Neural Representation of Time across Complementary Reference Frames
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eLife Assessment
This study presents a valuable finding on the neural representation of time from two distinct egocentric and allocentric reference frames. The presentation of evidence in the version of the original submission is incomplete, as further conceptual clarifications, methodological details, and addressing potential confounds would strengthen the study. The work will be of interest to cognitive neuroscientists working on the perception and memory of time.
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Abstract
Abstract
Humans conceptualize time in terms of space, allowing flexible time construals from various perspectives. We can travel internally through a timeline to remember the past and imagine the future (i.e., mental time travel) or watch from an external standpoint to have a panoramic view of history (i.e., mental time watching). However, the neural mechanisms that support these flexible temporal construals remain unclear. To investigate this, we asked participants to learn a fictional religious ritual of 15 events. During fMRI scanning, they were guided to consider the event series from either an internal or external perspective in different tasks. Behavioral results confirmed the success of our manipulation, showing the expected symbolic distance effect in the internal-perspective task and the reverse effect in the external-perspective task. We found that the activation level in the posterior parietal cortex correlated positively with sequential distance in the external-perspective task but negatively in the internal-perspective task. In contrast, the activation level in the anterior hippocampus positively correlated with sequential distance regardless of the observer’s perspectives. These results suggest that the hippocampus stores the memory of the event sequences allocentrically in a perspective-agnostic manner. Conversely, the posterior parietal cortex retrieves event sequences egocentrically from the optimal perspective for the current task context. Such complementary allocentric and egocentric representations support both the stability of memory storage and the flexibility of time construals.
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eLife Assessment
This study presents a valuable finding on the neural representation of time from two distinct egocentric and allocentric reference frames. The presentation of evidence in the version of the original submission is incomplete, as further conceptual clarifications, methodological details, and addressing potential confounds would strengthen the study. The work will be of interest to cognitive neuroscientists working on the perception and memory of time.
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Reviewer #1 (Public review):
Summary:
In this fMRI study, the authors wished to assess neural mechanisms supporting flexible "temporal construals". For this, human participants learned a story consisting of fifteen events. During fMRI, events were shown to them and they were instructed to consider the event from "an internal" or from "an external" perspective. The authors found opposite patterns of brain activity in the posterior parietal cortex and the anterior hippocampus for the internal and the external viewpoint. They conclude that allocentric sequences are stored in the hippocampus, whereas egocentric sequences are used in the parietal cortex. The claims align with previous fMRI work addressing this question.
Strengths:
The research topic is fascinating, and very few labs in the world are asking the question of how time is …
Reviewer #1 (Public review):
Summary:
In this fMRI study, the authors wished to assess neural mechanisms supporting flexible "temporal construals". For this, human participants learned a story consisting of fifteen events. During fMRI, events were shown to them and they were instructed to consider the event from "an internal" or from "an external" perspective. The authors found opposite patterns of brain activity in the posterior parietal cortex and the anterior hippocampus for the internal and the external viewpoint. They conclude that allocentric sequences are stored in the hippocampus, whereas egocentric sequences are used in the parietal cortex. The claims align with previous fMRI work addressing this question.
Strengths:
The research topic is fascinating, and very few labs in the world are asking the question of how time is represented in the human brain. Working hypotheses have been recently formulated, and this work seems to want to tackle some of them.
Weaknesses:
The current writing is fuzzy both conceptually and experimentally. I cannot provide a sufficiently well-informed assessment of the quality of the experimental work because there is a paucity of details provided in the report. Any future revisions will likely improve transparency.
(1) Improving writing and presentation:
The abstract and the introduction make use of loaded terms such as "construals", "mental timeline", "panoramic views" in very metaphoric and unexplained ways. The authors do not provide a comprehensive and scholarly overview of these terms, which results in verbiage and keywords/name-dropping without a clear general framework being presented. Some of these terms are not metaphors. They do refer to computational concepts that the authors should didactically explain to their readership. This is all the more important that some statements in the Introduction are misattributed or factually incorrect; some statements lack attributions (uncited published work).
Once the theory, the question, and the working hypothesis are clarified, the authors should carefully explain the task.
(2) The experimental approach lacks sufficient details to be comprehensible to a general audience. In my opinion, the results are thus currently uninterpretable. I highlight only a couple of specific points (out of many). I recommend revision and clarification.
a) No explanation of the narrative is being provided. The authors report a distribution of durations with no clear description of the actual sequence of events. The authors should provide the text that was used, how they controlled for low-level and high-level linguistic confounds.
b) The authors state, "we randomly assigned 15 phrases to the events twice". It is impossible to comprehend what this means. Were these considered stimuli? Controls? IT is also not clear which event or stimulus is part of the "learning set" and whether these were indicated to be such to participants.
c) The left/right counterbalancing is not being clearly explained. The authors state that there is counterbalancing, but do not sufficiently explain what it means concretely in the experiment. If a weak correlation exists between sequential position and distance, it also means that the position and the distance have not been equated within. How do the authors control for these?
d) The authors used two tasks. In the "external perspective" one, the authors asked participants to report whether events were part of the same or a different part of the day. In the "internal perspective one", the authors asked participants to project themselves to the reference event and to determine whether the target event occurred before or after the projected viewpoint. The first task is a same/different recognition task. The second task is a temporal order task (e.g., Arzy et al. 2009). These two asks are radically different and do not require the same operationalization. The authors should minimally provide a comprehensive comparison of task requirements, their operationalization, and, more importantly, assess the behavioral biases inherent to each of these tasks that may confound brain activity observed with fMRI.
e) The authors systematically report interpreted results, not factual data. For instance, while not showing the results on behavioral outcomes, the authors directly interpret them as symbolic distance effects.
Crucially, the authors do not comment on the obvious differences in task difficulty in these two tasks, which demonstrates a substantial lack of control in the experimental design. The same/different task (task 1 called "external perspective") comes with known biases in psychophysics that are not present in the temporal order task (task 2 called " internal perspective"). The authors also did not discuss or try to match the performance level in these two tasks. Accordingly, the authors claim that participants had greater accuracy in the external (same/different) task than in the internal task, although no data are shown and provided to support this report. Further, the behavioral effect is trivialized by the report of a performance accuracy trade-off that further illustrates that there is a difference in the task requirements, preventing accurate comparison of the two tasks.
All fMRI contrasts are also confounded by this experimental shortcoming, seeing as they are all reported at the interaction level across a task. For instance, in Figure 4, the authors report a significant beta difference between internal and external tasks. It is impossible to disentangle whether this effect is simply due to task difference or to an actual processing of the duration that differs across tasks, or to the nature of the representation (the most difficult to tackle, and the one chosen by the authors).
Conclusion:
In conclusion, the current experimental work is confounded and lacks controls. Any behavioral or fMRI contrasts between the two proposed tasks can be parsimoniously accounted for by difficulty or attentional differences, not the claim of representational differences being argued for here.
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Reviewer #2 (Public review):
Summary:
Xu et al. used fMRI to examine the neural correlates associated with retrieving temporal information from an external compared to internal perspective ('mental time watching' vs. 'mental time travel'). Participants first learned a fictional religious ritual composed of 15 sequential events of varying durations. They were then scanned while they either (1) judged whether a target event happened in the same part of the day as a reference event (external condition); or (2) imagined themselves carrying out the reference event and judged whether the target event occurred in the past or will occur in the future (internal condition). Behavioural data suggested that the perspective manipulation was successful: RT was positively correlated with sequential distance in the external perspective task, while a …
Reviewer #2 (Public review):
Summary:
Xu et al. used fMRI to examine the neural correlates associated with retrieving temporal information from an external compared to internal perspective ('mental time watching' vs. 'mental time travel'). Participants first learned a fictional religious ritual composed of 15 sequential events of varying durations. They were then scanned while they either (1) judged whether a target event happened in the same part of the day as a reference event (external condition); or (2) imagined themselves carrying out the reference event and judged whether the target event occurred in the past or will occur in the future (internal condition). Behavioural data suggested that the perspective manipulation was successful: RT was positively correlated with sequential distance in the external perspective task, while a negative correlation was observed between RT and sequential distance for the internal perspective task. Neurally, the two tasks activated different regions, with the external task associated with greater activity in the supplementary motor area and supramarginal gyrus, and the internal condition with greater activity in default mode network regions. Of particular interest, only a cluster in the posterior parietal cortex demonstrated a significant interaction between perspective and sequential distance, with increased activity in this region for longer sequential distances in the external task, but increased activity for shorter sequential distances in the internal task. Only a main effect of sequential distance was observed in the hippocampus head, with activity being positively correlated with sequential distance in both tasks. No regions exhibited a significant interaction between perspective and duration, although there was a main effect of duration in the hippocampus body with greater activity for longer durations, which appeared to be driven by the internal perspective condition. On the basis of these findings, the authors suggest that the hippocampus may represent event sequences allocentrically, whereas the posterior parietal cortex may process event sequences egocentrically.
Strengths:
The topic of egocentric vs. allocentric processing has been relatively under-investigated with respect to time, having traditionally been studied in the domain of space. As such, the current study is timely and has the potential to be important for our understanding of how time is represented in the brain in the service of memory. The study is well thought out, and the behavioural paradigm is, in my opinion, a creative approach to tackling the authors' research question. A particular strength is the implementation of an imagination phase for the participants while learning the fictional religious ritual. This moves the paradigm beyond semantic/schema learning and is probably the best approach besides asking the participants to arduously enact and learn the different events with their exact timings in person. Importantly, the behavioural data point towards successful manipulation of internal vs. external perspective in participants, which is critical for the interpretation of the fMRI data. The use of syllable length as a sanity check for RT analyses, as well as neuroimaging analyses, is also much appreciated.
Weaknesses/Suggestions:
Although the design and analysis choices are generally solid, there are a few finer details/nuances that merit further clarification or consideration in order to strengthen the readers' confidence in the authors' interpretation of their data.
(1) Given the known behavioural and neural effects of boundaries in sequence memory, I was wondering whether the number of traversed context boundaries (i.e., between morning-afternoon, and afternoon-evening) was controlled for across sequential length in the internal perspective condition? Or, was it the case that reference-target event pairs with higher sequential numbers were more likely to span across two parts of the day compared to lower sequential numbers? Similarly, did the authors examine any potential differences, whether behaviourally or neurally, for day part same vs. day part different external task trials?
(2) I would appreciate further insight into the authors' decision to model their task trials as stick functions with duration 0 in their GLMs, as opposed to boxcar functions with varying durations, given the potential benefits of the latter (e.g., Grinband et al., 2008). I concur that in certain paradigms, RT is considered a potential confound and is taken into account as a nuisance covariate (as the authors have done here). However, given that RTs appear to be critical to the authors' interpretation of participant behavioural performance, it would imply that variations in RT actually reflect variations in cognitive processes of interest, and hence, it may be worth modelling trials as boxcar functions with varying durations.
(3) The activity pattern across tasks and sequential distance in the posterior parietal cortex appears to parallel the RT data. Have the authors examined potential relationships between the two (e.g., individual participant slopes for RT across sequential distance vs. activity betas in the posterior parietal cortex)?
(4) There were a few places in the manuscript where the writing/discussion of the wider literature could perhaps be tightened or expanded. For instance:
i) On page 16, the authors state 'The negative correlation between the activation level in the right PPC and sequential distance has already been observed in a previous fMRI study (Gauthier & van Wassenhove, 2016b). The authors found a similar region (the reported MNI coordinate of the peak voxel was 42, -70, 40, and the MNI coordinate of the peak voxel in the present study was 39, -70, 35), of which the activation level went up when the target event got closer to the self-positioned event. This finding aligns with the evidence suggesting that the posterior parietal cortex implements egocentric representations.' Without providing a little more detail here about the Gauthier & van Wassenhove study and what participants were required to do (i.e., mentally position themselves at a temporal location and make 'occurred before' vs. 'occurred after' judgements of a target event), it could be a little tricky for readers to follow why this convergence in finding supports a role for the posterior parietal cortex in egocentric representations.
ii) Although the authors discuss the Lee et al. (2020) review and related studies with respect to retrospective memory, it is critical to note that this work has also often used prospective paradigms, pointing towards sequential processing being the critical determinant of hippocampal involvement, rather than the distinction between retrospective vs. prospective processing.
iii) The authors make an interesting suggestion with respect to hippocampal longitudinal differences in the representation of event sequences, and may wish to relate this to Montagrin et al. (2024), who make an argument for the representation of distant goals in the anterior hippocampus and immediate goals in the posterior hippocampus.
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