Cortical networks underlying mechanisms of time perception

Abstract

Precise timing of sensory information from multiple sensory streams is essential for many aspects of human perception and action. Animal and human research implicates the basal ganglia and cerebellar systems in timekeeping operations, but investigations into the role of the cerebral cortex have been limited. Individuals with focal left (LHD) or right hemisphere (RHD) lesions and control subjects performed two time perception tasks (duration perception, wherein the standard tone pair interval was 300 or 600 msec) and a frequency perception task, which controlled for deficits in time-independent processes shared by both tasks. When frequency perception deficits were controlled, only patients with RHD showed time perception deficits. Time perception competency was correlated with an independent test of switching nonspatial attention in the RHD but not the LHD patients, despite attention deficits in both groups. Lesion overlays of patients with RHD and impaired timing showed that 100% of the patients with anterior damage had lesions in premotor and prefrontal cortex (Brodmann areas 6, 8, 9, and 46), and 100% with posterior damage had lesions in the inferior parietal cortex. All LHD patients with normal timing had damage in these same regions, whereas few, if any, RHD patients with normal timing had similar lesion distributions. These results implicate a right hemisphere prefrontal-inferior parietal network in timing. Time-dependent attention and working memory functions may contribute to temporal perception deficits observed after damage to this network.

Fig. 1.

Axial sections showing the location of lesions in 19 individuals with left hemisphere damage. Case numbers are displayed beneath each series of sections and are ordered according to whether lesions were largely anterior or posterior to the central sulcus. The letter a refers to individuals with impaired frequency perception, and the letter b refers to individuals with impaired duration perception.

Fig. 2.

Axial sections showing the location of lesions in 18 individuals with right hemisphere damage. Case numbers are displayed beneath each series of sections and are ordered according to whether lesions were largely anterior or posterior to the central sulcus. The letter a next to the case number refers to individuals with impaired frequency perception, and the letter brefers to individuals with impaired duration perception.

Fig. 3.

Mean (SE) difference thresholds for the 300 msec (black bars) and 600 msec (white bars) conditions of the duration perception task. The top graph (a) displays the data from all subjects, and the bottom graph (b) includes data only from subjects who performed within normal limits on the frequency perception task.

Fig. 4.

Lesion overlap in individuals with damage primarily anterior or posterior to the central sulcus. Axial sections show overlap for left hemisphere (on the left of each section) and right hemisphere (on the right of each section) lesions in individuals with intact frequency perception. Thelines on the lateral view show the location of the corresponding axial sections. The color scale indicates the percentage of patients within a particular group with damage in an area. a, Overlapping lesions in patients with anterior lesions and impaired performance on the duration perception task. Only three patients with RHD were impaired on this task, and the common areas of infarction (yellow) were found on Section 9 (top row) andSection 10 (bottom row). No individuals with LHD were impaired on duration perception. b, Overlapping lesions in patients with anterior lesions and normal performance on the duration perception task. A region onSection 9 shows 100% overlap in the three patients with LHD. There were no common areas of infarction in the two RHD patients (i.e., blue indicates a lesion from one patient).c, Overlapping lesions in patients with posterior lesions and impaired performance on the duration perception task. Seven patients with RHD were impaired on this task, and the common area of infarction (yellow) was found on Section 9 (top row). Only two LHD patients were impaired on this task, and the common area of infarction is seen on Section 8 (bottom row). d, Overlapping lesions in patients with posterior lesions and normal performance on the duration perception task. Section 9 shows 100% overlap in six patients with LHD. There were no common areas of infarction in the three RHD patients (i.e., green and redsignify lesions from one and two patients, respectively).