Effects of stimulus-driven synchronization on sensory perception

Abstract

Background: A subject's ability to differentiate the loci of two points on the skin depends on the stimulus-evoked pericolumnar lateral inhibitory interactions which increase the spatial contrast between regions of SI cortex that are activated by stimulus-evoked afferent drive. Nevertheless, there is very little known about the impact that neuronal interactions - such as those evoked by mechanical skin stimuli that project to and coordinate synchronized activity in adjacent and/or near-adjacent cortical columns - could have on sensory information processing.

Methods: The temporal order judgment (TOJ) and temporal discriminative threshold (TDT) of 20 healthy adult subjects were assessed both in the absence and presence of concurrent conditions of tactile stimulation. These measures were obtained across a number of paired sites - two unilateral and one bilateral - and several conditions of adapting stimuli were delivered both prior to and concurrently with the TOJ and TDT tasks. The pairs of conditioning stimuli were synchronized and periodic, synchronized and non-periodic, or asynchronous and non-periodic.

Results: In the absence of any additional stimuli, TOJ and TDT results obtained from the study were comparable across a number of pairs of stimulus sites - unilateral as well as bilateral. In the presence of a 25 Hz conditioning sinusoidal stimulus which was delivered both before, concurrently and after the TOJ task, there was a significant change in the TOJ measured when the two stimuli were located unilaterally on digits 2 and 3. However, in the presence of the same 25 Hz conditioning stimulus, the TOJ obtained when the two stimuli were delivered bilaterally was not impacted. TDT measures were not impacted to the same degree by the concurrent stimuli that were delivered to the unilateral or bilateral stimulus sites. This led to the speculation that the impact that the conditioning stimuli - which were sinusoidal, periodic and synchronous - had on TOJ measures was due to the synchronization of adjacent cortical ensembles in somatosensory cortex, and that the synchronization of these cortical ensembles could have been responsible for the degradation in temporal order judgment. In order to more directly test this hypothesis, the synchronized 25 Hz conditioning stimuli that were delivered during the initial TOJ test were replaced with asynchronous non-periodic 25 Hz conditioning stimuli, and these asynchronous conditioning stimuli did not impact the TOJ measures.

Conclusion: The results give support to the theory that synchronization of cortical ensembles in SI could significantly impact the topography of temporal perception, and these findings are speculated to be linked mechanistically to previously reported co-activation plasticity studies. Additionally, the impact that such synchronizing conditioning stimuli have on TOJ - which can be measured relatively quickly - could provide an effective means to assess the functional connectivity of neurologically compromised subject populations.

Figure 1

Protocol details. Panel A: Two sequential vibrotactile pulses were delivered during the Stimulus Interval, one to each of either skin site A or B. Subject was queried as to which skin site received the first pulse during the Response Interval, and this was followed by a 5 sec delay before the onset of the subsequent trial. Panel B: Pulse delivery sequence for the TOJ and TDT tasks during each 1 sec Stimulus Interval. Order of delivery (skin site A or B) was randomized on a trial-by-trial basis, and inter-pulse interval was decreased or increased, depending on subject response. Panel C: Exemplary 25 Hz conditioning stimulus delivered concurrently with TOJ/TDT task. Panel D: Two non-periodic asynchronous stimuli were delivered concurrently with the TOJ and TDT tests. Panel E: Two non-periodic but synchronous stimuli were delivered concurrently with the TOJ and TDT tests.

Figure 2

TOJ and TDT measures obtained from 3 different paired skin sites. The TOJ (solid bars) is not significantly different (ANOVA; p > 0.01) across the different sites of stimulation. The TDT (open bars) is not significantly different than TOJ at any of the sites of stimulation (p > 0.01).

Figure 3

Performance metrics obtained at each of the pairs of stimulus sites under 3 different conditions of concurrent stimulation (0, 25 Hz, and 200 Hz). Panel A: Hand dorsum. Note that TOJ thresholds are significantly elevated with the presence of both the 25 Hz and 200 Hz conditioning stimuli (p < 0.01). Panel B: Unilateral digit tips 2 & 3. The 200 Hz conditioning stimulus, although it has an impact on the TOJ measure (p < 0.01) does not have as pronounced an effect on the digit tips as on the hand dorsum. Panel C: Bilateral digit tips 2. Conditioning stimuli had no significant effect when applied on bilateral digit tips (p > 0.21).

Figure 4

Comparison of periodic vs. nonperiodic stimuli. Replacing synchronized 25 Hz vibrotactile conditioning stimuli (results shown in Figure 3) with asynchronous, nonperiodic stimuli resulted in no significant change from the control condition.