustained theta in the same sites – a signature consistent with frontal-midline theta, the canonical correlate of cognitive control. Because BOLD couples to HFB and is largely blind to low-frequency power, the medial-prefrontal "deactivation" reported during cognitive tasks is the HFB-suppression half of a dissociation whose low-frequency half moves oppositely; the deactivation is faithfully measured but does not amount to disengagement. Paper III uses spectral cross-classification to show that mentalizing recruits autobiographical-like computation along the same hierarchy, graded (Autobiographical > Self ≈ Other > Cognitive) and short of full autobiographical engagement, with self and other differing in timing rather than content. Together, the papers show that what fMRI represents as one activation is a sequence, a spectrum, and a computation – dimensions that, as paper IV argues, source-localized EEG and MEG can recover non-invasively and at scale. Restoring them does not overturn the fMRI view of the social brain; it recovers what the map leaves out and, in one case, reverses the sign of the inference the map supports.