Research reportSomatotopic representation of tactile duration: evidence from tactile duration aftereffect
Introduction
When a vibration is delivered to us, we perceive not only its frequency and intensity, but also its duration. The perception of tactile duration is fundamental to a wide range of human activities, such as playing the piano and video games. However, in past decades, although some somesthetic senses, such as tactile texture and location perceptions, have been well studied [1], we still know little about where tactile duration is encoded in the brain.
It is generally accepted that there is no specific organ dedicated to time discrimination. Time is one of the amodal and emergent properties of events. To account for this amodal nature, some models used a metaphor of a central clock for time measurement [[2], [3], [4]]. This clock typically includes a pacemaker and an accumulator, which extract durations from different modalities, indicating a supramodal mechanism for duration processing. According to these models, tactile duration should be encoded in cortical areas beyond the primary somatosensory cortex (S1). This view is supported by evidence that the superior temporal gyrus (STG) in the auditory cortex is involved in processing the duration of tactile events, suggesting a supramodal role of the STG in tactile duration perception [5,6]. However, modality-specific view is supported by the mismatch negativity (MMN) components which were locked to unimodal auditory and tactile duration deviants and were generated in individual sensory cortical regions [7]. Furthermore, recent studies suggest that S1 is involved in tactile temporal processing [8,9]. Therefore, the processing level at which tactile duration is encoded remains incompletely understood.
We have investigated this issue by using the adaptation aftereffect paradigm. Adaptation aftereffects, as the “psychophysicist’s microelectrode” [10], have been widely used to uncover the sensory processing mechanisms in the brain. Previous adaptation research has shown that sensory stimuli were represented at various cortical processing levels, according to their complexity. For example, in vision, tilt aftereffect has been attributed to low-level orientation processing, with high specificity to retinal location [11,12]. In contrast, face aftereffect generalized to different retinal locations [13], orientations [14], and stimulus sizes [15], suggesting a high-level representation of faces. Adaptation aftereffects were also observed in other sensory modalities, including the tactile modality [16]. Perceptions of tactile properties, including size [17], distance[18], curvature [19,20], shape [21], motion [22,23], and roughness [24] are susceptible to adaptation, manifested as repulsive perceptual aftereffects. For example, in the well-known curvature aftereffect, participants judged a flat surface to be concave after being exposed to a convex surface, and vice-versa [19].
Similar to the aftereffects in the spatial domain, repetitive exposure to a duration results in the duration-selective repulsive aftereffect [[25], [26], [27]]. For example, prolonged adaptation to short visual durations (e.g.,160 ms) leads to the overestimation of the intermediate visual durations (e.g., 320 ms) presented subsequently, while prolonged adaptation to long durations (e.g., 640 ms) results in the underestimation of the same intermediate durations [25]. The duration aftereffect has also been used extensively to deduce the neural bases of duration perception in recent years. Studies have found that the duration aftereffects in vision and audition were modality specific [25,28]. Studies also showed that the duration aftereffect was contingent on the auditory frequency [28,29], but not on visual orientation and space [28,30,31]. Although the duration aftereffects in vision and audition have received much attention, surprisingly, there has been little work on the duration aftereffect in touch.
An empirical question about the tactile duration adaptation is whether and how a repulsive tactile duration aftereffect could be observed. With the presumed repulsive duration aftereffect in the tactile domain, the level of cortical mechanisms underlying the aftereffect is an important question. This question could be firstly addressed by examining the sensory transferability of the adaptation aftereffect. If the adaptation aftereffect could transfer between different sensory modalities, the supramodel processing view would gain support. Otherwise, a modality-specific adaptation mechanism would play a pivotal role in the aftereffect. For example, a cross-modal adaptation aftereffect on facial emotion suggests a high-level, supramodal representation of emotion [32]. Secondly, experimental results from topographic generalization could help to address this question. The cortical representations of body parts (i.e., somatotopic organization) have been established in mammals and humans [[33], [34], [35]]. In the tactile domain, the cortical representation of hand in S1 contains a detailed finger topography [36]. In the finger topography, studies have explored the cortical processing of many tactile properties, including orientation, pressure, and roughness. Benefits from discrimination learning on those properties could only transfer to adjacent and homologous fingers, indicating early cortical processing mechanisms [37,38]. The noticeable transfer of the curvature aftereffect between fingers regardless of the hands also indicates that the neural processing of curvature information involves the somatosensory cortex shared by fingers of both hands [39,40]. To our best knowledge, the potential topographic generalization of the tactile duration aftereffect has not been studied.
In the present study, we investigated whether the duration aftereffect could be observed in the tactile modality as in the visual and auditory modalities, to uncover the timing mechanisms for sub-second tactile duration processing. In Experiment 1, we observed the repulsive tactile duration aftereffect with both the methods of single stimuli (Experiment 1A) and duration reproduction (Experiment 1B). Moreover, we showed that the aftereffect was tuned around the adapting duration (Experiment 1C). In Experiment 2, we investigated its processing level by looking into the transferability of the tactile duration aftereffect between the auditory and tactile modalities. Experiment 2 implemented two paradigms: consecutive adaptation to either auditory or tactile duration (Experiment 2A) and simultaneous adaptation to both auditory and tactile durations (Experiment 2B). In Experiment 3, we further examined the topographic generalization of the tactile duration aftereffect. The results from Experiments 2 and 3 showed that the tactile duration aftereffect was modality specific, and was organized within a somatotopic framework, suggesting the somatotopic representation of tactile duration.
Section snippets
Experiments 1A, B and C:Adaptation to tactile duration induces the tactile duration aftereffect
We used the methods of single stimuli (Experiment 1A) and duration reproduction (Experiment 1B) to investigate whether adaptation to a tactile duration could affect subsequent tactile duration perception. In the method of single stimuli, participants classified a test duration as shorter or longer, compared with the mean of a group of test durations (i.e., the internal mean). This method is simple yet reliable, but the internal mean is initially formed before adaptation and could be
Experiments 2A and B: Tactile duration aftereffect is modality specific
Although Experiment 1 has established the existence of the tactile duration aftereffect, the processing level for this tactile aftereffect is still unclear. According to previous studies, auditory and tactile perceptions can interplay in a variety of behavioral contexts [[48], [49], [50], [51]]. It has been shown that processing of auditory and tactile signals shares some common neural substrates [52,53]. For example, studies have found a supramodal role of the STG in tactile duration
Experiment 3: Tactile duration aftereffect is organized within a somatotopic framework
Experiment 3 investigated the topographic generalization of the aftereffect. If the tactile duration aftereffect is specific to the adapted finger or could generalize to fingers dictated by the topographic distance, this aftereffect might originate at the stage of somatotopic processing. However, a possible spread of the adaptation effect across all fingers regardless of the topographic distance, would indicate higher-level mechanisms in the somatosensory system. In Experiment 3, we
General discussion
In the present study, we explored whether and how duration adaptation in the tactile modality affects the perception of subsequent durations. Our results demonstrated the repulsive tactile duration aftereffect with passive touch. After prolonged adaptation to a shorter tactile duration, participants perceived subsequent medium tactile durations as being longer. When the adapting tactile duration was longer, the same subsequent medium tactile durations were perceived shorter. The tactile
Conclusion
The present findings demonstrate that duration adaptation bidirectionally modulates the tactile duration perception. The adaptation effect was tuned around the adapting duration, was modality specific and organized within a somatotopic framework. The present study thus provides new insights into the tactile timing mechanism: sub-second tactile duration perception mobilizes the somatotopic processing. In human-machine interaction, the choice of duration is importance for designing and rendering
Conflict of interest
The authors declare no competing financial interests.
Acknowledgements
This work was supported by Project Crossmodal LearningNSFC 61621136008/DFG TRR-169, MOST 2015CB351800, NSFC 31421003, NSFC 61527804, NSFC 31671168, NSFC 31800965, and China Postdoctoral Science Foundation2018M630011.
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Spatial selectivity of the visual duration aftereffect in the sub-second range: An event-related potentials study
2022, Behavioural Brain ResearchCitation Excerpt :Researchers have studied the properties and neural mechanisms of the duration aftereffect. The duration aftereffect is bidirectionally negative, can be produced in visual, auditory, and tactile channels, and is modality-specific [7–9]. However, controversies remain regarding the neural substrates of the visual duration aftereffect and brain regions associated with neural adaptation.
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2022, Trends in Cognitive SciencesCitation Excerpt :Perceptual after-effects produced by adaptation also extend to other quantities, such as visual duration [82] (Figure 3D) and visual object size [89–91], and other sensory modalities, such as auditory numerosity [3] and auditory duration [82,92] (Figure 3E). In the haptic modality, there is evidence for adaptation after-effects for tactile numerosity [93], motor movement rate [94], tactile duration [95], and haptic object size [96] (Figure 3F). Similar to visual numerosity (Figure 3A–C), we propose that changes in the responses of neurons with different tuning functions mediate these changes in perception.
Electrophysiological correlates of the somatotopically organized tactile duration aftereffect
2021, Brain ResearchCitation Excerpt :This study hence revealed a coherent behavioral-electrophysiological link for the somatotopically organized tactile duration aftereffect. Consistent with our previous study (Li et al., 2019), behavioral results provided further evidence that the effect size of the tactile duration aftereffect is contingent on the topographic distance between fingers. Specifically, the aftereffect could transfer to adjacent fingers (even when the frequency of the tactile stimulus was relatively low, i.e., 30 Hz, see Fig. S1B), but not homologous fingers.