Processing of temporal information and the basal ganglia: new evidence from fMRI

Abstract

Temporal information processing is a fundamental brain function, which might include central timekeeping mechanisms independent of sensory modality. Psychopharmacological and patient studies suggest a crucial role of the basal ganglia in time estimation. In this study, functional magnetic resonance imaging (fMRI) was applied in 15 healthy right-handed male subjects performing an auditory time estimation task (duration discrimination of tone pairs in the range of 1,000-1,400 ms) and frequency discriminations (tone pairs differing in pitch, around 1,000 Hz) as an active control task. Task difficulty was constantly modulated by an adaptive algorithm (weighted up-down method) reacting on individual performance. Time estimation (vs rest condition) elicited a distinct pattern of cerebral activity, including the right medial and both left and right dorsolateral prefrontal cortices (DLPFC), thalamus, basal ganglia (caudate nucleus and putamen), left anterior cingulate cortex, and superior temporal auditory areas. Most activations showed lateralisation to the right hemisphere and were similar in the frequency discrimination task. Comparing time and frequency tasks, we isolated activation in the right putamen restricted to time estimation only. This result supports the notion of central processing of temporal information associated with basal ganglia activity. Temporal information processing in the brain might thus be a distributed process of interaction between modality-dependent sensory cortical function, the putamen (with a timing-specific function), and additional prefrontal cortical systems related to attention and memory. Further investigations are needed to delineate the differential contributions of the striatum and other areas to timing.

A right hemispheric prefrontal system for cognitive time measurement

“…The well established influence of dopamine upon subjective time measurement has led to the suggestion that the basal ganglia, a cluster of nuclei which are heavily innervated by dopamine, may house a time-dependent process, or at least be involved in timing. Cellular recordings showing that cells in this area can fire in a temporally specific manner (Matell et al, 2003) as well as a number of well controlled neuroimaging studies (Pouthas et al, 2005b;Nenadic et al, 2003;Coull, 2004;Coull et al, 2004a) reinforce this possibility. Support is not universal, however, as many other imaging studies have failed to find timing related activity in these structures (Macar et al, 2002;Tracy et al, 2000;Maquet et al, 1996;Sakai et al, 1999;Lewis and Miall, 2003a), or have found it only when control conditions are not subtracted from timing conditions (Rao et al, 2001;Coull and Nobre, 1998).…”

Relations among fluid intelligence, sensory discrimination and working memory in middle to late childhood – A latent variable approach

“…Studies looking at the activation during sensory discrimination tasks have shown that certain brain areas are only activated during specific sensory discrimination tasks (e.g., the right putamen in duration discrimination tasks; Nenadic et al, 2003) while other regions, such as the areas in the dorsolateral prefrontal cortex (DLPFC), that have previously been linked to WM (see e.g., MacDonald, Cohen, Stenger, & Carter, 2000) are activated during various sensory discrimination tasks, including pitch, color, auditory duration, visual duration, and intensity discrimination (Ferrandez et al, 2003;Livesey, Wall, & Smith, 2007;Nenadic et al, 2003). These results show that brain areas that are considered to be fundamental for WM functioning (DLPFC; see e.g., Barbey, Koenigs, & Grafman, 2013;Owen, 2000;Smith & Jonides, 1999) are also activated in a wide variety of sensory discrimination tasks, supporting the assumption that some WM resource is activated during sensory discrimination.…”

Impaired time perception and motor timing in stimulant-dependent subjects

“…Neuroimaging studies have shown that temporal processing is associated with activation in right prefrontal regions (Rao et al, 2001;Rubia et al, 1998;Rubia and Smith, 2004). Other neuroimaging studies of timing have implicated a fronto-striatal network as the neural basis of the internal clock (Cuoll et al, 2004;Hinton and Meck, 2004;Nenadic et al, 2003). Pharmacological studies on animals and humans support the general hypothesis that fronto-striatal circuits are critical for temporal processing.…”