Direct cortical stimulation of human posteromedial cortex

Abstract

Background: The posteromedial cortex (PMC) is a collective term for an anatomically heterogeneous area of the brain constituting a core node of the human default mode network (DMN), which is engaged during internally focused subjective cognition such as autobiographical memory.

Methods: We explored the effects of causal perturbations of PMC with direct electric brain stimulation (EBS) during presurgical epilepsy monitoring with intracranial EEG electrodes.

Results: Data were collected from 885 stimulations in 25 patients implanted with intracranial electrodes across the PMC. While EBS of regions immediately dorsal or ventral to the PMC reliably produced somatomotor or visual effects, respectively, we found no observable behavioral or subjectively reported effects when sites within the boundaries of PMC were electrically perturbed. In each patient, null effects of PMC stimulation were observed for sites in which intracranial recordings had clearly demonstrated electrophysiologic responses during autobiographical recall.

Conclusions: Direct electric modulation of the human PMC produced null effects when standard functional mapping methods were used. More sophisticated stimulation paradigms (e.g., EBS during experimental cognitive tests) will be required for testing the causal contribution of PMC to human cognition and subjective experience. Nonetheless, our findings suggest that some extant theories of PMC and DMN contribution to human awareness and subjective conscious states require cautious re-examination.

© 2017 American Academy of Neurology.

Figures

Figure 1. PMC and EBS sites

(A) Schematic of anatomic regions of interest is shown. Posteromedial cortex (PMC; purple) reflects posterior medial parietal cortex, which is ventral to the marginal branch of the cingulate sulcus (mbCgS) and dorsal to the parieto-occipital sulcus (PoS; calcarine sulcus [CS] also shown). PMC is therefore intermediate between dorsal (red) medial motor/somatomotor cortex and ventral medial occipital cortex (green). For electric brain stimulation (EBS), bipolar pairs of neighboring electrodes are used, and EBS can therefore occur within an anatomic region of interest (1–3) or at/across the boundary of anatomic regions (4). (B) Visualization of all electrode sites used for EBS on a normalized cortical surface (Montreal Neurological Institute; left hemisphere). All right hemisphere sites have been reflected onto the left hemisphere. Colors of electrodes are based on the native anatomic location within participants, making direct anatomic mapping to the normalized surface imprecise. CC = corpus callosum.

Figure 2. Count data for regional effects of EBS

(A) Bar plot shows count data for entire dataset, depicting the rate of observed (positive) and null (negative) stimulations. (B) Bar plot shows count data (all regions) for all effective stimulations across the 5 categories of classification. (C–E) Bar plots show the effects of stimulation for the dorsal (C), posteromedial cortex (PMC; D), and ventral (E) regions of interest. Stimulation in dorsal regions produces the bulk of motor/somatomotor effects, whereas stimulation of ventral regions produces the majority of visual effects. PMC shows minimal stimulation effects; however, all of these observations come from stimulations performed on boundary stimulation pairs, which will jointly engage either dorsal or ventral regions. When these confounded pairs are excluded, no positive effects remain for PMC. EBS = electric brain stimulation.

Figure 3. PMC null EBS effects observed at task positive sites

(A) Stimulation effects are shown for an example participant (P6), with a linear continuous electrocorticography (ECoG) array spanning all anatomic regions of interest. Within this participant, subsequent stimulation across the array shows that ventral stimulations produce reliable visual effects (e.g., “I see a bunch of waves,” right lower visual field) followed by no effects on stimulation of the posteromedial cortex (PMC) and then the observation of motor effects (e.g., “Right leg jerk”) with the transition to dorsal regions. The transition of effects closely matches our anatomic boundaries (marginal branch of the cingulate sulcus [mbCgS] and parieto-occipital sulcus [PoS]) and helps to highlight the influence of boundary pair stimulations on observed/reported effects. While the PMC sites display no effects, it is not because this region is pathologic or otherwise nonfunctional. (B) Time-frequency plots are shown for 3 PMC electrodes from panel A (1–3). Each spectrogram displays characteristic properties of ECoG response such as high-frequency power increase and concomitant low-frequency suppression. These responses are during task conditions of autobiographical retrieval in which the participant must respond if an autobiographical statement is true or false (e.g., “I ate fruit this morning”). This spectral response is selective to episodic retrieval conditions and has a replicable late onset, consistent with the time course of retrieval search. These data have previously been published and replicated elsewhere., CS = calcarine sulcus; EBS = electric brain stimulation.