Neural substrates of time perception and impulsivity

Abstract

Several studies provide empirical evidence for the association between impulsivity and time perception. However, little is known about the neural substrates underlying this function. This investigation examined the influence of impulsivity on neural activation patterns during the encoding and reproduction of intervals with durations of 3, 9 and 18 s using event-related functional magnetic resonance imaging (fMRI). Twenty-seven subjects participated in this study, including 15 high impulsive subjects that were classified based on their self-rating. FMRI activation during the duration reproduction task was correlated with measures of two self-report questionnaires related to the concept of impulsivity (Barratt Impulsiveness Scale, BIS; Zimbardo Time Perspective Inventory, ZTPI). Behaviorally, those individuals who under-reproduced temporal intervals also showed lower scores on the ZTPI future perspective subscale and higher scores on the BIS. FMRI activation revealed an accumulating pattern of neural activity peaking at the end of the 9- and 18-s intervals within right posterior insula. Activations of brain regions during the reproduction phase of the timing task, such as those related to motor execution as well as to the ‘core control network’ – encompassing the inferior frontal and medial frontal cortices, the anterior insula as well as the inferior parietal cortex – were significantly correlated with reproduced duration, as well as with BIS and ZTPI subscales. In particular, the greater activation in these regions the shorter were the reproduced intervals, the more impulsive was an individual and the less pronounced the future perspective. Activation in the core control network, thus, may form a biological marker for cognitive time management and for impulsiveness.

Introduction

Empirical evidence suggests associations between impulsiveness, impulsive decision making, and an altered sense of time (Berlin and Rolls, 2004, Rubia et al., 2009, Wittmann et al., 2007). Although impulsivity in general can be characterized by an individual's rapid response without appropriate forethought (Sweitzer et al., 2008), different methods of assessment – ranging from questionnaires to various behavioral tasks – do not necessarily correlate (Carrillo-de-la-Peña et al., 1993, Gerbing and Patton, 1987). These dissociations imply that the concept of impulsivity consists of multiple components (Arce and Santisteban, 2006). Nevertheless, impulsivity can be defined as a pattern of unplanned actions without regard for the negative consequences that might follow, i.e. to prefer immediate gains over long-term consequences; this construct has been successfully linked to many psychiatric syndromes including substance use and dependence (Lane et al., 2003b, Moeller et al., 2001). We have proposed that impulsive choices such as opting for smaller and sooner rewards over larger but delayed rewards are due to the subjective overestimation of the duration of the delay (Wittmann and Paulus, 2008, Wittmann and Paulus, 2009). In particular, highly impulsive person process time differently, i.e. they overestimate duration. Delays are experienced as too high of a cost, which becomes apparent in premature responses, a decreased tolerance to delays, poor foresight and the selection of relatively smaller rewards that can be consumed earlier (Rubia et al., 2009). Impulsive patients from psychiatric populations devalue (discount) temporally delayed rewards more strongly than comparison subjects (Crean et al., 2000, Kirby et al., 1999). Moreover, a stronger present time perspective and a less pronounced future time perspective predicts impulsive behavior and drug use (Keough et al., 1999). Time perspective is a fundamental dimension in the construction of subjective time partitioning human experience into past, present, and future. Drug-dependent persons, who show stronger impulsive behavior in decision making, score significantly lower on a future orientation scale and their future perspective is less extended (Petry et al., 1998, Smart, 1968).

Regarding the estimation of duration in the seconds-to-minutes range, several studies have shown that impulsive individuals overestimate and under-produce time intervals. An under-production of an interval is indicative of an overestimation of time; if more time has passed subjectively for an individual she will indicate earlier that a given duration has passed (Melges and Fougerousse, 1966). Patients with borderline personality disorder as well as patients with orbitofrontal cortex lesions, individuals who are highly impulsive, under-produced and overestimated time intervals in the multiple seconds range (Berlin et al., 2004, Berlin and Rolls, 2004). Cocaine and methamphetamine dependent patients participating in an inpatient alcohol and drug treatment program overestimated the duration of a 53 s interval, estimates that were mediated by higher self-reported impulsivity (Wittmann et al., 2007). Sleep-deprived subjects, compared to when they were well rested, discounted delayed rewards more strongly and under-produced as well as under-reproduced time intervals of multiple seconds duration (Reynolds and Schiffbauer, 2004). Children with attention deficit hyperactivity disorder (ADHD) show an altered timing performance in several domains of time perception and at the same time show stronger discounting of delayed rewards (Barkley et al., 2001a, Smith et al., 2002), findings that have led some investigators to propose that impulsiveness can essentially be described as a deficit in temporal processing (Rubia et al., 2009).

There is considerable uncertainty on how and where in the brain time is processed (Rubia and Smith, 2004, Wittmann, 2009a, Wittmann, 2009b). The lack of agreement as to which mechanisms account for the perception of time is evident by the number of different psychological and neural models (Wittmann and van Wassenhove, 2009). While there is evidence suggesting that the processing of duration relies on the integrity of the whole brain (Coslett et al., 2009), specific neural models have been proposed for the perception of time in the milliseconds-to-seconds range. Among these models are the coincidence detection model using oscillatory signals in cortico-striatal circuits (Matell and Meck, 2004), generalized magnitude processing for time, space and number in the right posterior parietal cortex (Bueti and Walsh, 2009), event timing and temporal prediction in the cerebellum (Ivry et al., 2002), working memory related integration in the right prefrontal cortex (Lewis and Miall, 2006), as well as the integration of self- and body processes in the anterior insula (Craig, 2008, Craig, 2009a). Other investigators assume memory-loss components as intrinsic features in theoretical models of time perception (Staddon, 2005, Wackermann and Ehm, 2006), or propose that the amount of energy spent during cognitive processing defines the subjective experience of duration (Eagleman and Pariyadath, 2009). In a recent event-related functional magnetic resonance imaging (fMRI) study we reported that activation in the dorsal posterior insular cortex was linked to the perception of time in a duration reproduction task using intervals of 9 and 18 s (Wittmann et al., 2010b). Neural time-activity curves showed that activation in the posterior insula increased linearly during the encoding interval of the task (i.e., during presentation of the tone that had to be temporally reproduced). A similar linear increase in activation was seen during the reproduction interval of the task in the anterior insula, inferior frontal and medial frontal cortices bilaterally. We suggested that this accumulator-like activity in the posterior insula during the encoding interval might signify an integration of body signals over time that could be used to represent duration.

Since temporal processing deficits are assumed to be associated with impulsivity, neuroimaging studies of duration processing in impulsive individuals could provide insight into the neural basis of time perception and of impulsiveness. To this end we selected a subset of student subjects with large variability on self-rated impulsivity for a functional magnetic resonance imaging (fMRI) study while they completed a duration reproduction task that had been used in a preceding functional imaging study with healthy controls (Wittmann et al., 2010b). We related performance in the duration reproduction task and related brain activation with self-report measures of impulsiveness (Barratt Impulsiveness Scale; BIS) (Barratt et al., 1999), of the temporal perspective (Zimbardo Time Perspective Inventory; ZTPI) (Zimbardo and Boyd, 1999), and performance in a delay discounting task — all of which have been shown to be related to trait impulsiveness (Barkley et al., 2001b, Rubia et al., 2009). Subjects were selected on the basis that they were healthy young students with a wide range of trait impulsivity. We, therefore, conducted careful psychiatric and medical assessments to make sure that the students did not fulfill any DSM-IV criteria for psychiatric diagnoses.

Specifically, we examined whether trait impulsivity would relate to neural activation of accumulator-like activity in the posterior insula during the encoding of intervals in the timing task or whether impulsivity would relate to more frontal brain regions during the reproduction phase of the task. We used a task with three durations that had to be reproduced: 3 s, 9 s, and 18 s. The longest time interval is of a magnitude that has so far not been employed in an fMRI study with impulsive individuals. Most behavioral studies showing an overestimation of duration in impulsive individuals used intervals in the multiple-seconds-to-minutes range. With the choice of 9 s and 18 s intervals we compromised in having comparably long intervals and at the same time having a feasible duration for an fMRI setting. Moreover, in having both shorter and longer time intervals, we were able to specifically probe whether brain activation for the two longer durations correlates more with impulsivity measures than the shorter interval. Specifically, evidence suggests that temporal intervals up to around 3 s are governed by different mechanisms than intervals exceeding this approximate time range (Pöppel, 2009, Ulbrich et al., 2006).