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W4313154170 abstract "Article Figures and data Abstract Editor's evaluation Introduction Results Discussion Methods Data availability References Decision letter Author response Article and author information Metrics Abstract Posterior cingulate cortex (PCC) is an enigmatic region implicated in psychiatric and neurological disease, yet its role in cognition remains unclear. Human studies link PCC to episodic memory and default mode network (DMN), while findings from the non-human primate emphasize executive processes more associated with the cognitive control network (CCN) in humans. We hypothesized this difference reflects an important functional division between dorsal (executive) and ventral (episodic) PCC. To test this, we utilized human intracranial recordings of population and single unit activity targeting dorsal PCC during an alternated executive/episodic processing task. Dorsal PCC population responses were significantly enhanced for executive, compared to episodic, task conditions, consistent with the CCN. Single unit recordings, however, revealed four distinct functional types with unique executive (CCN) or episodic (DMN) response profiles. Our findings provide critical electrophysiological data from human PCC, bridging incongruent views within and across species, furthering our understanding of PCC function. Editor's evaluation This is an exciting manuscript that provides fundamental new insights into one of the most enigmatic brain regions; the posterior cingulate cortex. Using electrophysiological recordings from dorsal and ventral PCC subregions, the authors provide compelling evidence for a dorsal-executive and ventral-episodic functional subdivision. This paper will be of high interest to a broad range of neuroscientists. https://doi.org/10.7554/eLife.80722.sa0 Decision letter Reviews on Sciety eLife's review process Introduction Despite being routinely observed in studies of human brain function, the posterior cingulate cortex (PCC) remains one of the least understood neocortical areas, with little consensus as to its role in cognition (Leech and Sharp, 2014; Leech and Smallwood, 2019). Anatomically, PCC reflects the caudal aspect of the cingulate cortex, wrapping around the posterior trunk and splenium of the corpus callosum (Vogt et al., 1995; Vogt et al., 2001; Margulies et al., 2009; Figure 1B). Physiologically, PCC displays high basal levels of metabolic activity (Raichle et al., 2001; Buckner et al., 2008). Clinically, a growing literature suggests PCC is implicated in the progression of neurodegenerative and psychiatric disease (Leech and Sharp, 2014; Vogt, 2019). However, the deep medial location and rich vascularization of PCC (Bernier et al., 2018) limit the occurrence of focal insult and corresponding neuropsychological findings, often foundational to understanding many other brain regions (Vaidya et al., 2019). Figure 1 Download asset Open asset Intracranial recordings sites, PCC anatomy, task design, and predicted neural responses. (A) Anatomical locations, normalized to MNI space, of intracranial sEEG depth electrodes targeting the posterior aspect of the cingulate cortex, with the distal contact of probes containing microwires indicated in green. (B) Anatomy of human PCC, differentiating dorsal (dPCC) and ventral (vPCC) subregions and demarcating regional sulci following the most recent definitions in PCC (Petrides, 2018; Willbrand et al., 2022). (C) Attention/Memory Switch task procedure and example stimuli. The task included two executive attention conditions: search and add, two episodic memory conditions: past and future, and a rest condition. Each trial was proceeded by a cue indicating the forthcoming task condition and was followed by a trial response period, excluding rest (see Methods). (D) Schematic of the putative neural response profiles to the task conditions for episodic/DMN (default mode network) selectivity vs. executive/CCN (cognitive control network) selectivity. At present, theorizing on the function of human PCC is typically limited to its role as a core node of the default mode network (DMN) (Raichle et al., 2001; Fox et al., 2005; Fransson, 2005; Fransson and Marrelec, 2008; Buckner and DiNicola, 2019). Whereby, a large functional neuroimaging literature shows that PCC, as part of the DMN, displays high basal levels of activity that are reduced during a variety of tasks, especially those requiring focused attention and cognitive control (Shulman et al., 1997; Raichle et al., 2001; Harrison et al., 2008; Anticevic et al., 2012). Consequently, the DMN is often reported as being anti-correlated or oppositional to other brain systems, such as the dorsal attention or cognitive control networks (DAN; CCN) that are engaged during attention demanding tasks (Fox et al., 2005; Fransson, 2005; Uddin et al., 2009). These findings led to the DMN, and in turn PCC, to be termed ‘task-negative’, as opposed to ‘task-positive’ regions (Fox et al., 2005; Uddin et al., 2019). However, hemodynamic activity in PCC is not decreased in all tasks (Spreng, 2012). In particular, it increases during episodic memory retrieval (Shannon and Buckner, 2004; Wagner et al., 2005; Vincent et al., 2006) and other internally focused cognitive tasks associated with self-referential thought and envisioning past or future scenarios (Svoboda et al., 2006; Hassabis and Maguire, 2007; Harrison et al., 2008; Spreng et al., 2009; Buckner and DiNicola, 2019). These findings highlight an alternate dichotomy where PCC/DMN function is associated with ‘internally’, versus ‘externally’, focused cognition (Buckner and Carroll, 2007; Andrews-Hanna et al., 2014). Supporting these neuroimaging findings, human intracranial recordings of PCC and surrounding posteromedial cortex (PMC) suggest clear electrophysiological evidence of activity suppression during external attention (Miller et al., 2009; Dastjerdi et al., 2011; Ossandón et al., 2011; Foster et al., 2012; Foster et al., 2015) and activity enhancement during cued episodic thought (Foster et al., 2012; Foster et al., 2015; Fox et al., 2018). In contrast, electrophysiological studies in the non-human primate have focused on the contributions of PCC to cognitive control (Hayden et al., 2010), decision making (McCoy et al., 2003; McCoy and Platt, 2005; Pearson et al., 2009), and value judgement (Hayden et al., 2008; Heilbronner et al., 2011) – conditions thought to anti-correlate with PCC engagement in humans. Together, single unit recordings in the macaque PCC during economic decisions have led to a hypothesized role in strategy selection (Pearson et al., 2009; Pearson et al., 2011; Heilbronner and Platt, 2013), further emphasizing a much more executive function, in apparent contrast to the common focus of human data. However, studies of human decision making and value judgements consistently observe PCC engagement (Bartra et al., 2013; Clithero and Rangel, 2014; Oldham et al., 2018), yet such findings have received limited attention (compared to anterior cingulate cortex) and therefore limited integration with studies of the DMN (Acikalin et al., 2017). We hypothesized that these apparently contradictory findings reflect, in part, a failure to appreciate the specific anatomical organization of PCC. Contemporary studies of human brain network organization suggest that PCC contains putative subregions associated with multiple distinct functional systems (Andrews-Hanna et al., 2010; Yeo et al., 2011; Leech et al., 2012; Bzdok et al., 2015; Glasser et al., 2016; Braga and Buckner, 2017; Gordon et al., 2017b). For example, functional connectivity patterns are consistent with estimated structural connectivity, with prefrontal cingulum tracts entering primarily via the dorsal aspect of PCC, whereas medial temporal lobe tracts enter via its ventral aspect (Greicius et al., 2009). Evidence for PCC subregional organization also derives from homologous cytoarchitectural and connectivity data in humans and non-human primates (Vogt et al., 1995; Vogt et al., 2001; Vogt and Laureys, 2005; Parvizi et al., 2006; Vogt et al., 2006; Margulies et al., 2009). Together, these data convey a dissociation of the dorsal and ventral PCC (Figure 1B). Such a division suggests that dorsal PCC (dPCC) may be associated with executive control systems of the frontal lobe and ventral PCC (vPCC) may be associated with episodic memory systems of the medial-temporal lobe (Vincent et al., 2008; Spreng et al., 2010; Leech et al., 2011). This subregional perspective better reconciles functional views of PCC across species, as studies in the non-human primate have exclusively focused on the dPCC (often termed area CGp; McCoy et al., 2003). As noted above, extant data from humans suggests executive attention demanding tasks typically suppress electrophysiological activity within human PCC, consistent with DMN function (Buckner and DiNicola, 2019). In contrast, electrophysiological evidence of PCC engagement during executive tasks, consistent with CCN function, is more limited (Daitch and Parvizi, 2018). Based on human neuroimaging and non-human primate electrophysiology, we hypothesized that subregions of PCC, specifically within its dorsal aspect, should be engaged during executive attention demanding tasks more than memory demanding tasks. Whereby, dPCC should reflect an electrophysiological response profile more consistent with the CCN rather than the DMN (Figure 1D). To test this, we leveraged human intracranial electrophysiology via local field potential (LFP) and single neuron recordings targeting dPCC to capture neural activity during randomly alternating executive attention and episodic memory demanding tasks. We observed that neural populations within dPCC, as captured by the LFP, showed significantly greater responses (in broadband gamma, BBG; 70–150 Hz) during executive compared to episodic conditions. Strikingly, functional clustering of single unit activity revealed multiple functional cell types within dPCC. A majority of single units responded selectively to only one of the two executive attention tasks (visual search or arithmetic), suggesting distinct populations underlie the observed CCN-like LFP response. However, a third functional cell type showed clear selectivity to both episodic memory conditions (past and future event scenarios) as well as suppression to both executive task conditions, highly consistent with DMN function. A final functional cell type displayed increased firing during cued rest periods, also a feature of the DMN. Together, these data provide clear electrophysiological evidence for executive processing within dPCC, consistent with the non-human primate, but also suggest a rich functional organization at the single unit level. These findings are discussed within the context of a growing literature examining the varied functional organization of associative cortices, like PCC, via precision neuroimaging. Careful consideration of this rich functional organization will be critical for better understanding the role of PCC in cognition and disease. Results Intracranial PCC recordings during an attention/memory switch task Electrophysiological activity in PCC was recorded by stereo-electroencephalography (sEEG) depth electrodes in 20 subjects undergoing invasive monitoring for epilepsy (female = 8; male = 12; see Methods). Across subjects, 35 electrodes were localized to the PCC region, 29 within dPCC and 6 within vPCC (Figure 1A and B). As the focus of this study, subsequent analyses concentrated on dPCC recording sites. Subjects performed an attention/memory switch task consisting of randomly alternating trials of executive attention conditions (search or add) and episodic construction conditions (past or future), engaging executive and episodic processes respectively (Figure 1C; see Methods). These conditions reflect tasks well known to differentially drive both CCN and DMN systems (Figure 1D) as observed via human neuroimaging and intracranial electrophysiology (Jerbi et al., 2010; Ossandón et al., 2011; Foster et al., 2012; Ossandón et al., 2012; Foster et al., 2015; Daitch and Parvizi, 2018; Fox et al., 2018). Task performance showed high accuracy for the executive conditions (mean accuracy: 86.47% for search; 92.59% for add) and robust vividness scores for the cued episodic conditions (modal vividness response: ‘strong’ for past; ‘strong’ for future). Task selectivity of LFP in dorsal PCC For macro-electrode sEEG recordings, activation of local neural populations can be captured by amplitude changes in the broadband gamma (BBG) frequency range (70–150 Hz) of the recorded local field potential (LFP) (Ray and Maunsell, 2011; Bartoli et al., 2019). BBG activity is strongly correlated with both blood-oxygen-level-dependent (BOLD) fMRI and population firing rate, making it a useful marker for reconciling human neuroimaging and non-human primate electrophysiology findings (Miller, 2010). We found that dPCC displayed increased activity specifically within the BBG range during the cue and early task execution of the executive attention conditions, search and add. An example dPCC recording site and time-frequency response is shown in Figure 2A and B. Group data (nprobes = 29, nsubjects = 19) shows BBG activation within dPCC to be transient and peaked following the onset of search and add tasks (Figure 2C). During early task execution, from task onset to 1000 ms (1000–2000 ms post-cue), group mean BBG amplitude was greatest for the search condition, followed by the add condition, with low mean responses for past, future, and rest conditions. A mixed-effects model with task as a fixed effect and subject/electrode as random effects, revealed a significant main effect of task on BBG amplitude for the same task window. Specifically, mean BBG amplitude was significantly higher for the search task compared to add, past, future, and rest conditions (search-add: t(5093)=3.859, p=0.0011; search-past: t(5093)=8.092, p<0.0001; search-future: t(5093)=8.573, p<0.0001; search-rest: t(5093)=8.706, p<0.0001), and furthermore, was significantly higher for the add task compared to past, future, and rest conditions (add-past: t(5093)=4.236, p=0.0002; add-future: t(5093)=4.717, p<0.0001; add-rest: t(5093)=4.847, p<0.0001). These data provide clear support for an executive functional response profile within dPCC, which is highly consistent with the CCN and oppositional to that predicted for the DMN (Figure 1D). In contrast, sites within vPCC (nprobes = 6) showed the converse BBG response profile across conditions, consistent with the DMN and prior observations (Dastjerdi et al., 2011; Foster et al., 2012; Foster et al., 2015), where BBG responses were greater during late task execution (2000–3000 ms after task onset) for the episodic task conditions (see Figure 2—figure supplement 1). A mixed effects model revealed a significant main effect of condition on BBG amplitude, with vPCC mean BBG amplitude being significantly higher for past than all other conditions (past-add: t(1253)=8.841, p<0.0001; past-search: t(1253)=5.151, p<0.0001; past-rest: t(1253)=3.978, p=0.0007; past-future: t(1253)=3.020, p=0.0216), and significantly lower for add than all other conditions (add-past: t(1253)=–8.841, p<0.0001; add-future: t(1253)=–5.811, p<0.0001; add-rest: t(1253)=–4.863, p<0.0001; add-search: t(1253)=–3.690, p=0.0022). Figure 2 with 1 supplement see all Download asset Open asset Executive condition selectivity of LFP BBG task responses in dPCC. (A) Location of a representative dPCC electrode in subject N9. (B) Time-frequency spectrogram for electrode in (A) depicting amplitude (% change) dynamics over time for each task condition. Amplitude in the BBG frequency range is increased during the cue and early task performance of attention conditions (search/add). (C) Group mean (nprobes = 29, nsubjects = 19) BBG amplitude (with s.e.m. shading) over time, aligned to trial onset, across conditions for all dPCC electrodes. Black vertical lines indicate time of cue and task onset. (D) Group mean BBG amplitude (with s.e.m.) during early task execution (task onset to 1000 ms) across conditions for all dPCC electrodes. Together, these data show increased activity of dPCC populations during early task execution of executive attention conditions, consistent with the CCN. See Figure 2—figure supplement 1 for vPCC data. Anatomical organization of PCC activity To examine the distribution of responses across PCC recording sites, all electrode locations were normalized to MNI space and depicted with their respective mean BBG amplitude for early and late time periods of task execution for the combined executive (search/add) and episodic (past/future) conditions (Figure 3; See Methods). As shown in Figure 3A, executive activity during an early time window (task onset to 1 s) was maximal for sites closer to the callosal sulcus within dPCC (i.e. inferior aspect of dPCC). When considering a later time period of task execution, 2–3 s after task onset, population selectivity appeared to follow a more dorsal/ventral gradient with executive activity more dorsal and mnemonic activity more ventral within PCC (Figure 3C/D). While PCC is often viewed as synonymous with DMN function, human neuroimaging often reports on executive control tasks engaging dPCC (Leech et al., 2011). Indeed, meta-analytic association of neuroimaging studies for the term ‘cognitive control’ identifies commonly reported activations within the inferior aspect of dPCC (Neurosynth association test; n studies = 598). The centroid of this cluster (threshold z>4) is shown in Figure 3 (green hexagon), proximal to many recording sites. Figure 3 Download asset Open asset Spatial clustering of LFP BBG responses across PCC. Mean LFP BBG response for each macro-electrode site within PCC averaged for the executive (search/add) (A/B) and episodic (past/future) (C/D) task conditions during early (task onset to 1000 ms; left) and late (2000–3000 ms into task; right) task execution. Electrode coordinates are shown in MNI voxel space, collapsed for the x-dimension (i.e. collapsed for left/right hemispheres). Green symbol indicates the centroid maxima of the association map for search term ‘cognitive control’ at z>4.0 from Neurosynth meta-analysis. BBG responses predominate for the executive task conditions during the early task window, specifically for electrodes more proximal to the callosal sulcus. However, BBG responses to the episodic task conditions emerge during the late task window, specifically for more ventral sites. Ventral PCC electrodes (n=6) are indicated with a dashed outline. Task selectivity of single units in dorsal PCC Microwires extending from the distal tip of a subset of sEEG probes allowed for recording, detecting, and sorting single unit spiking activity within dPCC (nprobes = 6; nunits = 91; See Methods). Overall, PCC neurons varied in their mean firing rate, but predominately displayed sparse firing properties, with a group mean spike rate of 1.7 Hz (across entire task). Initially, when averaging all units, group mean firing rates suggested limited task specific responses and wide variability (Figure 4—figure supplement 1A). Inspection of individual firing rates indicated this was due to a diversity of opposing functional selectivity profiles across units. Therefore, we applied unsupervised hierarchical clustering of units based on the similarity of task response profiles to identify putative functional types (See Methods; Figure 4—figure supplement 1). Strikingly, this clustering revealed four clear functional types, with several unique response features. Figure 4 shows example unit raster plots and instantaneous firing rates over time for each of the four identified cell types. Two functional types (1 and 2) showed increased firing rates to the executive task conditions, consistent with LFP findings. However, these units displayed a more specific level of selectivity than that of the population data. These two functional types showed condition-specific selectivity within the executive tasks, where Type 1 (nunits = 13) was selective for the search condition only, whereas Type 2 (nunits = 34) was selective for the add condition only. Similar to LFP BBG responses, Type 1 and 2 units showed increased activity beginning during the cue period and continuing to increase with task engagement. Overall, Type 1 and 2 unit groups are consistent with LFP evidence for CCN-like executive processing within dPCC but suggest distinct functional cell types underlie the observed LFP BBG responses. In contrast to the LFP data, two additional functional unit groups reliably showed response profiles consistent with the DMN. Whereby, Type 3 units (nunits = 26), displayed firing rates that were increased for both the past and future episodic conditions, weakly elevated for the rest condition, and suppressed for both executive task conditions (search/add; Figure 4C). Such a response profile is highly consistent with the DMN predicted responses (Figure 1D). Furthermore, unlike Type 1 and 2 units, Type 3 units showed a more delayed increase in firing rate, occurring well after the start of task engagement. Finally, Type 4 units (nunits = 18) primarily displayed increased firing rates to the rest condition, which is another related functional property often associated with the DMN (Dastjerdi et al., 2011). These units, which typically showed higher basal firing rates, increased firing after the cue was presented. Consistent with our observations, there was initially no significant main effect of task condition on firing rate (p=0.55) prior to considering cluster type. There was, however, a significant effect of cluster type on mean task firing rate (p=0.01) and a significant interaction between task condition and cluster type (p<0.0001). To quantify the consistency of cluster membership, we performed hierarchical clustering through a complete leave-one-out process, resulting in a 94% identical cluster rate. Importantly, each of the four functional cell types were observed on multiple microwire probes, indicating that none of the cluster types originated from a single subject or recording site. Furthermore, each microwire probe gave rise to units of different selectivity types, suggesting a more mixed organization at the single unit level. Together, these findings in part support LFP observations, but further suggest a richer and more complex array of functional organization within dPCC. These data provide the first single unit evidence of both CCN and DMN function within human PCC. Figure 4 with 1 supplement see all Download asset Open asset Four functional single unit types in dPCC. (A) Example isolated single unit waveforms. (B) Raster plots and instantaneous firing rate traces for four example isolated single units shown in (A). Example units show distinct functional selectivity profiles across task conditions. (C) Mean instantaneous firing rates (with s.e.m. shading) across task conditions for the four functional single unit types identified based on unsupervised similarity clustering (See Methods & Figure 4—figure supplement 1; Type 1 nunits = 13; Type 2 nunits = 34; Type 3 nunits = 26; Type 4 nunits = 18). (D) Mean firing rate (with s.e.m.) for the four functional single unit types (averaged over task onset to 2 s into task execution). In (B) and (C), black vertical lines indicate time of cue and task onset. Discussion Intracranial recordings targeting human dPCC revealed strong electrophysiological evidence of executive task engagement. Dorsal PCC neural populations, as captured by LFP broadband gamma activity, displayed executive processing activity profiles consistent with that of cognitive control regions, as opposed to the episodic/DMN activity commonly attributed to the entire PCC (Fox et al., 2018). Across-subject consideration of the spatial organization of population responses showed some clustering of executive selectivity inferior within dPCC near the callosal sulcus. The unique opportunity to record single neuron activity in human dPCC illuminated a far richer functional heterogeneity, beyond what could be discerned at the population level. Neurons in dPCC exhibited distinct selectivity profiles for specific executive attention tasks (search or add), consistent with, but more selective than, LFP data. In addition, while not observed in the LFP, a distinct set of neurons showed a clear DMN type of functional profile selective to either episodic processing (past and future) conditions or rest periods. Together, these findings allow for reconciliation of conflicting reports of PCC function between species and begin to unveil the complex functional contributions of single neurons in dPCC to executive and episodic processing. Executive processing in human PCC Historically, human PCC has been functionally considered within its role as a member of the DMN, active during internally focused cognition and memory retrieval and deactivated during attention demanding tasks (Buckner et al., 2008; Buckner and DiNicola, 2019). Such a functional role of PCC is in direct contrast to the functional view predominating from non-human primate electrophysiology studies, examining its contributions to executive processes including strategy selection and decision making (Pearson et al., 2011). Based on the common dorsal targeting of PCC recordings in these studies (termed area CGp), we sought to reconcile conflicting reports by focusing on the electrophysiology of human dPCC during a task that required performance of both executive and episodic processing. We found that neural populations in human dPCC showed significantly stronger BBG amplitude LFP responses during executive attention conditions (search/add) than episodic retrieval conditions, reflective of executive processing. Thus, when specifically examining dorsal PCC, population selectivity is more cohesive with the non-human primate electrophysiological data than the traditional DMN view of PCC in the human literature. By providing electrophysiological evidence of executive activity within human dPCC, these findings provide evidence of homology between the functions of macaque area CGp and human dPCC (i.e. area 23d in both species Vogt et al., 1987; Vogt et al., 1995). Further, they highlight the importance of considering subregional variation in PCC. Importantly, these findings are consistent with a selection of literature from human neuroimaging, typically unincorporated with the DMN/memory literature (Acikalin et al., 2017), which implicates specifically dPCC with executive control processes as well as certain aspects of value-based decisions (Bartra et al., 2013; Clithero and Rangel, 2014; Oldham et al., 2018). Functional organization of PCC The heterogeneity of functional responses in PCC prompts the question of the spatial organization of the region. As previously noted, cytoarchitecture, structural connectivity, and network parcellations suggest subregional distinctions between dorsal and ventral PCC (Vogt et al., 1995; Vincent et al., 2008; Greicius et al., 2009). Electrophysiology studies, though limited, have alternatively suggested a more mixed functional mosaic throughout PCC and posteromedial cortex more broadly (Daitch and Parvizi, 2018). Our findings reveal clustering of early executive selectivity inferiorly within dPCC along the callosal sulcus, adding to evidence for a dorsal/ventral gradient for executive and episodic responses. Electrodes with executive activity were observed proximal to voxels associated with ‘cognitive control’ in fMRI studies, linking our findings with dPCC activations appearing in neuroimaging data. These results begin to illuminate that there is some functional organization of heterogeneous activity on the population level, as opposed to a totally mixed mosaic. Population selectivity appears to vary by dorsal/ventral subregions, though the division between subregions is complex and likely subject to individual differences. Regarding the present study, we note that our focus was on dPCC, with vPCC being more sparsely sampled, limiting a full characterization of functional gradients. However, we also note that our vPCC findings are consistent with a number of intracranial studies showing DMN-like responses within PCC (Fox et al., 2018). Precision fMRI within individuals emphasizes the impact of individual variability, particularly in associative cortices and their putative networks (Braga and Buckner, 2017). Indeed, precision neuroimaging specifically highlights the dPCC as region of interest in assessing individual variability (Gordon et al., 2017a). A much larger spatial sampling of recording sites throughout dorsal and ventral PCC, in addition to further consideration of individual anatomy, will be required to determine this organization. As precision functional data might not always be available for individuals, how might functional organization within PCC be inferred? Our electrophysiological observations are broadly consistent with recent large-scale examination of PCC sulcal anatomy which identified a new tertiary sulcus (inframarginal sulcus) as a useful landmark for the transition from DMN to CCN within dPCC (Willbrand et al., 2022). Further integration of invasive electrophysiology and precision neuroimaging within subjects will be critical for elucidating key features of PCC functional neuroanatomy and its variability across individuals (Gordon et al., 2017b). Single neuron executive and episodic selectivity Acquisition of single neuron spiking activity within human dPCC unveiled distinct functional profiles and organizational principles not observable through population recordings alone. Functiona" @default.
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W4313154170 title "Editor's evaluation: Distinct population and single-neuron selectivity for executive and episodic processing in human dorsal posterior cingulate" @default.
W4313154170 doi "https://doi.org/10.7554/elife.80722.sa0" @default.
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