Temporal discounting when outcomes are experienced in the moment: Validation of a novel paradigm and comparison with a classic hypothetical intertemporal choice task.

When faced with intertemporal choices, people typically devalue rewards available in the future compared to rewards more immediately available, a phenomenon known as temporal discounting. Decisions involving intertemporal choices arise daily, with critical impact on health and financial wellbeing. Although many such decisions are "experiential" in that they involve delays and rewards that are experienced in real-time and can inform subsequent choices, most studies have focused on intertemporal choices with hypothetical outcomes (or outcomes delivered after all decisions are made). The present study focused on experiential intertemporal choices. First, a novel intertemporal choice task was developed and validated, using delays experienced in real time and artistic photographs as consumable perceptual rewards. Second, performance on the experiential task was compared to performance on a classic intertemporal choice task with hypothetical outcomes. Involvement of distinct processes across tasks was probed by examining differential relations to state and trait anxiety. A two-parameter logistic function framework was proposed to fit indifference point data. This approach accounts for individual variability not only in the delay at which an individual switches from choosing the delayed to more immediate option, but also in the slope of that switch. Fit results indicated that the experiential task elicited temporal discounting, with effective trade-off between delay and perceptual reward. Comparison with the hypothetical intertemporal choice task suggested distinct mechanisms: first, temporal discounting across the two tasks was not correlated; and second, state and trait anxiety both were associated with choice behavior in the experiential task, albeit in distinct ways, whereas neither was significantly associated with choice behavior in the hypothetical task. The engagement of different processes in the experiential compared to hypothetical task may align with neural evidence for the recruitment of the hippocampus in animal but not in classic human intertemporal choice studies.

Episodic processes in moral decisions: Evidence from medial temporal lobe amnesia.

Theoretical accounts of moral decision making imply distinct ways in which episodic memory processes may contribute to judgments about moral dilemmas that entail high conflict between a harmful action and a greater good resulting from such action. Yet, studies examining the status of moral judgment in amnesic patients with medial temporal lobe (MTL) lesions have yielded inconsistent results. To examine whether and how episodic processes contribute to high conflict moral decisions, amnesic patients with MTL damage and control participants were asked to judge the moral acceptability of a harmful action across two conditions that differed in the framing of the moral question. We predicted that personal (but not abstract) framing would engage episodic processes involved in mental simulation, yielding a selective impairment in MTL patients in the personal framing condition. This prediction was not confirmed as neither patients nor controls were influenced by the framing of the moral question. With the exception of a patient whose lesion extended into the amygdala bilaterally, patients were less willing than controls to endorse the utilitarian option, rejecting the harmful action despite its beneficial outcome. They also rated actions as emotionally more intense than did controls. These findings suggest that episodic processes involved in mental simulation are necessary to prospectively evaluate action-outcome contingencies.

The status of semantic memory in medial temporal lobe amnesia varies with demands on scene construction.

Semantic memory is typically preserved in medial temporal lobe (MTL) amnesia. However, there are instances of impairment, such as in the recall of semantic narratives. As some forms of semantic knowledge play out in a spatial context, one possible explanation is that semantic memory impairments, when observed, relate to demands on scene construction - the ability to bind and maintain spatial information in a coherent representation. To investigate whether semantic memory impairments in MTL amnesia can be understood with reference to a deficit in scene construction, the current study examined knowledge of scripts that vary in the extent to which they play out in a scene context in nine patients with MTL amnesia and eighteen healthy control subjects. Scripts are routine activities characterized by an ordered set of actions, including some that are essential for completing the activity. Comparing performance on scene-based scripts (e.g., buying groceries at the grocery store) and object-based scripts (e.g., addressing a letter), we found that patients generated the same number of total action steps as controls for both types of script, but patients were selectively impaired at generating essential actions steps for scene-based scripts. Furthermore, patients made more sequencing and idiosyncratic errors than controls in the scene-based, but not in the object-based, scripts. These findings demonstrate that the hippocampus plays a critical role in the retrieval of semantic knowledge about everyday activities when such retrieval entails scene construction.

Relational processing in the semantic domain is impaired in medial temporal lobe amnesia.

It has been argued that the hippocampus supports cognition by virtue of its role in flexibly binding together distinct elements of experience. Such 'relational processing' enables us to (re)construct episodic representations of real or imagined events. The present study examined whether hippocampally mediated relational processing also contributes to the construction of semantic representations. To do so, we asked amnesic individuals with medial temporal lobe (MTL) lesions including the hippocampus to generate hypothetical meanings for novel word compounds (e.g., cactus carpet), a task that requires existing concepts to be flexibly linked. The quality of definitions and number of features generated for the novel compounds were lower in patients with MTL lesions than in control participants. Whereas the subset of patients with lesions extending into lateral temporal cortex had additional difficulty generating meanings for pre-existing compounds (e.g., bus station), patients with lesions limited to the MTL showed no such deficit, indicating that their impairment in the novel compound condition was not due to reduced access to semantic information. These findings suggest that the role of hippocampally mediated relational processing extends beyond the episodic domain to include the generation of novel semantic representations.

Self-related processing and future thinking: Distinct contributions of ventromedial prefrontal cortex and the medial temporal lobes.

Episodic future thinking depends on a core network of regions that involves, in addition to the medial temporal lobes (MTL), the ventromedial prefrontal cortex (vmPFC). Neuroimaging studies suggest that vmPFC is particularly involved when future thinking requires consideration of self-relevant information, but lesion evidence for a special role of vmPFC in constructing self-relevant scenarios is limited. To clarify the involvement of vmPFC in future thinking, eight patients with vmPFC lesions were asked to imagine future events pertaining to the self or to another person, and their performance was contrasted with that of eight patients with MTL lesions. Patients with vmPFC lesions were no more detailed in their description of future events pertaining to the self than of events pertaining to another person. In contrast, like controls, patients with MTL lesions showed a self-benefit, despite impoverished performance overall. These findings accord with evidence from neuroimaging studies and elucidate the distinct contributions of vmPFC and MTL to future thinking.

Neuropsychological Investigations of Human Amnesia: Insights Into the Role of the Medial Temporal Lobes in Cognition.

The past 30 years of research on human amnesia has yielded important changes in our understanding of the role of the medial temporal lobes (MTL) in memory. On the one hand, this body of evidence has highlighted that not all types of memory are impaired in patients with MTL lesions. On the other hand, this research has made apparent that the role of the MTL extends beyond the domain of long-term memory, to include working memory, perception, and future thinking. In this article, we review the discoveries and controversies that have characterized this literature and that set the stage for a new conceptualization of the role of the MTL in cognition. This shift toward a more nuanced understanding of MTL function has direct relevance for a range of clinical disorders in which the MTL is implicated, potentially shaping not only theoretical understanding but also clinical practice. (JINS, 2017, 23, 732-740).

How does the hippocampus shape decisions?

Making optimal decisions depends on an appreciation of the value of choices. An important source of information about value comes from memory for prior experience. Such value-based learning has historically been considered the domain of a striatal memory system. However, recent developments suggest that memorial representations supported by the hippocampus may also contribute to decision making. Unlike striatal representations, hippocampal ones are flexible; they can be modified and updated as new information is acquired. In this paper we argue that the hippocampus plays a pivotal role in value-based decision making via three flexible learning mechanisms: (1) updating, (2) generalization, and (3) construction.

Attention and implicit memory: priming-induced benefits and costs have distinct attentional requirements.

Attention at encoding plays a critical and ubiquitous role in explicit memory performance, but its role in implicit memory performance (i.e., priming) is more variable: some, but not all, priming effects are reduced by division of attention at encoding. A wealth of empirical and theoretical work has aimed to define the critical features of priming effects that do or do not require attention at encoding. This work, however, has focused exclusively on priming effects that are beneficial in nature (wherein performance is enhanced by prior exposure to task stimuli), and has overlooked priming effects that are costly in nature (wherein performance is harmed by prior exposure to task stimuli). The present study takes up this question by examining the effect of divided attention on priming-induced costs and benefits in a speeded picture-naming task. Experiment 1 shows that the costs, but not the benefits, are eliminated by division of attention at encoding. Experiment 2 shows that the costs (as well as the benefits) in this task are intact in amnesic participants, demonstrating that the elimination of the cost in the divided attention condition in Experiment 1 was not an artifact of the reduced availability of explicit memory in that condition. We suggest that the differential role of attention in priming-induced performance costs and benefits is linked to differences in response competition associated with these effects. This interpretation situates the present findings within a theoretical framework that has been applied to a broad range of facilitatory priming effects.

The medial temporal lobes are critical for reward-based decision making under conditions that promote episodic future thinking.

In the present study, we investigated the effect of medial temporal lobe (MTL) damage on human decision making in the context of reward-based intertemporal choice. During intertemporal choice, humans typically devalue (or discount) a future reward to account for its delayed arrival (e.g., preferring $30 now over $42 in 2 months), but this effect is attenuated when participants engage in episodic future thinking, i.e., project themselves into the future to imagine a specific event. We hypothesized that this attenuation would be selectively impaired in amnesic patients, who have deficits in episodic future thinking. Replicating previous work, in a standard intertemporal choice task, amnesic patients showed temporal discounting indices similar to healthy controls. Consistent with our hypothesis, while healthy controls demonstrated attenuated temporal discounting in a condition that required participants first to engage in episodic future thinking (e.g., to imagine spending $42 at a theatre in 2 months), amnesic patients failed to demonstrate this effect. Moreover, as expected, amnesic patients' narratives were less episodically rich than those of controls. These findings extend the range of tasks that are shown to be MTL dependent to include not only memory-based decision-making tasks but also future-oriented ones.

Sharing mental simulations and stories: hippocampal contributions to discourse integration.

Accumulating evidence suggests that mental simulation of the future and past relies on common processes supported by the hippocampus. However, it is currently unknown whether the hippocampus also supports the ability to share these mental simulations with others. Recently, it has been proposed that language and language-related structures in the brain are particularly important for communicating information not tied to the immediate environment, and indeed specifically evolved so that humans could share their mental time travels into the future and the past with others. The current study investigated whether processes supported by the hippocampus are necessary for effectively communicating the contents of one's mental simulations by examining the discourse of amnesic patients with medial temporal lobe damage. In Experiment 1 we tested whether patients can produce integrated discourse about future and past events by measuring lower-level discourse cohesion and higher-level discourse coherence. Striking reductions in both measures were observed in amnesic patients' narratives about novel future events and experienced past events. To investigate whether these deficits simply reflected concurrent reductions in narrative content, in Experiment 2 we examined the status of discourse integration in patients' verbal narratives about pictures, which contained an equivalent amount of narrative content as controls'. Discourse cohesion and coherence deficits were also present when patients generated narratives based on pictures, and these deficits did not depend on the presence of neural damage outside the hippocampus. Together, these results reveal a pervasive linguistic integration deficit in amnesia that is not limited to discourse about the past or the future and is not simply secondary to reductions in narrative content. More broadly, this study demonstrates that the hippocampus supports the integration of individual narrative elements into coherent and cohesive discourse when constructing complex verbal accounts, and plays a critical role in the effective communication of information to others.

Medial temporal and neocortical contributions to remote memory for semantic narratives: evidence from amnesia.

Studies of remote memory for semantic facts and concepts suggest that hippocampal lesions lead to a temporally graded impairment that extends no more than ten years prior to the onset of amnesia. Such findings have led to the notion that once consolidated, semantic memories are represented neocortically and are no longer dependent on the hippocampus. Here, we examined the fate of well-established semantic narratives following medial temporal lobe (MTL) lesions. Seven amnesic patients, five with lesions restricted to the MTL and two with lesions extending into lateral temporal cortex (MTL+), were asked to recount fairy tales and bible stories that they rated as familiar. Narratives were scored for number and type of details, number of main thematic elements, and order in which the main thematic elements were recounted. In comparison to controls, patients with MTL lesions produced fewer details, but the number and order of main thematic elements generated was intact. By contrast, patients with MTL+ lesions showed a pervasive impairment, affecting not only the generation of details, but also the generation and ordering of main steps. These findings challenge the notion that, once consolidated, semantic memories are no longer dependent on the hippocampus for retrieval. Possible hippocampal contributions to the retrieval of detailed semantic narratives are discussed.

Medial temporal lobe contributions to short-term memory for faces.

The role of the medial temporal lobes (MTL) in short-term memory (STM) remains a matter of debate. Whereas imaging studies commonly show hippocampal activation during short-delay memory tasks, evidence from amnesic patients with MTL lesions is mixed. It has been argued that apparent STM impairments in amnesia may reflect long-term memory (LTM) contributions to performance. We challenge this conclusion by demonstrating that MTL amnesic patients show impaired delayed matching-to-sample (DMS) for faces in a task that meets both a traditional delay-based and a recently proposed distractor-based criterion for classification as an STM task. In Experiment 1, we demonstrate that our face DMS task meets the proposed distractor-based criterion for STM classification, in that extensive processing of delay-period distractor stimuli disrupts performance of healthy individuals. In Experiment 2, MTL amnesic patients with lesions extending into anterior subhippocampal cortex, but not patients with lesions limited to the hippocampus, show impaired performance on this task without distraction at delays as short as 8 s, within temporal range of delay-based STM classification, in the context of intact perceptual matching performance. Experiment 3 provides support for the hypothesis that STM for faces relies on configural processing by showing that the extent to which healthy participants' performance is disrupted by interference depends on the configural demands of the distractor task. Together, these findings are consistent with the notion that the amnesic impairment in STM for faces reflects a deficit in configural processing associated with subhippocampal cortices and provide novel evidence that the MTL supports cognition beyond the LTM domain.

Losing sight of the future: Impaired semantic prospection following medial temporal lobe lesions.

The ability to imagine the future (prospection) relies on many of the same brain regions that support memory for the past. To date, scientific research has primarily focused on the neural substrates of episodic forms of prospection (mental simulation of spatiotemporally specific future events); however, little is known about the neural substrates of semantic prospection (mental simulation of future nonpersonal facts). Of particular interest is the role of the medial temporal lobes (MTLs), and specifically the hippocampus. Although the hippocampus has been proposed to play a key role in episodic prospection, recent evidence suggests that it may not play a similar role in semantic prospection. To examine this possibility, amnesic patients with MTL lesions were asked to imagine future issues occurring in the public domain. The results showed that patients could list general semantic facts about the future, but when probed to elaborate, patients produced impoverished descriptions that lacked semantic detail. This impairment occurred despite intact performance on standard neuropsychological tests of semantic processing and did not simply reflect deficits in narrative construction. The performance of a patient with damage limited to the hippocampus was similar to that of the remaining patients with MTL lesions and amnesic patients' impaired elaboration of the semantic future correlated with their impaired elaboration of the semantic past. Together, these results provide novel evidence from MTL amnesia that memory and prospection are linked in the semantic domain and reveal that the MTLs play a critical role in the construction of detailed, multi-element semantic simulations.

Intact implicit verbal relational memory in medial temporal lobe amnesia.

To elucidate the role of the hippocampus in unaware relational memory, the present study examined the performance of amnesic patients with medial temporal lobe (MTL) lesions on a cued category-exemplar generation task. In contrast to a prior study in which amnesic patients showed impaired performance (Verfaellie et al., Cognitive, Affective, and Behavioral Neuroscience, 2006, 6, 91-101), the current study employed a task that required active processing of the context word at test. In this version of the task, amnesic patients, like control participants, showed enhanced category exemplar priming when the context word associated with the target at study was reinstated at test. The finding of intact implicit memory for novel associations following hippocampal lesions in a task that requires flexible use of retrieval cues is inconsistent with a relational memory view that suggests that the hippocampus is critical for all forms of relational memory, regardless of awareness. Instead, it suggests that unaware memory for within-domain associations does not require MTL mediation.

MEDIAL TEMPORAL LOBE CONTRIBUTIONS TO FUTURE THINKING: EVIDENCE FROM NEUROIMAGING AND AMNESIA.

Following early amnesic case reports, there is now considerable evidence suggesting a link between remembering the past and envisioning the future. This link is evident in the overlap in neural substrates as well as cognitive processes involved in both kinds of tasks. While constructing a future narrative requires multiple processes, neuroimaging and lesion data converge on a critical role for the medial temporal lobes (MTL) in retrieving and recombining details from memory in the service of novel simulations. Deficient detail retrieval and recombination may lead to impairments not only in episodic, but also in semantic prospection. MTL contributions to scene construction and mental time travel may further compound impairments in amnesia on tasks that pose additional demands on these processes, but are unlikely to form the core deficit underlying amnesics' cross-domain future thinking impairment. Future studies exploring the role of episodic memory in other forms of self-projection or future-oriented behaviour may elucidate further the adaptive role of memory.

Medial temporal lobe damage causes deficits in episodic memory and episodic future thinking not attributable to deficits in narrative construction.

The medial temporal lobe (MTL) makes critical contributions to episodic memory, but its contributions to episodic future thinking remain a matter of debate. By one view, imagining future events relies on MTL mechanisms that also support memory for past events. Alternatively, it has recently been suggested that future thinking is independent of MTL-mediated processes and can be supported by regions outside the MTL. The current study investigated the nature and necessity of MTL involvement in imagining the future and tested the novel hypothesis that the MTL contributes to future thinking by supporting online binding processes related to narrative construction. Human amnesic patients with well characterized MTL damage and healthy controls constructed narratives about (1) future events, (2) past events, and (3) visually presented pictures. While all three tasks place similar demands on narrative construction, only the past and future conditions require memory/future thinking to mentally generate relevant narrative information. Patients produced impoverished descriptions of both past and future events but were unimpaired at producing detailed picture narratives. In addition, future-thinking performance positively correlated with episodic memory performance but did not correlate with picture narrative performance. Finally, future-thinking impairments were present when MTL lesions were restricted to the hippocampus and did not depend on the presence of neural damage outside the MTL. These results indicate that the ability to generate and maintain a detailed narrative is preserved in amnesia and suggest that a common MTL mechanism supports both episodic memory and episodic future thinking.

Implicit memory for novel associations between pictures: effects of stimulus unitization and aging.

Studies of implicit memory for novel associations have focused primarily on verbal materials and have highlighted the contribution of conceptually unitized representations to such priming. Using pictorial stimuli in a perceptual identification task, we examined whether new association priming can occur at a purely perceptual level. By manipulating the spatial contiguity of stimuli, we also evaluated whether such priming requires the creation of perceptually unitized representations. Finally, we examined the status of such priming in aging. In Experiment 1, we found that spatial contiguity of stimuli is not necessary for novel pictorial association priming to emerge, although such contiguity does enhance the magnitude of associative priming. In Experiment 2, we found that new association priming is age invariant, regardless of spatial contiguity. In Experiment 3, we provide additional evidence that pictorial association priming is perceptually based. These findings expand the scope and delineate the conditions of novel association priming and inform theories about the nature of implicit memory for new associations.

Impaired category fluency in medial temporal lobe amnesia: the role of episodic memory.

Memory tasks are often classified as semantic or episodic, but recent research shows that these types of memory are highly interactive. Category fluency, for example, is generally considered to reflect retrieval from semantic memory, but behavioral evidence suggests that episodic memory is also involved: participants frequently draw on autobiographical experiences while generating exemplars of certain categories. Neuroimaging studies accordingly have reported increased medial temporal lobe (MTL) activation during exemplar generation. Studies of fluency in MTL amnesics have yielded mixed results but were not designed to determine the precise contributions of episodic memory. We addressed this issue by asking MTL amnesics and controls to generate exemplars of three types of categories. One type tended to elicit autobiographical and spatial retrieval strategies (AS). Another type elicited strategies that were autobiographical but nonspatial (AN). The third type elicited neither autobiographical nor spatial strategies (N). Amnesic patients and control participants generated exemplars for eight categories of each type. Patients were impaired on all category types but were more impaired on AS and AN categories. After covarying for phonemic fluency (total FAS score), the N category impairment was not significant, but the impairment on AS and AN categories remained. The same results were obtained for patients with lesions restricted to the MTL and those with more extensive lesions. We conclude that patients' episodic memory impairment hindered their performance on this putatively semantic task. This interaction between episodic and semantic memory might partially account for fluency deficits seen in aging, mild cognitive impairment, and Alzheimer's disease.