Somatosensory Temporal Discrimination Threshold Involves Inhibitory Mechanisms in the Primary Somatosensory Area

Abstract

Somatosensory temporal discrimination threshold (STDT) is defined as the shortest time interval necessary for a pair of tactile stimuli to be perceived as separate. Although STDT is altered in several neurological disorders, its neural bases are not entirely clear. We used continuous theta burst stimulation (cTBS) to condition the excitability of the primary somatosensory cortex in healthy humans to examine its possible contribution to STDT. Excitability was assessed using the recovery cycle of the N20 component of somatosensory evoked potentials (SEP) and the area of high-frequency oscillations (HFO). cTBS increased STDT and reduced inhibition in the N20 recovery cycle at an interstimulus interval of 5 ms. It also reduced the amplitude of late HFO. All three effects were correlated. There was no effect of cTBS over the secondary somatosensory cortex on STDT, although it reduced the N120 component of the SEP. STDT is assessed conventionally with a simple ascending method. To increase insight into the effect of cTBS, we measured temporal discrimination with a psychophysical method. cTBS reduced the slope of the discrimination curve, consistent with a reduction of the quality of sensory information caused by an increase in noise. We hypothesize that cTBS reduces the effectiveness of inhibitory interactions normally used to sharpen temporal processing of sensory inputs. This reduction in discriminability of sensory input is equivalent to adding neural noise to the signal.

Significance statement: Precise timing of sensory information is crucial for nearly every aspect of human perception and behavior. One way to assess the ability to analyze temporal information in the somatosensory domain is to measure the somatosensory temporal discrimination threshold (STDT), defined as the shortest time interval necessary for a pair of tactile stimuli to be perceived as separate. In this study, we found that STDT depends on inhibitory mechanisms within the primary somatosensory area (S1). This finding helps interpret the sensory processing deficits in neurological diseases, such as focal dystonia and Parkinson's disease, and possibly prompts future studies using neurostimulation techniques over S1 for therapeutic purposes in dystonic patients.

Keywords: high-frequency oscillations; somatosensory evoked potentials; somatosensory temporal discrimination threshold; transcranial magnetic stimulation.

Figure 1.

STDT values for the left (left column) and right (right column) index finger before (T0), immediately after (T1), and 30 min after (T2) real (black lines) and sham (gray lines) cTBS over S1 (top row) and S2 (bottom row). cTBS delivered on S1, in the real condition, produced a significant increase of STDT values from T0 to T1 (p < 0.001) and from T0 to T2 (p = 0.008) (black line, top left). Error bars indicate standard error. Asterisks indicate significant differences.

Figure 2.

Psychometric curve representing the result of the behavioral task (Experiment 4). The horizontal dotted lines represent the probability of 25% and 75% of “2” responses on the y-axis (25p and 75p). The black dashed vertical lines represent the interval between 25p and 75p on the x-axis before cTBS, whereas the gray dashed vertical lines represent the interval between 25p and 75p after cTBS on the x-axis. Because the PRT can be calculated by the formula (75p − 25p)/2, the vertical dashed lines gives an idea about the effect of cTBS on PRT.

Figure 3.

RTs. The continuous line represents RT before cTBS, whereas the dotted line shows RT after cTBS. Difference in RT at ISI between 30 and 90 ms are significant (see Results). Error bars indicate standard error.

Figure 4.

N20 latency (left) and amplitude (right) before (T0), immediately after (T1), and 30 min after (T2) real (black lines) and sham (gray lines) cTBS over S1. cTBS delivered on S1, in the real condition, produced a significant decrease of N20 amplitude from T0 to T1 (p < 0.01) and from T0 to T2 (p < 0.01) (black line, right).

Figure 5.

N20 recovery cycle at ISI of 5 ms (R5; black line), 20 ms (R20; gray line), and 40 ms (R40; dashed line) before (T0), immediately after (T1), and 30 min after (T2) real (left) and sham (right) cTBS over S1. cTBS delivered on S1, in the real condition, produced a significant increase of R5 from T0 to T1 (p < 0.01) and from T0 to T2 (p < 0.01) (black line, left). Error bars indicate standard error. Asterisks indicate significant differences.

Figure 6.

Left column, A wide-band SEP showing the N20–P25 complex (A) and the same recording bandpass filtered between 400 and 800 Hz showing HFO (B) in one of the subjects. As shown, e-HFO and l-HFO can be divided by the N20 peak. The average starts 5 ms after the stimulation artifact, which was removed manually. Right column, e-HFO (C) and l-HFO (D) area before (T0), immediately after (T1), and 30 min after (T2) real (gray line) and sham (black line) cTBS over S1. cTBS delivered on S1, in the real condition, produced a significant increase in e-HFO area from T0 to T1 (p < 0.01) and from T0 to T2 (p < 0.01) (black line, left) and a decrease in l-HFO area from T0 to T1 (p = 0.003) and from T0 to T2 (p = 0.01) (black line, right). HFO area is expressed in μV² × 10⁻⁴. Error bars indicate standard error. Asterisks indicate significant differences.

Figure 7.

Correlations between STDT and R5 (top row) and between STDT and l-HFO (bottom row) after cTBS on S1; T0/T1 ratio (left column) and T0/T2 ratio (right column). Changes in STDT induced by cTBS delivered over S1 were significantly correlated with the changes induced on R5 and on l-HFO at T1 and T2.

Figure 8.

Right (T4, black line) and left (T3, gray line) N120 amplitude before (T0), immediately after (T1), and 30 min after (T2) cTBS delivered on the right S2. S2–cTBS produced a significant decrease of right N120 amplitude, recorded at T4, from T0 to T1 (p < 0.01) and from T0 to T2 (p < 0.01). Error bars indicate standard error. Asterisks indicate significant differences.