Patients with focal lesions to the vmPFC were selectively impaired in projecting themselves to the future and in recognizing relative-future events

An asymmetry in past and future mental time travel following vmPFC damage. Elisa Ciaramelli, Filomena Anelli, Francesca Frassinetti. Social Cognitive and Affective Neuroscience, nsaa163, December 31 2020. https://doi.org/10.1093/scan/nsaa163

Abstract: The role of ventromedial prefrontal cortex (vmPFC) in mental time travel toward the past and the future is debated. Here, patients with focal lesions to the vmPFC and brain-damaged and healthy controls mentally projected themselves to a past, present or future moment of subjective time (self-projection) and classified a series of events as past or future relative to the adopted temporal self-location (self-reference). We found that vmPFC patients were selectively impaired in projecting themselves to the future and in recognizing relative-future events. These findings indicate that vmPFC damage hinders the mental processing of and movement toward future events, pointing to a prominent, multifaceted role of vmPFC in future-oriented mental time travel.

Keywords: mental time travel, self-projection, episodic memory, future thinking, vmPFC

Discussion

The present study investigated the effect of vmPFC damage on two component processes of MTT: the ability to project the self in time to assume different temporal perspectives (self-projection), and to determine, for each event in a series, whether it has already happened or is yet to happen relative to the currently assumed time perspective (self-reference). We found a striking asymmetry in the effect of vmPFC damage on both aspects of MTT, which hindered vmPFC patients’ possibility to project the self to the future, but not the past or the present, and to recognize relative-future but not relative-past events.

Before discussing, in turn, each aspect of vmPFC patients’ deficit in future-oriented MTT, we wish to emphasize that this deficit is not a common consequence of brain damage, for example reflective of a shortening of future time perspective following illness and perceived vulnerability (Ciaramelli et al., 2019). Indeed, problems with future-oriented MTT were consistently present in vmPFC patients but not in control patients with brain damage not involving vmPFC. Our results are also unlikely to reflect poor comprehension of self-projection or task instructions on the vmPFC patients’ part. Indeed, all participants, including vmPFC patients, were slower at recognizing events while assuming a past or future (compared to present) time perspective, a robust finding reflecting the cognitive cost of self-projection (Arzy et al., 2008, 2009; Anelli et al., 2016a,b; Gauthier et al., 2019). That this pattern was observed also in vmPFC patients strongly suggests they did indeed try and abandon the present moment to mentally move toward the subjective past and future. The vmPFC patients’ self-projection toward the future, however, went often awry, as indicated by an abnormal number of errors while processing events from that time perspective, as if patients failed at assuming (or maintaining) a future self-location, while they were normally capable to project the self back to the past. This finding aligns with recent neuroimaging evidence that during MTT the medial prefrontal cortex exhibit graded, progressively increasing activation with the succession of past, present and future self-projection (Gauthier et al., 2019).

The selective deficit in future-oriented self-projection we detected in vmPFC patients stands in contrast to previous studies showing a pervasive impairment in remembering the past and imagining the future in vmPFC patients (Bertossi et al., 2016a,b), which also characterizes amnesic patients with medial temporal lobe lesions (Race et al., 2011). These findings, however, are only apparently in conflict. Indeed, previous studies had used MTT tasks requiring both the adoption of past and future temporal perspective and the construction of complex events from those perspectives (Bertossi et al., 2016b), while the task we used here only involves the former. Thus, while impaired construction of both past and future experiences in previous studies may reflect a general problem in assembling detail-rich events, apparent even when vmPFC (as well as medial temporal lobe) patients have to construct atemporal experiences (Hassabis et al., 2007; Bertossi et al., 2016a; see also De Luca et al., 2018), the present findings insulate an additional problem vmPFC patients have in assuming a future temporal perspective, above and beyond their event construction deficit, which affects MTT upstream. In contrast, patients with medial temporal lobe lesions have proven able to project the self in (future) time (Dalla Barba, 2001; Arzy et al., 2009; Kwan et al., 2013; Craver et al., 2014), and their problems in imagining future experiences are likely to be fully explained by impaired event construction (McCormick et al., 2019). Indeed, a single-case study of an amnesic patient with bilateral medial temporal damage using the same paradigm we have used here found no impairment in self-projection (Arzy et al., 2009). Our findings make contact with previous evidence that vmPFC patients have more problems in constructing future compared to atemporal experiences (Bertossi et al., 2016a), an asymmetry not present in medial temporal lobe amnesia (Hassabis  et al., 2007), and that, when asked to enumerate personal future life events, vmPFC patients produce events less far ahead into the future than do brain-damaged controls, suggestive of a short future time perspective (Fellows  and Farah, 2005). Also, vmPFC patients (but, again, not medial temporal lobe amnesiacs; Kwan et al., 2013) show increased delay discounting (Sellitto et al., 2010; Peters and D’Esposito, 2016), in line with the view that they fail to conceive the future, even in purely semantic, abstract terms, hence devalue future rewards.

Why would vmPFC be necessary for future-oriented self-projection? It has been shown that self-projection to one’s personal past/future typically originates from the activation of high-level knowledge structures, such as schematic representations of life time periods and the self (e.g. when I graduated and when I will have a child), to then possibly converge on specific events of one’s personal timeline (Conway and Pleydell-Pearce, 2000; D’Argembeau and Mathy, 2011; D’Argembeau, 2020). Imagining the future relies more on schema-based knowledge than remembering the past, because we have no direct experience of future events (Anderson and Dewhurst, 2009; Berntsen and Bohr, 2010; Rubin, 2014). Knowledge about personal goals (e.g. I want to become a researcher) is especially effective in driving the construction of ones’ personal future (D’Argembeau and Mathy, 2011). The vmPFC is critical for appropriate processing of schema-related information (Burgess and Shallice, 1996; Ghosh et al., 2014), including knowledge about the self (Philippi et al., 2012; Verfaellie et al., 2019) and personal goals (D’Argembeau et al., 2010). We argue, therefore, that vmPFC patients failed to project the self to the future due to an inability in activating schematic knowledge critical to construct a mental representation of their personal future, so as to assume the perspective of their future self. This interpretation aligns with current views of the dynamics of MTT, according to which vmPFC initiates the activation of high-order autobiographical knowledge (e.g. lifetime periods and self schema), from which the hippocampus may then access (McCormick et al., 2019; D’Argembeau, 2020; Dafni-Merom and Arzy, 2020; see also Barry et al., 2019) or process (Schurr et al., 2018) specific experiences.

Orthogonal to their impairment in future self-projection, vmPFC patients additionally showed a deficit in self-referencing future events, that is, in recognizing events lying ahead in the future with respect to their assumed location in subjective time (whether past, present or future), which were misclassified more often than relative-past events. Healthy as well as brain-damaged controls showed a comparable performance in recognizing relative-future and relative-past events, hence the selective deficit evinced by vmPFC patients with relative-future events is unlikely to merely reflect task difficulty. Note, also, that vmPFC patients’ false recognition of future events also emerged in the past self-location condition, that is, when dealing with events that were not actually future (with respect to the present time), and therefore it does not simply denote a problem in distinguishing familiar from novel events, or factual from potential, hypothetical events (see also Anelli et al., 2018).

One is tempted to interpret vmPFC patients’ deficit as reflecting disordered chronology. The vmPFC, together with the basal forebrain, is indeed thought to support the correct assignment of memories to their correct place in time (Moscovitch, 1995; Tranel and Jones, 2006), and confabulation, a consequence of vmPFC damage, consists of memories that are often false in temporal context (Schnider, 2003; Gilboa et al., 2006; Bertossi et al., 2016b). Moreover, the vmPFC is engaged while individuals orient themselves in time (Peer et al., 2015), and determining the temporal distance between the self and an event engages the prefrontal cortex (Gauthier et al., 2019). Yet impaired chronology is again too general an interpretation for vmPFC patients’ performance in this task, as it would have led to an equal distribution of wrong attributions of relative-future events to the past and of relative-past events to the future, while vmPFC patients only showed an increased tendency to falsely recognize relative-future events as past.

According to one prominent view, the timing of one’s memories is not indicated by stable ‘time tags’ marking each of them in succession (Friedman, 1993), but dynamically reconstructed by strategic processes depending on retrieval goals (Burgess and Shallice, 1996). We propose that vmPFC patients’ false recognition of relative-future events reveals a specific deficit in monitoring novelty signals originating from events that, with respect to the current self-position in time, are yet to happen, which felt wrongly familiar. This deficit is reminiscent of other instances of false recognition in vmPFC patients. For example, in recognition memory tasks, vmPFC patients falsely recognize distractors that were targets in previous runs of the experiment (Schnider, 2003), or with which they had pre-experimental experience (Ciaramelli and Ghetti, 2007), as if they failed to appreciate that, in the context of the current run or experiment, they were novel. More generally, vmPFC patients tend to assimilate irrelevant information into activated schemata (Ghosh et al., 2014). One could argue, therefore, that vmPFC patients failed at using a schema of the current reality to identify (future) events that mismatched the schema because they were not previously experienced. This deficit had an impact on recognition of personal as well as general relative-future events, consistent with previous evidence of false recognition in both domains following vmPFC damage (Schnider, 2003; Gilboa et al., 2006; Ciaramelli and Ghetti, 2007), in fact depriving vmPFC patients fully of a view of the future.

We end by noting some limitations and future directions of our work. The sample size is small, and therefore some effects may have gone undetected due to limited statistical power. Future studies involving more vmPFC patients will help confirm the selective deficit we observed in future MTT and link it to specific vmPFC subregions. Also, our results show that, even though control patients did not show a future MTT impairment at the group level, a few of them did, suggesting that other (e.g. temporo-parietal) regions may be causally linked to future self-projection and self-reference. Again, testing this hypothesis will require recruiting larger samples of patients, and with more homogeneous lesion sites than our control patient group. Finally, the task we used can detect whether patients place events correctly in the (relative) past and future, but not whether they would put the events in the correct chronological order with respect to one another within the past or the future. Thus, a future direction of the study is to test whether the disadvantage observed in vmPFC patients in processing future events is limited to the recognition of events, or it would extend to their ordering.

In summary, we have shown that vmPFC patients have a multifaceted impairment of future MTT, being unable to project themselves to the future, and to anticipate the events that await them in the future, pointing to a prominent role of vmPFC in future-oriented cognition. Future self-projection and self-reference have a profound impact on future-oriented choice: taking the perspective of one’s future self reduces discounting of future rewards (Peters and Büchel, 2010), and the anticipation of future events is associated with goal-directed behavior and motivation (Boyer, 2008). Thus, the future-oriented MTT deficit we detected in vmPFC patients is likely to play a role in their steep delay discounting (Sellitto et al., 2010), poor problem-solving (Peters et al., 2017) and apathy (Fellows and Farah, 2005). If so, cueing future thinking (Peters and Büchel, 2010), or the deployment of spatial attention toward future locations of the mental timeline (Anelli et al., 2016b), may be effective in pushing patients’ temporal horizon ahead into the future, reducing their shortsightedness.