The functional neuroanatomy of temporal discrimination

Abstract

Two identical stimuli, such as a pair of electrical shocks to the skin, are readily perceived as two separate events in time provided the interval between them is sufficiently long. However, as they are presented progressively closer together, there comes a point when the two separate stimuli are perceived as a single stimulus. Damage to posterior parietal cortex, peri-supplementary motor area (peri-SMA), and basal ganglia can disturb this form of temporal discrimination. Our aim was to establish, in healthy subjects, the brain areas that are involved in this process. During functional magnetic resonance imaging scanning, paired electrical pulses, separated by variable inter-stimulus intervals (5-110 msec), were delivered to different sites on one forearm (8-64 mm from the midline). Subjects were required to simply detect the stimulus (control task) or to identify a stimulus property. For temporal discrimination (TD), subjects reported whether they felt one or two stimuli. For spatial discrimination, they reported whether the stimuli were located on the right or left side of the forearm. Subjects reported their choice by pressing a button with the opposite hand. Our results showed that discrimination, as opposed to simply detection, activated several brain areas. Most were common to both discrimination tasks. These included regions of prefrontal cortex, right postcentral gyrus and inferior parietal lobule, basal ganglia, and cerebellum. However, activation of pre-SMA and anterior cingulate was found to be specific to the TD task. This suggests that these two frontal regions may play a role in the temporal processing of somatosensory events.

Figure 1.

a, Schematic drawing of the electrode array, also showing the imaginary longitudinal midline used as a reference for the SD task. b, Behavioral performance of one representative subject for the SD task in the prescanning behavioral session. Behavioral performance of the same subject for the temporal discrimination task is shown. The filled circles in b and c indicate electrode locations and time intervals chosen for fMRI scanning. Shaded areas correspond to the electrode positions and inter-stimulus intervals associated with inconsistent responses (i.e., penumbra).

Figure 3.

Top, Rendered view of the lateral surface of the left and right hemispheres, showing regions activating for both SD and TD, versus control. Bottom, Transverse sections on the canonical MR T1 template, showing anatomical details for the activations found in the head of caudate, right insula, and a sagittal section through subthalamic and cerebellar clusters (all activations are not visible in the surface-rendered projections). The plots show the pattern of activation for the four conditions of TD and four conditions of SD. Effect sizes represent the activation for each condition compared with baseline. The level of activity for each active condition corresponds to the contrast associated with the comparison of the active condition against baseline (using between-subject variability to calculate SE). As shown in the plots, all areas were activated above control, regardless of type of discrimination and consistency of response. SPM threshold p FDR corrected = 0.05. H/l, High/low-response consistency; R, right electrodes; 1, short ISIs; L, left electrodes; 2, long ISIs.

Figure 4.

Coronal and transversal sections on the canonical MR T1 template, showing anatomical details for the activations found in postcentral gyrus and S2. The plots show the pattern of activation for the four conditions of TD and four conditions of SD. Effect sizes represent the activation for each condition compared with baseline. All areas were activated above control, regardless of type of discrimination and consistency of response. SPM threshold p FDR corrected = 0.05. H/l, High/low-response consistency; R, right electrodes; 1, short ISIs; L, left electrodes; 2, long ISIs.

Figure 5.

Activations observed for the direct comparison of TD versus SD rendered onto the canonical brain surface (top view) and onto a sagittal section close to the midline. The plots illustrate that only the TD task activated above control, and that activations occurred regardless of response consistency. SPM threshold p small volume correction corrected = 0.05. H/l, High/low-response consistency; R, right electrodes; 1, short ISIs; L, left electrodes; 2, long ISIs.

Figure 2.

Grand mean of the consistency index for the 14 subjects, showing the behavioral performance during fMRI for SD (open squares, continuous line) and TD (filled circles, dotted line). On the x-axis are different ISI-electrode configurations, with short ISI (TD task) and leftward electrodes (SD task) plotted on the left of this graph (note that the exact ISI values and electrode position will vary for each subject, because these were determined individually). As expected, responses to electrode positions-intervals in the penumbra (gray shading) were less consistent than responses to limit-range conditions. Behaviorally, there was no significant effect of task or interaction between task and consistency.