The substantia nigra pars compacta and temporal processing

Abstract

The basal ganglia and cerebellum are considered to play a role in timing, although their differential roles in timing remain unclear. It has been proposed that the timing of short milliseconds-range intervals involves the cerebellum, whereas longer seconds-range intervals engage the basal ganglia (Ivry, 1996). We tested this hypothesis using positron emission tomography to measure regional cerebral blood flow in eight right-handed males during estimation and reproduction of long and short intervals. Subjects performed three tasks: (1) reproduction of a short 500 ms interval, (2) reproduction of a long 2 s interval, and (3) a control simple reaction time (RT) task. We compared the two time reproduction tasks with the control RT task to investigate activity associated with temporal processing once additional cognitive, motor, or sensory processing was controlled. We found foci in the left substantia nigra and the left lateral premotor cortex to be significantly more activated in the time reproduction tasks than the control RT task. The left caudate nucleus and right cerebellum were more active in the short relative to the long interval, whereas greater activation of the right putamen and right cerebellum occurred in the long rather than the short interval. These results suggest that the basal ganglia and the cerebellum are engaged by reproduction of both long and short intervals but play different roles. The fundamental role of the substantia nigra in temporal processing is discussed in relation to previous animal lesion studies and evidence for the modulating influence of dopamine on temporal processing.

Figure 1.

Time reproduction > control RT: left SNc. Left substantia nigra pars compacta activation [(−4, −12, −8)] greater in the time reproduction tasks (SHORT ± LONG) than the control reaction time task. Activations are shown on the MNI reference brain, on sagittal, coronal, and horizontal views. Parameter estimates for the left substantia nigra pars compacta showing increased activity during timing tasks compared with the control reaction time task across all subjects. Significant at p > 0.001, uncorrected. L, Left; R, right.

Figure 2.

Time reproduction > control RT: left premotor cortex. Left premotor cortex activation [(−24, 2, 44)] greater in the time reproduction tasks (SHORT ± LONG) than the control reaction time task. Activations are shown on the MNI reference brain, on sagittal, coronal, and horizontal views. Parameter estimates for the left premotor cortex showing increased activity during timing tasks compared with the control reaction time task across all subjects. Significant at p > 0.001, uncorrected. L, Left; R, right.

Figure 3.

SHORT > LONG. Results are displayed as statistical parametric maps in sagittal, coronal, and transverse projections in stereotactic space. Significant at p > 0.001, uncorrected. L, Left; R, right.

Figure 4.

SHORT > LONG: left caudate nucleus and right cerebellar hemisphere. a, Left caudate nucleus [(−14, −10, 20)] activation greater in the SHORT reproduction task than in the LONG reproduction task. Parameter estimates showing mean activation for each subject are also displayed. b, Right cerebellar hemisphere [(36, −74, −38)] activation greater in the SHORT reproduction task than in the LONG reproduction task. Parameter estimates showing mean activation for each subject are also displayed. Activations are shown on the MNI reference brain, on sagittal, coronal, and horizontal views. Significant at p > 0.001, uncorrected. L, Left; R, right.

Figure 5.

LONG > SHORT. Results are displayed as statistical parametric maps in sagittal, coronal, and transverse projections in stereotactic space. Significant at p > 0.001, uncorrected. L, Left; R, right.

Figure 6.

LONG > SHORT: right putamen and right cerebellar hemisphere. a, Right putamen [(34, 8, 4)] activation greater in the LONG reproduction task than in the SHORT reproduction task. Parameter estimates showing mean activation for each subject are also displayed. b, Right putamen [(34, 8, 4)] activation greater in the LONG reproduction task than in the SHORT reproduction task. Enlarged image is shown. c, Right cerebellar hemisphere [(30, −60, −18)] activation greater in the LONG reproduction task than in the SHORT reproduction task. Parameter estimates showing mean activation for each subject are also displayed. Activations are shown on the MNI reference brain, on sagittal, coronal, and horizontal views. Significant at p > 0.001, uncorrected. L, Left; R, right.