Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing

Abstract

Our understanding of the human default mode network derives primarily from neuroimaging data but its electrophysiological correlates remain largely unexplored. To address this limitation, we recorded intracranially from the human posteromedial cortex (PMC), a core structure of the default mode network, during various conditions of internally directed (e.g., autobiographical memory) as opposed to externally directed focus (e.g., arithmetic calculation). We observed late-onset (>400 ms) increases in broad high γ-power (70-180 Hz) within PMC subregions during memory retrieval. High γ-power was significantly reduced or absent when subjects retrieved self-referential semantic memories or responded to self-judgment statements, respectively. Conversely, a significant deactivation of high γ-power was observed during arithmetic calculation, the duration of which correlated with reaction time at the signal-trial level. Strikingly, at each recording site, the magnitude of activation during episodic autobiographical memory retrieval predicted the degree of suppression during arithmetic calculation. These findings provide important anatomical and temporal details-at the neural population level-of PMC engagement during autobiographical memory retrieval and address how the same populations are actively suppressed during tasks, such as numerical processing, which require externally directed attention.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Anatomy of the PMC. (A) PMC (highlighted region in purple), which forms a core node of the default mode network, is located on the medial surface of the brain. (B) The PMC is bounded ventrally by the parieto-occipital sulcus (which divides it from the cuneus); dorsally by the cingulate sulcus (cgs) and its marginal branch (mb); and extends anteriorly to approximately mid-cingulate level before it joins the anterior cingulate cortex. The PMC contains the PCC (areas 23a, 23b, and 23c), RSC (areas 29 and 30), medial parietal cortex (area 7m), and a transitional cortical area 31. The RSC is superficially visible as gyral cortex around areas 29 and 30; however, it extends perisplenially around the corpus callosum (cc) hidden within the callosal sulcus (cs; B and C).

Fig. 2.

Response magnitude across conditions. (A) Electrode locations from all subjects on a standardized Montreal Neurological Institute brain, with the PMC marked in purple. PMC electrodes responsive to the self-episodic condition have red fill and other PMC sites have black fill. Electrodes falling outside the anatomical boundaries of the PMC are filled in white. (B) Mean HG response across conditions for all electrodes that were identified as significantly responsive during the self-episodic condition (11, marked red in A). Mean HG response for these electrodes was significantly different across conditions [one-way ANOVA; F(4,40) = 17.43, P < 0.001], with post hoc test showing self-episodic, self-semantic, and math to be significantly different from all other conditions (**P < 0.01, corrected). Scatter correlation plots of mean HG response for all PMC electrodes (n = 33, marked black in A) comparing the self-episodic condition with self-semantic (C), self-judgment (D), rest (E), and math (F) conditions, respectively.

Fig. 3.

Response magnitude to the self-episodic condition predicts trial-by-trial suppression during math condition. (A) Scatter correlation plot of HG response magnitude to the self-episodic condition with correlation value between trial-based HG math suppression and math RT (Fisher z) for all PMC channels. Those electrodes that showed higher magnitude responses to the self-episodic condition (x axis) also showed the strongest correlation between HG math suppression and RT (y axis). (B) For example, electrodes with strong HG response magnitudes to the self-episodic conditions also showed strong suppression of HG magnitude during the math condition (as noted above in Fig. 2). Additionally, these channels also displayed a stronger trial-by-trial–based correlation of suppression duration and trial duration (RT) for the math condition (C). (D and E) Consequently, those sites with lower response magnitudes during the self-episodic condition showed much weaker (nonsignificant) suppression duration vs. RT correlation for the math condition.

Fig. 4.

HG response latency to self-episodic condition across the PMC. (A) HG onset (Left, relative to stimulus onset; Stim) and offset (Right, relative to response; Resp) latency for the self-episodic condition sorted in ascending order and colored relative to ventral or dorsal location indicated in C for all responsive electrodes (n = 11). (B) Mean duration of HG response (above threshold) for self-episodic condition for ventral and dorsal electrodes (n.s., no significant difference). (C) Schematic of the PMC and the ventral/dorsal division used for electrode classification. Latencies show a trend for greater delays in response for dorsal sites compared with more ventral sites. Scatter correlation of HG onset (D) and offset (E) with RT, shown for all PMC electrodes (n = 33). As there was no significant correlation with onset/offset and RT, the differences in latencies shown in A are more likely related to anatomical differences rather than consistent behavioral differences between ventral and dorsal groups.