Accumulation of neural activity in the posterior insula encodes the passage of time

Department of Psychiatry, University of California San Diego, 8939 Villa La Jolla Dr, Suite 200, La Jolla, CA 92037-0985, USA.
Neuropsychologia (Impact Factor: 3.3). 08/2010; 48(10):3110-20. DOI: 10.1016/j.neuropsychologia.2010.06.023
Source: PubMed


A number of studies have examined the perception of time with durations ranging from milliseconds to a few seconds, however the neural basis of these processes are still poorly understood and the neural substrates underlying the perception of multiple-second intervals are unknown. Here we present evidence of neural systems activity in circumscribed areas of the human brain involved in the encoding of intervals with durations of 9 and 18s in a temporal reproduction task using event-related functional magnetic resonance imaging (fMRI). During the encoding there was greater activation in more posterior parts of the medial frontal and insular cortex whereas the reproduction phase involved more anterior parts of these brain structures. Intriguingly, activation curves over time show an accumulating pattern of neural activity, which peaks at the end of the interval within bilateral posterior insula and superior temporal cortex when individuals are presented with 9- and 18-s tone intervals. This is consistent with an accumulator-type activity, which encodes duration in the multiple seconds range. Given the close connection between the dorsal posterior insula and ascending internal body signals, we suggest that the accumulation of physiological changes in body states constitutes our experience of time. This is the first time that an accumulation function in the posterior insula is detected that might be correlated with the encoding of time intervals.

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Available from: Marc Wittmann, Oct 05, 2015
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    • "Recordings in functional magnetic resonance imaging (fMRI) indicated that activity within the insular cortex increased continuously during the perception of duration (Wittmann et al., 2010, 2011). Moreover, the experience of temporal delay between external acoustic stimulation and the heart beat is related to anterior insula activation (Critchley et al., 2004). "
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    ABSTRACT: Recent research suggests that bodily signals and interoception are strongly related to our sense of time. Mindfulness meditators train to be aware of their body states and therefore could be more accurate at interval timing. In this study, n = 22 experienced mindfulness meditators and n = 22 matched controls performed both, an acoustic and a visual duration reproduction task of 8, 14, and 20 s intervals, while heart rate and skin conductance were continuously assessed. In addition, participants accomplished a heart beat perception task and two selective attention tasks. Results revealed no differences between meditators and controls with respect to performance in duration reproduction or attentional capacities. Additionally no group difference in heart beat perception scores was found. Across all subjects, correlational analyses revealed several associations between performance in the duration reproduction tasks and psychophysiological changes, the latter being also related to heart beat perception scores. Furthermore, former findings of linearly increasing cardiac periods and decreasing skin conductance levels during the auditory duration estimation task (Meissner and Wittmann, 2011) could be replicated, and these changes could also be observed during a visual duration reproduction task. In contrast to our earlier findings, the heart beat perception test was not related with timing performance. Overall, although experienced meditators did not differ from matched controls with respect to duration reproduction and interoceptive awareness, this study adds significantly to the emerging view that time perception is related to autonomic regulation and awareness of body states.
    Frontiers in Psychology 09/2015; 6:1215. DOI:10.3389/fpsyg.2015.01215 · 2.80 Impact Factor
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    • "Here, we show a correlation between activation responses in the anterior insula and RT during the TOP task (Fig. 5). This finding is also consistent with the accumulation function of the anterior insula, which postulates that our sense of time reflects the accumulation of physiological changes in body states (Wittmann et al. 2010; Bueti and Macaluso 2011). The anterior insula is also involved in TD learning (Sutton and Barto 1981; Sutton 1988) during Pavlovian conditioning. "
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    ABSTRACT: Temporal prediction (TP) is needed to anticipate future events and is essential for survival. Our sense of time is modulated by emotional and interoceptive (corporal) states that are hypothesized to rely on a dopamine (DA)-modulated "internal clock" in the basal ganglia. However, the neurobiological substrates for TP in the human brain have not been identified. We tested the hypothesis that TP involves DA striato-cortical pathways, and that accurate responses are reinforcing in themselves and activate the nucleus accumbens (NAc). Functional magnetic resonance imaging revealed the involvement of the NAc and anterior insula in the temporal precision of the responses, and of the ventral tegmental area in error processing. Moreover, NAc showed higher activation for successful than for unsuccessful trials, indicating that accurate TP per se is rewarding. Inasmuch as activation of the NAc is associated with drug-induced addictive behaviors, its activation by accurate TP could help explain why video games that rely on TP can trigger compulsive behaviors.
    Cerebral Cortex 11/2014; DOI:10.1093/cercor/bhu269 · 8.67 Impact Factor
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    • "The first was the identification of DMN activity as a reduction in gamma power within frontal-midline regions during a time-production (TP) task compared with resting state. The choice of the TP task to index a reduction in DMN activity was based on previous work showing that timing systematically activates several cortical regions, including: (i) attentional regions, such as the right parietal and dorsolateral prefrontal cortex (DLPFC) (reviewed by Walsh, 2003; Oliveri et al., 2009; Wittmann, 2009), consistent with a great body of behavioral studies showing that attention is mandatory for accurate timing (reviewed by Brown, 1997); (ii) the supplementary motor area (SMA) (Coull and Nobre, 1998; Ferrandez et al., 2003; Coull, 2004; Macar et al., 2004) and (iii) the anterior insular cortex (Craig, 2002, 2009; Wittmann et al., 2010). The right parietal and SMA regions are part of the dorsal attention network (Corbetta et al., 2008), comprising a task-activated network, also named the 'extrinsic system', suggested to be antagonistic to the task-inactivated DMN (Fox et al., 2005; Golland et al., 2007; Tian et al., 2007) and the DLPFC and anterior insular cortex are part of the frontoparietal control system, interposed between the 'intrinsic' and 'extrinsic' systems (Vincent et al., 2008) and possibly adjudicating between these two potentially competing brain systems (Vincent et al., 2008; Spreng et al., 2010; Smallwood et al., 2012). "
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    ABSTRACT: The default mode network (DMN) has been largely studied by imaging, but not yet by neurodynamics, using electroencephalography (EEG) functional connectivity (FC). mindfulness meditation (MM), a receptive, non-elaborative training is theorized to lower DMN activity. We explored: (i) the usefulness of EEG-FC for investigating the DMN and (ii) the MM-induced EEG-FC effects. To this end, three MM groups were compared with controls, employing EEG-FC (–MPC, mean phase coherence). Our results show that: (i) DMN activity was identified as reduced overall inter-hemispheric gamma MPC during the transition from resting state to a time production task and (ii) MM-induced a state increase in alpha MPC as well as a trait decrease in EEG-FC. The MM-induced EEG-FC decrease was irrespective of expertise or band. Specifically, there was a relative reduction in right theta MPC, and left alpha and gamma MPC. The left gamma MPC was negatively correlated with MM expertise, possibly related to lower internal verbalization. The trait lower gamma MPC supports the notion of MM-induced reduction in DMN activity, related with self-reference and mind-wandering. This report emphasizes the possibility of studying the DMN using EEG-FC as well as the importance of studying meditation in relation to it.
    Social Cognitive and Affective Neuroscience 11/2014; 9(10). DOI:10.1093/scan/nst153 · 7.37 Impact Factor
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