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Cona, Giorgia (2012) Cognitive and electroencephalograohic markers of healthy and pathological aging. [Ph.D. thesis]

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Abstract (english)

The present thesis is composed of two main parts. In the first part, the effect of aging was investigated on performance and on event-related potentials (ERPs) associated with several goal-directed cognitive tasks. In the second part, cognitive and ERP changes were explored in patients with minimal hepatic encephalopathy, a syndrome characterized by cognitive and neurophysiological abnormalities in patients with liver cirrhosis.


It is a truism that as people grow older, performance on a large number of cognitive tasks declines. These age-sensitive tasks include simple and choice reaction times (RTs) tasks, tests of episodic memory, working-memory tasks, tasks involving executive functions, spatial and reasoning abilities, mental rotation (e.g., Kausler, 1991; Salthouse, 1991). Given that deficits are so widespread across the cognitive domains, it is reasonable to assume that a limited number of mechanisms might be responsible. Different theories tried to address this issue. Some of them suggested that cognitive deficits in aging are due to a reduction in the amount of attentional resources (Craik, 1986; Craik & Byrd, 1982), or a slowing down of processing speed (Salthouse, 1996), or a decline in the inhibitory control of working-memory contents (Hasher & Zacks, 1988).
One explanation that has recently gained some prominence is the increasing impairment of executive control with age, likely related to age-specific changes in prefrontal cortex (“theory of Cognitive Control”, also called “goal maintenance account”; Braver & West, 2008; Raz, 2000; West, 1996). Executive control is intended as the ability to represent, maintain and update goal information in order to exert control over behaviour and thoughts (Cohen et al., 1996). According to Miyake and collaborators (2000), executive control is not a single function, but is composed of several cognitive sub-processes, namely shifting, updating and inhibition.
To explore the role of executive control in explaining the age-related cognitive decline, the effect of cognitive aging was measured on those tasks involving high recruitment of such ability. Specifically, the first study of the present thesis (Experiment 1) investigated the age-related changes on a time-based prospective memory (PM) task, and focused on exploring the effect of aging on ERPs. Time-based PM refers to the ability of remembering to perform an action at a specific point in the future, (for example, remembering to attend an appointment at 3 pm; Brandimonte et al., 1996; Einstein & McDaniel, 2000; Kliegel et al., 2009). A fundamental process required for successfully accomplishing PM tasks is the ability to maintain and update the PM intentions (i.e., goal information) active in memory. Such ability, being impaired based on the “theory of cognitive control”, might be the factor determining the age-related alterations observed in time-based PM tasks. The analysis of ERPs elicited in time-based PM tasks is useful to test this hypothesis, and to better clarify the mechanisms responsible for age-related alterations in these kinds of tasks.
The second study focused on the relationship between executive control and cognitive aging by comparing performance of older and younger adults on a task in which the executive control load was manipulated. The task, called Inhibitory Control task (ICT; Bajaj et al., 2008a), is indeed composed of three different conditions, which varies for the executive resources needed. I expected that, if the executive control is the key factor responsible for cognitive impairment in aging, thus the deleterious effect of age on performance would be greater as the executive load increases. Moreover, ICT provides an investigation of the age-related alterations on ERPs associated with the different processes composing executive control, such as updating, shifting, and response inhibition (Miyake et al., 2000).
The two studies will be described in details below.

Experiment 1: ERP mechanisms underlying age-related alterations in Time-Based Prospective Memory.
There is a general agreement, across studies on PM, towards a deleterious effect of age on time-based PM performance (Bastin & Meulemans, 2002; McDaniel & Einstein, 1992; Park et al., 1997; see Henry, MacLeod, Phillips, & Crawford, 2004, for a review).
According to Craik’s theory (Craik, 1986), since in PM tasks there are no explicit prompts from the environment that instigate the retrieval of intention, individuals need to engage self-initiated and attentional demanding processes to retrieve the PM intentions. Given that aging is associated with a reduction in the availability of these attentional resources, thus PM performance would be altered in older people.
On the other hand, according to the “theory of cognitive control” (or “goal maintenance account”; Braver & West, 2008), older adults have difficulties in the maintenance of goal representations over an extended period. In the case of time-based PM, failure to maintain active the goal (i.e., the intention) would lead to failure to correctly execute the intended action.
Although a large number of studies investigated the impairment of time-based PM with aging, nevertheless none study has ever focused on neural activity underpinning such alterations. Therefore, in order to shed light on such poorly investigated issue, the present study explored the age-related alterations in the electrophysiological correlates of time-based PM tasks.
To this end, ERPs associated with ongoing task (i.e., a task executed concurrently with the PM task) were examined in 18 older and 15 younger adults and compared between a baseline block, in which individuals were required to perform merely the ongoing task; and a PM block, in which individuals were required to perform simultaneously the ongoing and the PM tasks. The ongoing task consisted in evaluating in five-letter strings whether the letters in second and fourth positions (target positions) were equal or different by pressing one of two possible keys. In the PM task, participants were required to remember to press the “PM key” every five minutes from the beginning of the block. To help them to estimating the passing of time, they had the opportunity to check the digital clock in any moment of the task by pressing another key. The ERPs were locked to ongoing trials (i.e., the strings of letter). Reaction times, accuracy and ERPs relative to ongoing trials were compared between the baseline and the PM block, for both younger and older adults. Moreover, the percentage of accuracy in PM task and the number of clock checks were recorded.
Concerning the behavioural results, older adults showed a lower percentage of accuracy in PM task respect to younger adults. Moreover, the older adults displayed a slowing down of RTs in the ongoing task, both in the baseline and in PM block, as compared to younger adults.
Concerning the ERPs of younger adults, the addition of a time-based PM task to an ongoing activity led to a sustained positive modulation of the ERPs elicited by the ongoing trials, mainly expressed over prefrontal and frontal regions. This frontal activity seems to reflect the load of maintaining the intention active in memory, as recently suggested (Cona et al., in press; West et al., 2011). On the other hand, in older adults these ERP modulations were more expressed over posterior regions. Interesting, a difference in the ERP amplitude between baseline and PM block was observed over prefrontal sites in younger adults (with the ERPs being more positive in PM block), but not in older adults. At first glance, the absence of the prefrontal mofulation in older adults seems to reflect their difficulties in keeping the PM intention in mind, as suggested by the “theory of cognitive control” (Braver & West, 2008).
Nevertheless, the exploration of the ERP differences as observed between the two groups in the baseline block allowed to better clarify the mechanisms responsible of these age-related changes in PM. Indeed in baseline block, compared to younger adults, older adults showed a lower P300 over parietal regions, and a higher P300 over prefrontal regions. The anteriorisation of the P300 shown by older adults has been well documented in literature (Daffner et al., 2006; 2011), and it is supposed to reflect the greater recruitment of attentional resources to compensate for olders’ difficulties in the ongoing task.
Taken together, these results suggest that older adults had difficulties already in the baseline block, and cope with such difficulties by recruiting additional frontal resources (as reflected by the anteriorisation of P300). If too many resources were allocated to perform the ongoing task, then fewer resources would be available to adequately maintain the intentions in memory, leading to an impaired PM performance. Therefore, it seems more reasonable that the decline in executive control, required for intention maintenance, is not the primary cause of the age-related changes in PM tasks, but rather is itself the consequence of a reduced amount of available resources, as postulated by Craik’s theory (1986).

Experiment 2: Influence of aging on ERP correlates of
executive control processes.
According to the “theory of cognitive control” (Braver & West, 2008), an age-related impairment in executive control is hypothesized to determine specific decrements in those cognitive tasks that are more demanding for that function. In order to test this prediction, we adopted the Inhibitory Control task (ICT; Bajaj et al., 2008a). During the ICT, a continuous stream of letters is presented, very quickly, one after the other. In the first part of the task, it is required to respond by pressing a key only to the target letters (i.e., “X” and “Y,”). Trials containing a target letter are labelled as Detect trials. In the second part, it is required to respond whenever the target letters are alternated (Go trials), as when an “X” is preceded by a “Y”, or vice versa, regardless of the irrelevant letters presented between them. In contrast, it must withhold response if target letters are repeated (Nogo trials), as when an “X” precedes another “X”, or a “Y” precedes another “Y”. In light of this, ICT includes trials requiring different demands of executive control. Detect trials requires to merely pay selective attention and to respond to specific stimuli. These trials are relatively low demanding in terms of executive control. Go trials are more demanding, implying the process of working memory updating. Finally, Nogo trials are the highest demanding trials since imply not only an updating process but also inhibitory control of response. According to the theory of control, differences on ICT performance between younger and older adults should be lowest in detect trials, intermediate in go trials and greatest in nogo trials.
Furthermore, this study was aimed at investigating the effect of age on the different processes composing the executive control (Miyake et al., 2000). Therefore it was explored the influence of aging on peak latency and amplitude of P3b, nogo-P3 and RON (i.e., reorienting negativity) components, which reflect updating, inhibition, and shifting processes, respectively. In order to better dissociate the ERP components related to these different processes, a partial least square (PLS) analysis was run. Seventeen younger and sixteen older adults performed the ICT.
Against the formulated predictions, older adults exhibited a worse performance in all kinds of trial, as from detect trials to nogo trials. More importantly, the age effect did not interact with the type of trials, hence was independent from the degree of executive control required to perform them. This means that executive control, when formulated as a unitary construct responsible for the age-related deficits in cognition, does not seem to be the elective factor for explaining the deficits shown in ICT task. In line with behavioural results, older adults showed a delay in all the ERP components studied (P3b, N2, RON, nogo-P3), regardless of the type of trial. These age-related alterations in the latency of the ERPs seem to reflect a slowing of speed of cognitive processing in the elderly individuals. Such an idea gives support to Sathouse's theory (Salthouse, 1996), which assumed that age-related cognitive decline might be due to a general reduction in the speed of processing.
Another relevant finding consists in the fact that the RON components were found particularly sensitive to aging. Specifically, these components, reflecting attentional shifting (Berti et al., 2008), were shown delayed and reduced in older adults. To my knowledge, only one study has investigated the age-related alterations in the RON components before, but utilizing an auditory distraction-paradigm (Horváth et al., 2009). Thus, the present study extended the results obtained in the work by Horváth, suggesting that the age-related impairment of attentional shifting occurred not only after distracter stimuli (as found by Horváth), but also after task-relevant ones. It suggests that in older adults shifting mechanism of attention take longer and is more effortful, probably because they are still engaged in processing the previous stimulus. Summarizing, electrophysiological and behavioural data converged in revealing that age-related cognitive impairment might be, at least partially, attributable to a general slowing of information processes. Indeed, coherently with the review by Verhaegen (2011), reduction on processing speed seems to explain cognitive deficits in elderly better than deterioration in executive control, when this is conceptualized as a unitary construct. On the other hand, a subprocess of executive control, attentional shifting, resulted particularly affected by age, and it could be another candidate to explain multiple age-related cognitive alterations.

1° Part: Conclusions
Although the present studies utilized different paradigms and tasks, they converged in revealing that executive control does not play a crucial role in determining the age-related deficits seen in these tasks. Rather, a decline in more basic, or lower-level, mechanisms seems to be the key factor to explain the multitude of age-related cognitive deficits. Specifically, the analysis of the ERPs allowed to highlight that age-related alterations were more likely due to a reduction: 1) in the amount of available resources and 2) in processing speed.
The age-related alterations concerned mainly ERPs over prefrontal regions and were they were mainly expressed as delay in the ERP latencies. Interestingly, compensatory mechanisms in older adults were also observed, and were reflected in the increase of amplitude of several components (respect to the younger adults). This led to the suggestion that aging does not simply mean cognitive and neural decline, but may also involve adaptive cognitive and neural responses.


Hepatic encephalopathy (HE) is a neuropsychiatric syndrome occurring in acute or chronic liver failure. The detection of the first, sometimes apparently negligible, signs of hepatic encephalopathy is greatly important since this condition, called minimal hepatic encephalopathy (MHE; Ferenci et al., 1998), impinges on the health-related quality of life (Groeneweg et al., 1998; Zhou et al. 2009) and it is likely to affect driving ability (Wein et al., 2004). Furthermore, it has a negative prognostic value in relation to the occurrence of both bouts of overt hepatic encephalopathy and death (Amodio et al., 1999; Romero-Gomez et al., 2007). The profile of MHE is characterized by cognitive alterations that involve selective attention and executive functions, visuomotor ability, psychomotor speed, response inhibition, and response selection (Amodio et al., 2005). MHE also causes brain dysfunction detectable by slowing of the electroencephalogram (EEG) and prolonged ERPs, such as P300 (Amodio et al., 2005; Weissenborn et al., 2005). Therefore, where possible, the diagnosis of MHE is preferably based on a combination of psychometric and neurophysiological/psychophysiological tools.
The inhibitory control task (ICT) has been recently proposed as a simple diagnostic tool for MHE (Bajaj et al., 2007; 2008a). However, its applicability to different populations of patients with cirrhosis and its relation to other measures of MHE need to be confirmed. Therefore, Experiment 3 was designed to address this issue and was aimed at assessing the specificity and sensitivity of ICT for the diagnosis of MHE. The Experiment 4 focused on the effect of MHE on the ERPs elicited by ICT, in order to highlight cognitive and electrophysiological alterations characterizing MHE.
In order to further investigate the electrophysiological alterations of MHE, another study (Experiment 5) explored the intra-individual variability (IIV) of P300 parameters (i.e., latency and amplitude) in cirrhotic patients with MHE. There is an increasing interest in IIV of cognitive performance (e.g., of RTs) within the field of cognitive neuroscience (MacDonald et al., 2006), since IIV has been widely considered to be a behavioral indicator of compromised neural mechanisms (e.g., Hultsch, et al., 2000). Nevertheless, studies establishing links between intra-individual variability in behavioral and brain responses are sparse, with most evidence being indirect. MHE seems to be a suitable model of pathology for studying this relation, given that patients with MHE showed increased IIV of RTs (Elssas et al., 1985; Schiff et al., 2006).
Therefore, in Experiment 5, single-trial P300 parameters, obtained by means of a single-trial Bayesian estimation technique (D’Avanzo et al., 2011), were estimated to investigate the electrophysiological correlates of IIV of response speed and the relation between P300 parameters and RTs in normal individuals and in a population of patients with and without MHE.

Experiment 3 and 4:
The ICT as a suitable tool for detecting cognitive and ERP alterations in patients with liver cirrhosis.
In Experiment 3, seventy-five patients with cirrhosis and 55 healthy controls underwent the ICT in 2 reference centers for the study of hepatic encephalopathy. Patients were evaluated for MHE by psychometric hepatic encephalopathy score (PHES) and spectral electroencephalogram analyses. Performance on go and nogo trials was compared between the two groups. Patients with cirrhosis exhibited a higher number of errors in nogo trials (i.e., lures), and lower accuracy in go trials, as compared with controls. However, the number of lures was comparable among patients with and without MHE. Importantly, an inverse relation between accuracy in go trials and number of lures was shown when the go accuracy was particularly low. However this is not surprising: a low accuracy in go trials indicates that many trials had a missing response (in go trial an error is a missed response), but if a participant commits many missing responses, he/she is more likely to “perform” correctly on nogo trials (hence to not respond when actually it is required to not respond). In light of this, the low number of error in nogo trials is a spurious effect. Hence, a new variable (weighted lures) was codified, adjusting the number of lures based on go accuracy. This variable distinguished between patients with and without MHE. However, accuracy in go trials alone was as effective as a stand-alone variable. Therefore, testing inhibition (lures) does not seem to be superior to testing attention and working memory updating (go accuracy) for the detection of MHE.
In Experiment 4 the electrophysiological alterations related to cirrhosis were investigated in the ICT task by comparing ERPs in cirrhotic patients with MHE (N=13), without MHE (N=18) with ERPs in healthy controls (N=17). Specifically, the ERPs in detect, go and nogo trials were measured, reflecting processes of selective attention, working memory updating, and inhibition, respectively. Data were further analysed by means of a PLS analysis, was particularly suited to dissociate the ERP correlates of the different subprocesses. Findings from ANOVA and PLS analysis converged in showing selective alterations of the ERPs on detect trials in patients with MHE. Specifically these included a reduction in P3a amplitude over frontocentral sites and a delay in the P3b latency. Since detect trials involve principally attentional processes, alterations on these trials may indicate that MHE is associated with an impairment of low-level cognitive abilities, such as attention. This result corroborated the claim of Experiment 3, concerning the appropriateness to test for low-level abilities (i.e., attention) before, or together with, testing for high-level abilities (i.e., inhibition) for the diagnosis of MHE (Amodio et al., 2010). The second main, and unexpected, finding was the enhancement of several ERP components (namely, the N2 and nogo-P3) in cirrhotic patients without MHE. These electrophysiological changes might be a compensatory mechanism, reflecting the allocation of additional executive resources for overcoming the difficulties of the task (indeed, also patients without MHE had a reduction of P3a, which is an index of attentional processes).

Experiment 5: The IIV of P300 as an index for detecting neural dysfunctions in patients with liver cirrhosis
In patients with cirrhosis, an increased intra-individual variability of RTs has been described and qualified as a potential early sign of brain dysfunction (Schiff et al., 2006). Unfortunately, a neural counterpart of this phenomenon was not obtained yet. However, since a reduction in the amplitude of P300 has been observed in this patient population, it is possible to hypothesize that P300 amplitude reduction depends, at least in part, on the increased variability of single-trial P300 latency (as evidenced in other pathologies; e.g., Hultsch et al., 2000). Moreover, single-trial analysis might clarify the relation between RTs and P300 parameters, and evidence how this relation changed under pathological conditions, such as MHE.
EEG was recorded during the execution of a choice reaction time task (i.e., Simon task) in 14 cirrhotic patients with MHE (diagnosed on paper & pencil tests plus EEG), 15 cirrhotic patients without MHE and 14 healthy controls matched for age and educational level. Single-trial P300 amplitude and latency, together with their standard deviation, were obtained using a non-parametric bayesian estimation method. P300 was also measured with the classical method of averaging. RTs distribution and its relation with single-trial P300 amplitude and latency were analysed.
In cirrhotic patients, RTs were slower and more variable compared to those of controls. An increased variability in P300 latency was also detected. Linear multiple regression analysis revealed that average-based P300 amplitude reduction was predicted both by standard deviation of single-trial P300 latency and by single-trial P300 mean amplitude.
These results indicate that average-based P300 amplitude reduction in cirrhotic patients with MHE depends on both an increased variability of single-trial P300 latency, and a reduction in single-trial P300 amplitude. Interestingly, we also found that P300 latency increased and amplitude decreased in parallel with increasing RTs in normal participants, but not in cirrhotic patients with MHE. Thus, another sign of neural alteration might be the weaker relationship between RTs and P300 parameters observed in patients with MHE.
In summary, the present study suggests that, under normal conditions, a relation between P300 and RTs is detectable and the P300 is stable across trials; in contrast, when the brain does not function properly, as observed in patients with MHE, the relation between P300 and RTs vanishes, and neural responses become more variable.

2° Part: Conclusions
The use of ICT task provided several insights concerning the neural markers of MHE. Specifically, patients with MHE showed a prolongation and a reduction of the P300 components elicited in the detect trials of ICT task, reflecting deficits in selective and sustained attention. On the other side, patients without MHE displayed an enhancement of several ERP components (i.e., N2 and P3-nogo), which might reflect a compensatory neural mechanism.
The Experiment 5 better clarified the profile of P300 in cirrhotic patients. Indeed, such patients, especially those with MHE, showed an increased intra-individual variability of the P300 latency, which may contribute to the reduction of its amplitude.

The ERP technique was revealed to be a powerful tool to explore neural alterations underlying both the healthy and pathological aging. Interestingly, several patterns of ERP alterations were shared by older individuals and cirrhotic patients (e.g., the delay in several ERPs, or a ‘paradoxical’ enhancement of other components, such as N2). Such ERP alterations highlighted that 1) age- and MHE-related deficits in higher-level cognitive tasks might be due to alterations in lower-level functions or mechanisms, including attention deficits, the reduction of available resources or processing speed; 2) brain activity of older people and cirrhotic patients without MHE was similarly characterized by compensatory mechanisms, recruited to cope with the difficulties of the tasks

Abstract (italian)

La presente tesi si compone di due parti principali. Nella prima parte è stato studiato l’effetto dell’età sulla performance e sui potenziali evento-relati (ERP) elicitati in differenti compiti cognitivi. Nella seconda parte sono stati esplorati i cambiamenti elettrofisiologici (i.e., alterazioni a livello di ERP) e cognitivi che caratterizzano l’encefalopatia epatica minima (MHE), una sindrome neuropsichiatrica conseguente a cirrosi epatica.

All’avanzare dell’età, le persone mostrano difficoltà in diversi compiti cognitivi. Tali compiti comprendono ad esempio compiti di tempi di reazione (TR) semplice o di scelta, test di memoria episodica, compiti di working memory o che coinvolgono funzioni esecutive, abilità spaziali e di ragionamento, test di rotazione mentale (e.g., Kausler, 1991; Salthouse, 1991).
Dato che tali deficit sono così diffusi tra i diversi domini cognitivi, è ragionevole assumere che essi dipendano da un’alterazione a carico di un ristretto numero di meccanismi. Diverse teorie si sono occupate di rispondere a tale questione. Alcune di queste hanno suggerito, ad esempio, che l’invecchiamento cognitivo sia associato ad una riduzione nella quantità di risorse attenzionali disponibili (Craik, 1986; Craik & Byrd, 1982), ad un rallentamento nella velocità di elaborazione (Salthouse, 1996), o ad un declino nel controllo inibitorio delle informazioni contenute nella working memory (Hasher & Zacks, 1988).
Una spiegazione cha ha recentemente ricevuto largo consenso sostiene che alla base delle alterazioni cognitive legate all’età vi sia una disfunzione a livello di controllo esecutivo, probabilmente dovuta a cambiamenti a carico della corteccia prefrontale (“teoria del controllo cognitivo” conosciuta anche come “ipotesi del mantenimento degli obiettivi”; Braver & West, 2008; Raz, 2000; West, 1996). Per controllo esecutivo si intende la capacità di rappresentare, mantenere e aggiornare gli obiettivi in memoria al fine di esercitare un controllo sui pensieri e sul comportamento (Cohen et al., 1996). Sulla base del lavoro di Miyake e collaboratori (2000), il controllo non sembra essere una funzione unitaria, ma è composta da diversi sotto-processi cognitivi, quali lo shifting, l’aggiornamento nella working memory e l’inibizione.
Per esaminare il ruolo che ha il controllo esecutivo nello spiegare il declino cognitivo legato dell’invecchiamento, è stato testato l’effetto dell’età in quei compiti che sono stati dimostrati richiere un alto coinvolgimento di controllo esecutivo. In particolare, il primo studio di questa tesi (Esperimento 1) ha esaminato i cambiamenti, legati all’età, in un compito di memoria prospettica (MP) basata sul tempo, focalizzandosi sull’analisi di quelle modulazioni ERP che rifletterebbero il declino della MP nell’invecchiamento. La memoria prospettica basata sul tempo si riferisce infatti all’abilità di ricordarsi di eseguire un’azione in un particolare momento nel futuro (ad esempio, ricordarsi di andare ad un appuntamento alle tre; Brandimonte et al., 1996; Einstein & McDaniel, 2000; Kliegel et al., 2009). Un processo che è fondamentale per eseguire appropriatamente i compiti prospettici è il mantenimento e l’aggiornamento delle intenzioni prospettiche in memoria (che rappresentano altresì gli obiettivi del compito prospettico). Tali processi di mantenimento, essendo alterati nell’invecchiamento secondo la teoria del controllo cognitivo, potrebbero essere quindi il fattore chiave nel determinare le alterazioni osservate nei compiti di MP. L’analisi degli ERP elicitati dal compito prospettico si è rivelata utile per testare tale ipotesi, e per chiarire quali siano i meccanismi responsabili del declino in questo tipo di compiti.
Il secondo studio ha indagato la relazione tra controllo esecutivo e invecchiamento cognitivo confrontando la prestazione di individui giovani e quella di individui più anziani in un compito in cui veniva variato il carico di controllo esecutivo tra le condizioni. Il compito, chiamato Inhibitory Control Task (ICT) (Bajaj et al., 2008a) è, infatti, composto da tre differenti condizioni, che differiscono per le risorse esecutive necessarie. Se il controllo esecutivo è il fattore chiave nel determinare il deterioramento cognitivo osservato nei diversi compiti, allora l’effetto dell’età sulla performance all’ICT dovrebbe essere tanto maggiore quanto più elevato è il grado di controllo esecutivo richiesto. Inoltre, l’ICT ha permesso di studiare le alterazioni legate all’età negli ERP associati ai differenti meccanismi che compongono il controllo esecutivo, ovverosia l’aggiornamento nella working memory, l’updating e l’inibizione (Miyake et al., 2000).
I due studi saranno qui sotto descritti in dettaglio:

Esperimento 1: Meccanismi ERP sottostanti alle alterazioni, legate all’età, nella memoria prospettica basata sul tempo.
Esiste un generale consenso, tra gli studi sulla MP, riguardo all’effetto deleterio che ha l’invecchiamento sulle prestazioni in compiti di MP basata sul tempo (Bastin & Meulemans, 2002; McDaniel & Einstein, 1992; Park et al., 1997; vedere anche Henry, MacLeod, Phillips, & Crawford, 2004, per una rassegna).
Secondo la teoria di Craik (1986), poiché nei compiti di MP non ci sono espliciti suggerimenti dall’ambiente che aiutano il recupero dell’intenzione, gli individui necessiterebbero di un maggior reclutamento di processi attenzionali e auto-iniziati per recuperare le intenzioni. Dato che l’invecchiamento è associato ad una riduzione nella disponibilità di tali risorse attenzioni, ciò determinerebbe un’alterazione nella prestazione dei compiti di MP negli individui più anziani.
Dall’altra parte, secondo la teoria del controllo cognitivo (o anche detta “ipotesi del mantenimento degli obiettivi”; Braver & West, 2008), gli anziani avrebbero delle difficoltà nella rappresentazione e nel mantenimento degli obiettivi nel corso del tempo. Nel caso della MP basata sul tempo, i deficit nel mantenere attivi gli obiettivi (cioè le intenzioni) porterebbe ad un fallimento nell’eseguire con successo l’azione intesa.
Sebbene un elevato numero di studi abbia esaminato come la MP basata sul tempo declini con l’età, tuttavia nessuno studio si è mai occupato finora di indagare l’attività neurale alla base di tale declino. Per tale motivo, il presente studio ha avuto lo scopo di esplorare le alterazioni legate all’età dei meccanismi elettrofisiologici alla base della MP basata sul tempo.
A tal fine, gli ERP associati ad un compito detto ongoing (i.e., un compito eseguito simultaneamente al compito prospettico) sono stati analizzati in 18 anziani e di 15 giovani e sono stati confrontati tra due diversi blocchi: il blocco di baseline e il blocco prospettico. Nel blocco di baseline veniva chiesto ai partecipanti di eseguire solamente il compito ongoing, mentre nel blocco prospettico si chiedeva di eseguire, assieme al compito ongoing, anche il compito di MP. Il compito ongoing consisteva nel valutare, all’interno di stringhe di cinque lettere, se le lettere in seconda e quarta posizione fossero uguali o diverse premendo con la mano destra uno di due possibili tasti. Nel compito di MP basata sul tempo, ai partecipanti era richiesto di premere un tasto ogni 5 minuti a partire dall’inizio del blocco prospettico. Per aiutarli nella stima del tempo, era stata data loro la possibilità di controllare l’orologio (che sarebbe comparso sullo schermo qualora avessero premuto un ulteriore tasto). Gli ERP analizzati erano elicitati dalla comparsa dello stimolo ongoing (i.e., la stringa di lettere). I TR, l’accuratezza e gli ERP nelle prove ongoing sono stati analizzati confrontando il blocco di baseline e quello prospettico, sia nei giovani che negli anziani. Inoltre sono stati analizzati sia la percentuale di accuratezza nel compito prospettico che il numero di controlli dell’orologio.
Per quanto riguarda i risultati comportamentali, gli anziani mostravano una percentuale di accuratezza inferiore nel compito prospettico rispetto ai giovani. Inoltre gli anziani hanno mostrato un aumento dei TR al compito ongoing rispetto ai giovani, sia nella baseline che nel blocco prospettico.
A livello di dati elettrofisiologici, i giovani hanno mostrato delle modulazioni positive e sostenute degli ERP elicitati dagli stimoli ongoing dovute all’aggiunta del compito prospettico, che erano espresse maggiormente sopra le regioni frontali e prefrontali. Tali modulazioni riflettevano il carico nel mantenere le intenzioni attive in memoria, come recentemente suggerito (Cona et al., in press; West et al., 2011). Dall’altra parte, negli anziani, tali modulazioni erano maggiormente espresse sopra le regioni posteriori. È infatti interessante notare che i giovani, ma non gli anziani, mostravano una maggiore positività degli ERP nel blocco prospettico rispetto alla baseline a livello di siti frontopolari. Ad un primo sguardo, l’assenza della modulazione prefrontale negli anziani sembra riflettere la loro difficoltà nel mantenere in memoria le intenzioni prospettiche, in accordo con la teoria del controllo cognitivo (Braver & West, 2008). Tuttavia, l’analisi delle differenze ERP tra i due gruppi (già nella baseline) ha permesso di comprendere meglio quale fosse il meccanismo responsabile di questo peggioramento nella performance prospettica. Infatti nel blocco di baseline, se confrontati con i giovani, gli anziani mostravano una P300 meno ampia sopra le regioni parietali, e più ampia sopra le regioni prefrontali. L’anteriorizzazione della P300 negli anziani è un fenomeno già ben documentato in letteratura (Daffner et al., 2006; 2011) e sembra indicare il reclutamento di un maggior numero di risorse per compensare le difficoltà nell’eseguire il compito ongoing.
In generale, tali risultati suggeriscono che gli anziani hanno difficoltà già nel blocco di baseline, e che affrontano tali difficoltà reclutando risorse frontali addizionali (come indicato dall’anteriorizzazione della P300). Se troppe risorse sono reclutate per eseguire il compito ongoing, allora ne rimarrebbero meno per mantenere adeguatamente le intenzioni in memoria e ciò determinerebbe una performance peggiore al compito prospettico. Sembra quindi più ragionevole assumere che il declino nel controllo esecutivo, richiesto per mantenere le intenzioni in memoria, non sia la causa primaria dei cambiamenti nei compiti prospettici, ma piuttosto sia a sua volta la conseguenza di una minor disponibilità di risorse cognitive, come postulato nella teoria di Craik (1986).

Esperimento 2: Influenza dell’invecchiamento sugli ERP associati ai processi legati al controllo esecutivo.
Secondo la teoria del controllo cognitivo (Braver & West, 2008), un declino del controllo esecutivo dovuto all’età produrrebbe deficit in quei compiti cognitivi che coinvolgono in misura maggiore proprio quella funzione. Al fine di studiare tale ipotesi, abbiamo utilizzato l’Inhibitory Control Task (ICT; Bajaj et al., 2008a). Durante l’ICT, una serie di lettere viene presentata, molto velocemente, una dopo l’altra. Nella prima parte del compito è richiesto di premere un tasto quando compare o la lettera X o la Y. Le prove in cui compaiono tali lettere vengono definite prove Detect. Nella seconda parte del compito è richiesto di premere il tasto solo quando la X e la Y si alternano (prove Go), ad esempio quando la X è preceduta da una Y, o vice versa, indipendentemente dalle lettere che vengono presentate tra le due lettere target. Quando le lettere X e Y si ripetono (ad esempio, una X è preceduta da un’altra X), allora è necessario inibire la risposta (prove Nogo). In tal modo, l’ICT include prove che richiedono un differente grado di controllo esecutivo per essere eseguite. Infatti, le prove Detect richiedono semplicemente di prestare attenzione selettiva e di rispondere a specifici stimoli, e coinvolgono per questo un basso grado di controllo esecutivo. Le prove Go implicano anche un processo di aggiornamento nella working memory. Infine, le prove Nogo richiedono il maggior carico di controllo esecutivo, coinvolgendo non solo un processo di aggiornamento ma anche l’inibizione di risposta. Sulla base della teoria del controllo cognitivo, le differenze tra giovani e anziani nella prestazione all’ICT dovrebbero essere minori nelle prove detect, intermedie nelle prove go e massime nelle prove nogo.
In aggiunta, questo studio aveva lo scopo di studiare l’effetto dell’età sui singoli processi che compongono il controllo esecutivo (Miyake et al., 2000). Per tale motivo, è stato studiato l’effetto dell’età sull’ampiezza e la latenza della P3b, della P3-nogo e della RON (reorienting negativity) che riflettono rispettivamente i processi di aggiornamento, inibizione e shifting. Al fine di dissociare meglio quali fossero le componenti ERP legate ai differenti processi studiati, è stata condotta la partial least square (PLS) analisi. Diciassette giovani e sedici anziani hanno partecipato all’esperimento ed eseguito l’ICT. Contro le predizioni formulate, i dati comportamentali hanno rivelato come gli anziani avessero una performance peggiore rispetto ai giovani in tutti i tipi di prove, quindi dalle prove detect alle prove nogo. È importante notare che l’effetto dell’età non interagiva con il tipo di prova, ed era quindi indipendente dal grado di controllo esecutivo necessario per eseguire quella data prova. Ciò indica che il controllo esecutivo, quando inteso come costrutto unitario, non sembra essere il fattore elettivo responsabile dei deficit mostrati dagli anziani nell’ICT. In linea con i risultati comportamentali, gli anziani hanno mostrato un ritardo in tutte le componenti ERP indagate (P3b, N2, RON, P3-nogo), indipendentemente dal tipo di prova esaminata. Questo ritardo nella latenza degli ERP legato all’età sembra riflettere un generale rallentamento dei processi cognitivi. Tale idea offre supporto alla teoria di Salthouse (1996), la quale assume che il declino cognitivo legato all’età sia dovuto ad una generale riduzione nella velocità di elaborazione.
Un altro risultato rilevante consiste nel fatto che le componenti RON sono risultate particolarmente sensibili all’invecchiamento. Tali componenti, che riflettono lo shifting attenzionale (Berti et al., 2008), erano ritardate e meno ampie negli anziani rispetto ai giovani. Solamente uno studio finora ha indagato le alterazioni, legate all’età, a carico delle componenti RON, ma utilizzando un paradigma uditivo di distrazione (Horváth et al., 2009). In questo senso il presente studio ha esteso i risultati ottenuti nello studio di Horváth, suggerendo che un declino nello shift attenzionale non avviene solo dopo stimoli distraenti (come evidenziato da Horváth) ma anche dopo stimoli rilevanti per il compito. Sembra, infatti, che negli anziani il meccanismo di shifting dell’attenzione sia più lento e dispendioso, probabilmente a causa del fatto che essi sono ancora occupati ad elaborare lo stimolo precedente.
Riassumendo, i dati elettrofisiologici e comportamentali convergono nel rivelare che il peggioramento nei compiti cognitivi associato all’invecchiamento potrebbe essere, almeno parzialmente, spiegabile da un rallentamento generale di elaborazione delle informazioni. Infatti, coerentemente con le conclusioni formulate nella rassegna di Verheagen (2011), una riduzione nella velocità dei processi sembra spiegare meglio i deficit cognitivi dell’anziano, rispetto ad un possibile deterioramento nel controllo esecutivo (quando inteso come processo unitario). Dall’altra parte, un sottoprocesso del controllo esecutivo, lo shifting attenzionale, sembra essere particolarmente sensibile all’età, e potrebbe quindi rappresentare un possibile candidato per spiegare la molteplicità di deficit nell’anziano.

1° Parte: Conclusioni

Sebbene i presenti studi abbiano utilizzato differenti paradigmi e compiti, tuttavia convergono nel mostrare come il controllo esecutivo non giochi un ruolo cruciale nel determinare i deficit cognitivi evidenziati in questi compiti. Piuttosto, un declino nei processi più di base sembra essere il fattore chiave per spiegare la molteplicità dei deficit cognitivi nell’invecchiamento. In particolare, l’analisi degli ERP ha permesso di evidenziare che i cambiamenti legati all’età sono più probabilmente dovuti ad una riduzione: 1) nella disponibilità delle risorse cognitive, 2) nella velocità di elaborazione.
Le alterazioni elettrofisiologiche legate all’età sembrano interessare in misura maggiore le modulazioni ERP osservate a livello di siti prefrontali, ed sono particolarmente espresse in termini di ritardo delle latenze. È interessante notare la presenza di meccanismi compensatori negli anziani, riflessi in un aumento nell’ampiezza di diverse componenti (rispetto ai giovani). Ciò suggerisce che l’invecchiamento non solo implica un declino cognitivo e neurale, ma coinvolge anche risposte cognitive e neurali adattive.

L’encefalopatia epatica è una sindrome neuropsichiatrica che può presentarsi in pazienti con cirrosi epatica. Il rilevamento dei primi, seppur lievi, segni dell’encefalopatia epatica è estremamente importante. Questa iniziale e subclinica condizione, chiamata encefalopatia epatica minima (MHE; Ferenci et al., 1998) ha infatti un impatto sulla qualità della vita (Groeneweg et al., 1998; Zhou et al. 2009) e sull’abilità di guida (Wein et al., 2004). Inoltre, ha un valore prognostico negativo in relazione alla probabilità di sviluppare episodi di encefalopatia conclamata, nonché di morte (Amodio et al., 1999; Romero-Gomez et al., 2007). Il profilo della MHE è caratterizzato da alterazioni cognitive che coinvolgono processi quali l’attenzione selettiva, le funzioni esecutive, l’abilità visuo-motoria, la velocità di elaborazione, l’inibizione e la selezione di risposta (Amodio et al., 2005). La MHE causa anche una disfunzione cerebrale comunemente rilevabile sia dal rallentamento dell’elettroencefalogramma (EEG) sia dal ritardo osservato nelle latenze degli ERP, tra cui la P300 (Amodio et al., 2005; Weissenborn et al., 2005). Quindi, quando possibile, la diagnosi di MHE dovrebbe essere preferibilmente basata su una combinazione di indici neuropsicologici/neurofisiologici.
L’Inhibitory Control Task (ICT) è stato recentemente proposto come un semplice strumento diagnostico per la MHE (Bajaj et al. 2007; 2008a). Tuttavia, la sua applicabilità a differenti popolazioni di pazienti con cirrosi, così come la sua relazione con altre misure di MHE necessitano di essere confermate. Per tali motivi, è stato condotto un esperimento (Esperimento 3) che aveva lo scopo di valutare la specificità e la sensibilità dell’ICT per la diagnosi della MHE.
L’Esperimento 4 si è invece focalizzato di indagare l’effetto della MHE sugli ERP elicitati dall’ICT, in modo tale da ottenere informazioni sulle alterazioni cognitive ed elettrofisiologiche caratteristiche della MHE.
A proposito delle alterazioni elettrofisiologiche legate alla MHE, un ulteriore esperimento (Esperimento 5) ha indagato la variabilità intra-individuale dei parametri della P300 (latenza e ampiezza) nei pazienti cirrotici con MHE. C’è un crescente interesse riguardo alla variabilità nella prestazione cognitiva (e.g., nei TR) nel campo delle neuroscienze cognitive (MacDonald et al., 2006) poiché la VII è stata largamente considerata un possibile indice comportamentale di meccanismi neurali compromessi (e.g., Hultsch et al., 2000). Tuttavia gli studi che hanno stabilito un legame tra la VII delle risposte comportamentali e quella delle risposte neurali sono ancora pochi. La MHE sembra un valido modello di patologia per studiare questa relazione poiché i pazienti con MHE mostrano un aumento nella variabilità dei TR (Elsass et al., 1985; Schiff et al., 2006).
Per tale motivo, nell’Esperimento 5, i parametri delle P300 misurati per ogni singola epoca, attraverso la tecnica di stima Bayesiana (D’Avanzo et al., 2011), sono stati esaminati per studiare il correlato elettrofisiologico della VII nella velocità di risposta. Inoltre sono stati esplorati i possibili cambiamenti nella relazione tra i parametri della P300 e dei TR che avvengono in pazienti con MHE.

Esperimenti 3 e 4: L’ICT come strumento adatto per rilevare le alterazioni cognitive ed elettrofisiologiche in pazienti con cirrosi epatica.
Nell’Esperimento 3, 75 pazienti con cirrosi e 55 controlli sani hanno eseguito l’ICT presso due centri di riferimento per lo studio dell’encefalopatia epatica. I pazienti venivano valutati per la MHE attraverso il Psychometric Hepatic Encephalopathy Score (PHES) e le analisi spettrali dell’EEG. La performance alle prove go e nogo è stata comparata tra i due gruppi. I pazienti con cirrosi presentavano un maggior numero di errori (i.e., lures) nelle prove nogo, e mostravano un’accuratezza peggiore anche nelle prove go, rispetto ai controlli. Tuttavia, il numero di lures era comparabile tra pazienti con e pazienti senza MHE. È importante notare come ci fosse una relazione inversa tra accuratezza nelle prove go e numero di errori, quando l’accuratezza nelle prove go era particolarmente bassa. Questo non è sorprendente: una bassa accuratezza alle prove go indica che molte di queste prove avevano una risposta mancante (infatti nelle prove go un errore consiste in una risposta mancante); tuttavia se un individuo commette tante risposte mancanti, allora è più probabile che “esegua” correttamente le prove nogo (le quali infatti prevedono una mancanza di risposta come ‘risposta’ corretta). In questo senso il numero basso di errori alle prove nogo è un fenomeno spurio. È stata quindi codificata una nuova variabile (weighted lures, o “lures pesati”), in cui il numero di lure veniva aggiustato per la percentuale di accuratezza nelle prove go. Tale variabile si è mostrata in grado di differenziare i pazienti con e i pazienti senza MHE. L’accuratezza nelle prove go si è rivelata comunque essere una valida misura anche quando veniva considerata da sola. Quindi, per rilevare segni di MHE, testare l’inibizione (lures) non sembra essere superiore rispetto al testare l’attenzione e l’aggiornamento nella working memory (accuratezza nelle prove go).
L’Esperimento 4 ha permesso di studiare le alterazioni elettrofisiologiche legate alla cirrosi epatica ed evidenziate nelle prove che compongono l’ICT. In tale studio, sono stati analizzati gli ERP confrontando pazienti cirrotici con MHE (N=13), senza MHE (N=18) e individui di controllo (N=17). In particolare sono stati esaminati gli ERP elicitati dalle prove detect, go e nogo, in quanto possono essere un indice dei processi di attenzione selettiva, working memory e inibizione, rispettivamente. I dati sono stati inoltre analizzati attraverso l’analisi PLS, la cui efficacia nell’identificare variabili latenti è particolarmente adatta per dissociare i correlati ERP dei diversi processi. I risultati ottenuti dall’ANOVA e dall’analisi PLS hanno mostrato alterazioni associate alla MHE che interessavano selettivamente gli ERP nelle prove detect. Specificatamente, queste erano rappresentate da una riduzione della P3a a livello di siti frontocentrali e da un ritardo della P3b. Poiché le prove detect coinvolgono principalmente processi attenzionali, le alterazioni evidenziate in tali prove potrebbero indicare un deterioramento delle abilità cognitive più di base, quali l’attenzione. Questo risultato corrobora la conclusione ottenuta nell’esperimento 3, che concerne l’appropriatezza di testare abilità più di base (come l’attenzione) prima, o assieme, alla valutazione delle abilità più di alto livello (i.e., l’inibizione). Il secondo principale, e inaspettato, risultato consiste nell’aumento (invece di una diminuzione) dell’ampiezza di diverse componenti (cioè la N2, la P3-nogo) in pazienti cirrotici senza MHE. Questi cambiamenti elettrofisiologici potrebbero essere un meccanismo compensatorio e riflettere l’allocazione di risorse esecutive addizionali per far fronte alle difficoltà nell’eseguire il compito (anche i pazienti senza MHE mostrano infatti una riduzione nella P3a, indice di deficit attenzionali).

Esperimento 5: La VII della P300 come indice per rilevare disfunzioni neurali in pazienti con cirrosi epatica.
In pazienti con cirrosi, un’aumentata VII dei TR è già stata descritta, ed è stata considerata un possibile indice precoce di disfunzione cerebrale (Schiff et al., 2006). Sfortunatamente, la controparte neurale di questo fenomeno non è stata ancora dimostrata. Tuttavia, siccome una riduzione dell’ampiezza della P300 è stata osservata in questa popolazione di pazienti, allora è possibile ipotizzare che tale riduzione dipenda, almeno in parte, da un’aumentata variabilità delle latenze della P300 tra le singole epoche (come evidenziato per altre patologie, e.g., Hultsch et al., 2000). Per tali motivi, l’aumentata variabilità della P300, se evidenziata, potrebbe essere anch’essa un valido indice di disfunzione neurale. Inoltre, l’analisi della P300 per ogni singola epoca ha permesso di indagare la relazione tra i TR e i parametri (i.e., ampiezza e latenza) della P300, e comprendere come tale relazione cambi nel caso di patologie quali MHE.
L’EEG è stato misurato durante l’esecuzione di un compito di reazione di scelta (compito Simon) in 14 pazienti con MHE (diagnosticata sulla base di test e alterazioni all’EEG), 15 pazienti senza MHE e 14 individui sani di controlli. L’ampiezza e la latenza della P300, assieme alla loro rispettiva deviazione standard, sono state ottenute attraverso un metodo non parametrico di stima bayesiana. La P300 è stata anche misurata con il classico metodo dell’averaging. Infine sono state analizzate la distribuzione dei TR e la sua relazione con i parametri della P300.
Nei pazienti con cirrosi, i TR erano più lenti e più variabili rispetto ai controlli. Un aumento nella variabilità della latenza della P300 è stato anche mostrato in tali pazienti. La regressione lineare multipla ha evidenziato come l’ampiezza della P300 – misurata con il metodo dell’averaging – era predetta sia dalla deviazione standard della latenza della P300, che dalla sua ampiezza (entrambe misurate con il metodo bayesiano). Ciò indica che una ridotta P300 nei pazienti con MHE potrebbe anche dipendere da un’aumentata variabilità nella latenza della stessa.
Inoltre, è stato mostrato come la latenza della P300 aumentava e l’ampiezza diminuiva all’aumentare dei TR nei controlli, ma non nei pazienti con MHE. Un altro segno di alterazione sembra quindi essere la più debole relazione tra parametri comportamentali e la P300, come osservato nei pazienti con MHE.
Riassumendo, il presente studio ha suggerito come in condizioni normali vi sia una stretta relazione tra TR e P300, e la P300 sia stabile tra le diverse prove. In contrasto, quando vi è una disfunzione cerebrale, come nel caso della MHE, la relazione tra i diversi parametri è meno forte, e le risposte neurali diventano più variabili.

2° Parte: Conclusioni
L’utilizzo dell’ICT ha fornito diverse evidenze riguardo ai marker cognitivi e neurali della MHE. Specificatamente, i pazienti con MHE hanno mostrato un rallentamento e un’attenuazione delle componenti della P300 nelle prove detect. Ciò sembra indicare deficit a carico dell’attenzione selettiva e sostenuta. Dall’altra parte, i pazienti senza MHE hanno evidenziato un aumento nelle ampiezze di alcune componenti (N2 e P3-nogo), che potrebbe riflettere un meccanismo neurale compensatorio.
Infine l’esperimento 5 ha evidenziato il profilo della P300 nei pazienti con cirrosi. Infatti, tali pazienti, e specialmente coloro che presentavano MHE, hanno mostrato un aumento nella variabilità della latenza della P300, che può aver contribuito alla riduzione della sua ampiezza.

La tecnica dell’analisi ERP si è rivelata uno strumento utile per esplorare le alterazioni cognitive e neurali sottostanti sia all’invecchiamento sano sia a una condizione patologica, quale la MHE. Sono stati osservati alcuni pattern di alterazioni elettrofisiologiche comuni tra le persone anziane e pazienti con cirrosi epatica (e.g., rallentamento delle componenti ERP, aumento di alcune componenti, quali la N2). Tali alterazioni hanno evidenziato come 1) i deficit legati all’invecchiamento o alla MHE evidenziati in compiti cognitivi complessi sembrano dipendere da alterazioni a carico di meccanismi più di base (come deficit attentivi, o rallentamento nell’elaborazione degli stimoli); 2) l’attività neurale sia di individui anziani sia di pazienti senza MHE è similmente caratterizzata da meccanismi compensatori, reclutati per affrontare le difficoltà nell’eseguire i compiti

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EPrint type:Ph.D. thesis
Tutor:Bisiacchi, Patrizia S.
Ph.D. course:Ciclo 24 > Scuole 24 > SCIENZE PSICOLOGICHE > PSICOBIOLOGIA
Data di deposito della tesi:26 January 2012
Anno di Pubblicazione:26 January 2012
Key Words:aging, prospective memory, executive control, inhibition, inhibitory control task, ERPs, event-related potentials, minimal hepatic encephalopathy, single-trial analysis,
Settori scientifico-disciplinari MIUR:Area 11 - Scienze storiche, filosofiche, pedagogiche e psicologiche > M-PSI/02 Psicobiologia e psicologia fisiologica
Struttura di riferimento:Dipartimenti > Dipartimento di Psicologia Generale
Codice ID:4540
Depositato il:24 Oct 2012 12:04
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