Hoerl & McCormack (H&M) have proposed to distinguish between “temporal updating system” and “temporal reasoning system” to interpret comparative and developmental psychological findings about temporal information processing. On the one hand, we understand that their view is compelling, especially from the viewpoint of developmental psychology. On the other hand, they stayed away from discussing the neural correlates that may underlie the two systems. They did not discuss how the proposed view might influence interpretations of findings from clinical studies on temporal processing in neuropsychiatric disorders, either. Hence, we will discuss plausible neural correlates, which may underlie the temporal updating/reasoning systems, and dysfunction of these systems, which may yield altered temporal processing in neuropsychiatric disorders. The argument is based on empirical evidence obtained in behavioral and neuroimaging studies (including our own) conducted in humans.
Previously, we performed a few neuroimaging studies to gain insight into the neural substrates underlying temporal information processing in healthy humans (Aso et al. Reference Aso, Hanakawa, Aso and Fukuyama2010; Bushara et al. Reference Bushara, Hanakawa, Immisch, Toma, Kansaku and Hallett2003; Ohki et al. Reference Ohki, Gunji, Takei, Takahashi, Kaneko, Kita, Hironaga, Tobimatsu, Kamio, Hanakawa, Inagaki and Hiraki2016). Of particular relevance, Aso and colleagues studied neural networks underlying judgment and reproduction of time intervals in the range of hundred milliseconds to a second. The judgment and reproduction tasks were supposed to unveil neural mechanisms underlying sensory aspects and motor aspects of temporal processing, respectively. Although participants had to represent time intervals for a few seconds, the task did not necessarily require the representation of time as a dimension. Therefore, the task was likely subserved by the temporal updating system rather than by the temporal reasoning system. We found that both sensory and motor temporal processing involved cerebro-cerebellar networks. The key cerebral structure seemed to be the supplementary motor area (SMA), which was assumed to serve as a time controller sending timing signals to effectors and other brain regions (Aso et al. Reference Aso, Hanakawa, Aso and Fukuyama2010). The cerebellum was assumed to receive an efference copy of the timing signals and to serve as an “emulator” for both motor and sensory tasks (Grush Reference Grush2004). The SMA also has a connection with the basal ganglia (Hanakawa et al. Reference Hanakawa, Goldfine and Hallett2017), which are implicated in temporal information processing in the range of seconds to hours (Ivry Reference Ivry1996). It is therefore possible that the motor cortical-basal ganglia-cerebellar networks support the temporal updating system. Consistently, Miyazaki et al. (Reference Miyazaki, Kadota, Matsuzaki, Takeuchi, Sekiguchi, Aoyama and Kochiyama2016) reported the neural correlates of tactile temporal order judgment and found the involvement of the motor system (ventral and bilateral dorsal premotor cortex and posterior parietal cortex) in temporal information processing.
The neural architecture supporting the temporal reasoning system, if any, is less clear. Presumably, the temporal reasoning system is supported by long-term memory and needs a higher level of cognitive processes than the temporal updating system. Gilead et al. (Reference Gilead, Liberman and Maril2013), found that the use of future tense is associated with ventromedial prefrontal cortex. Similarly, evocation of past and future events induces brain activation in the medial prefrontal cortex, cuneus/precuneus, and the medial temporal lobes (Botzung et al. Reference Botzung, Denkova and Manning2008), which overlap with the default mode network. The default mode network comprising of the medial prefrontal cortex and medial/lateral parietal cortex is implicated in representing autonoesis, which should be closely related to the function of temporal reasoning system. Nevertheless, the default mode network exists in both humans and animals. Growing evidence suggests that the rostro-lateral prefrontal cortex (or frontopolar cortex) may represent the past and the future to guide goal-directed behavior (Tsujimoto et al. Reference Tsujimoto, Genovesio and Wise2011). Because the rostro-lateral prefrontal cortex is particularly developed in humans, the development of this cortical structure may provide an account for the capacity of temporal reasoning uniquely in humans as claimed.
Dysfunctions of the neural correlates of the temporal updating and reasoning systems may underlie abnormality in temporal information processing in neuropsychiatric disorders. Dysfunction of the SMA-basal ganglia network (Hanakawa et al. Reference Hanakawa, Goldfine and Hallett2017) may account for abnormality in temporal information processing in Parkinson's disease (Ivry Reference Ivry1996). Evidence indicates that patients with schizophrenia may have impaired temporal updating systems, having difficulty in interval discrimination, and temporal prediction tasks (Waters & Jablensky Reference Waters and Jablensky2009; Takeda et al. Reference Takeda, Matsumoto, Ogata, Maida, Murakami, Murayama, Shimoji, Hanakawa, Matsumoto and Nakagome2017; Ueda et al. Reference Ueda, Maruo and Sumiyoshi2018). Losak and his colleagues (Reference Losak, Huttlova, Lipova, Marecek, Bares, Filip and Kasparek2016) examined brain activity during a predictive timing task, which would concern the temporal updating system, in patients with schizophrenia. They found alteration of brain activity in several brain regions including the SMA and cerebellum, which again support the role of the motor cortical-basal ganglia-cerebellar networks in the temporal updating system. In a meta-analysis by Thönes & Oberfeld (Reference Thönes and Oberfeld2015), timing task performance, which would mainly concern the temporal updating system, showed no significant effects of depression.
Neuropsychiatric disorders may also have altered temporal reasoning systems, but much remains to be studied. Patients with schizophrenia may have distortion in the temporal reasoning system, presumably involved in prospective memory and mental time traveling (Fornara et al. Reference Fornara, Papagno and Berlingeri2017; Henry et al. Reference Henry, Rendell, Kliegel and Altgassen2007). Recently, some investigations elucidated that patients with depression might have impairment in the temporal reasoning system. For example, patients with depression show increased use of past tenses, reduced vividness of positive prospective memory and negative beliefs about the future (Morina et al. Reference Morina, Deeprose, Pusowski, Schmid and Holmes2011; Roepke & Seligman Reference Roepke and Seligman2015; Smirnova et al. Reference Smirnova., Cumming, Sloeva, Kuvshinova, Romanov and Nosachev2018). Abnormality in subjective speed of time flow, which is likely subserved by the temporal reasoning system, has also been implicated in bipolar disorders and depression (Northoff et al. Reference Northoff, Magioncalda, Martino, Lee, Tseng and Lane2018; Ratcliffe Reference Ratcliffe2012). Neural substrates underlying these abnormalities should be investigated more vigorously than now, under the concept of the dual systems.
H&M's dual system proposal may provide new account for the timing deficits observed in neuropsychiatric disorders. Further research will be needed to delineate the nature of the temporal information processing in neuropsychiatric disorders and responsible sites of regions/networks.
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Hoerl & McCormack (H&M) have proposed to distinguish between “temporal updating system” and “temporal reasoning system” to interpret comparative and developmental psychological findings about temporal information processing. On the one hand, we understand that their view is compelling, especially from the viewpoint of developmental psychology. On the other hand, they stayed away from discussing the neural correlates that may underlie the two systems. They did not discuss how the proposed view might influence interpretations of findings from clinical studies on temporal processing in neuropsychiatric disorders, either. Hence, we will discuss plausible neural correlates, which may underlie the temporal updating/reasoning systems, and dysfunction of these systems, which may yield altered temporal processing in neuropsychiatric disorders. The argument is based on empirical evidence obtained in behavioral and neuroimaging studies (including our own) conducted in humans.
Previously, we performed a few neuroimaging studies to gain insight into the neural substrates underlying temporal information processing in healthy humans (Aso et al. Reference Aso, Hanakawa, Aso and Fukuyama2010; Bushara et al. Reference Bushara, Hanakawa, Immisch, Toma, Kansaku and Hallett2003; Ohki et al. Reference Ohki, Gunji, Takei, Takahashi, Kaneko, Kita, Hironaga, Tobimatsu, Kamio, Hanakawa, Inagaki and Hiraki2016). Of particular relevance, Aso and colleagues studied neural networks underlying judgment and reproduction of time intervals in the range of hundred milliseconds to a second. The judgment and reproduction tasks were supposed to unveil neural mechanisms underlying sensory aspects and motor aspects of temporal processing, respectively. Although participants had to represent time intervals for a few seconds, the task did not necessarily require the representation of time as a dimension. Therefore, the task was likely subserved by the temporal updating system rather than by the temporal reasoning system. We found that both sensory and motor temporal processing involved cerebro-cerebellar networks. The key cerebral structure seemed to be the supplementary motor area (SMA), which was assumed to serve as a time controller sending timing signals to effectors and other brain regions (Aso et al. Reference Aso, Hanakawa, Aso and Fukuyama2010). The cerebellum was assumed to receive an efference copy of the timing signals and to serve as an “emulator” for both motor and sensory tasks (Grush Reference Grush2004). The SMA also has a connection with the basal ganglia (Hanakawa et al. Reference Hanakawa, Goldfine and Hallett2017), which are implicated in temporal information processing in the range of seconds to hours (Ivry Reference Ivry1996). It is therefore possible that the motor cortical-basal ganglia-cerebellar networks support the temporal updating system. Consistently, Miyazaki et al. (Reference Miyazaki, Kadota, Matsuzaki, Takeuchi, Sekiguchi, Aoyama and Kochiyama2016) reported the neural correlates of tactile temporal order judgment and found the involvement of the motor system (ventral and bilateral dorsal premotor cortex and posterior parietal cortex) in temporal information processing.
The neural architecture supporting the temporal reasoning system, if any, is less clear. Presumably, the temporal reasoning system is supported by long-term memory and needs a higher level of cognitive processes than the temporal updating system. Gilead et al. (Reference Gilead, Liberman and Maril2013), found that the use of future tense is associated with ventromedial prefrontal cortex. Similarly, evocation of past and future events induces brain activation in the medial prefrontal cortex, cuneus/precuneus, and the medial temporal lobes (Botzung et al. Reference Botzung, Denkova and Manning2008), which overlap with the default mode network. The default mode network comprising of the medial prefrontal cortex and medial/lateral parietal cortex is implicated in representing autonoesis, which should be closely related to the function of temporal reasoning system. Nevertheless, the default mode network exists in both humans and animals. Growing evidence suggests that the rostro-lateral prefrontal cortex (or frontopolar cortex) may represent the past and the future to guide goal-directed behavior (Tsujimoto et al. Reference Tsujimoto, Genovesio and Wise2011). Because the rostro-lateral prefrontal cortex is particularly developed in humans, the development of this cortical structure may provide an account for the capacity of temporal reasoning uniquely in humans as claimed.
Dysfunctions of the neural correlates of the temporal updating and reasoning systems may underlie abnormality in temporal information processing in neuropsychiatric disorders. Dysfunction of the SMA-basal ganglia network (Hanakawa et al. Reference Hanakawa, Goldfine and Hallett2017) may account for abnormality in temporal information processing in Parkinson's disease (Ivry Reference Ivry1996). Evidence indicates that patients with schizophrenia may have impaired temporal updating systems, having difficulty in interval discrimination, and temporal prediction tasks (Waters & Jablensky Reference Waters and Jablensky2009; Takeda et al. Reference Takeda, Matsumoto, Ogata, Maida, Murakami, Murayama, Shimoji, Hanakawa, Matsumoto and Nakagome2017; Ueda et al. Reference Ueda, Maruo and Sumiyoshi2018). Losak and his colleagues (Reference Losak, Huttlova, Lipova, Marecek, Bares, Filip and Kasparek2016) examined brain activity during a predictive timing task, which would concern the temporal updating system, in patients with schizophrenia. They found alteration of brain activity in several brain regions including the SMA and cerebellum, which again support the role of the motor cortical-basal ganglia-cerebellar networks in the temporal updating system. In a meta-analysis by Thönes & Oberfeld (Reference Thönes and Oberfeld2015), timing task performance, which would mainly concern the temporal updating system, showed no significant effects of depression.
Neuropsychiatric disorders may also have altered temporal reasoning systems, but much remains to be studied. Patients with schizophrenia may have distortion in the temporal reasoning system, presumably involved in prospective memory and mental time traveling (Fornara et al. Reference Fornara, Papagno and Berlingeri2017; Henry et al. Reference Henry, Rendell, Kliegel and Altgassen2007). Recently, some investigations elucidated that patients with depression might have impairment in the temporal reasoning system. For example, patients with depression show increased use of past tenses, reduced vividness of positive prospective memory and negative beliefs about the future (Morina et al. Reference Morina, Deeprose, Pusowski, Schmid and Holmes2011; Roepke & Seligman Reference Roepke and Seligman2015; Smirnova et al. Reference Smirnova., Cumming, Sloeva, Kuvshinova, Romanov and Nosachev2018). Abnormality in subjective speed of time flow, which is likely subserved by the temporal reasoning system, has also been implicated in bipolar disorders and depression (Northoff et al. Reference Northoff, Magioncalda, Martino, Lee, Tseng and Lane2018; Ratcliffe Reference Ratcliffe2012). Neural substrates underlying these abnormalities should be investigated more vigorously than now, under the concept of the dual systems.
H&M's dual system proposal may provide new account for the timing deficits observed in neuropsychiatric disorders. Further research will be needed to delineate the nature of the temporal information processing in neuropsychiatric disorders and responsible sites of regions/networks.