Tactile temporal order

• Dr. Shinya Yamamoto, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan

• Prof. Shigeru Kitazawa, Graduate School of Frontier Biosciences, Osaka University

The perception of tactile temporal order, the order of multiple touches to the skin in time, has long been a topic of research in psychophysics but has drawn new attention since the discovery that it depends not only on the stimulation interval but also on body postures in space. When two stimuli are delivered in succession one to each hand, 75% correct judgment is achieved with a Stimulus Onset Asynchrony (SOA) of approximately 20-60 ms (as long as the hands are not crossed). However, when the arms are crossed, judgments are often inverted at longer SOAs (100-200 ms), and correct judgments are recovered at much longer SOAs (0.5-1 s) yielding an N-shaped psychometric function in some individuals. The inverted judgment and the recovery are now considered to result from an initial erroneous remapping of the touch to the spatial location of the other hand and further remapping of the signal to the correct hand thereafter. Thus, tactile temporal order depends critically on the process of localizing tactile stimuli in space, which develops over time. Multiple regions are now implicated in the judgment of tactile temporal order, including the posterior parietal cortices for remapping tactile signals in space, and the perisylvian areas that are implicated in the temporal order judgment of visual stimuli as well.

What is unique about tactile temporal order?

The perception of temporal order between two events has been an important issue in psychophysics for many years (Hirsh and Sherrick, 1961; Efron, 1963; Sternberg and Knoll, 1973; Pöppel, 1997). However, tactile temporal order, the temporal order between two tactile stimuli, had been only one issue of many combinations of the three sensory modalities (visual, auditory, tactile, audio-visual, visuo-tactile, audio-tactile). Indeed, it was generally accepted that the brain can judge the order of two stimuli that are separated in time by 20-30 ms independent of the sensory modalities of these stimuli (Hirsh and Sherrick, 1961; Pöppel, 1997).

In the 2000s, tactile temporal order began to attract particular attention in two contexts. First, it was discovered that tactile temporal order is dramatically altered just by crossing the hands (Yamamoto and Kitazawa, 2001a; Shore et al., 2002b). This was a finding unique to the tactile modality, because we can cross the hands (tactile sense organs) in space but not the eyes or ears. Second, calibration in tactile temporal order, after the repeated presentation of a pair of stimuli in a particular order, occurred in the opposite direction (Miyazaki et al., 2006) compared to lag adaptation that had been discovered in audio-visual modalities (Fujisaki et al., 2004; Vroomen et al., 2004). Sound and light with fixed intervals are likely to originate from a single event. By contrast, two tactile signals with a fixed interval are most likely to originate from two different events.

Here, we review these recent findings on tactile temporal order and discuss their general implications.

Essential contribution of spatial coordinates and body postures to tactile temporal order

Temporal resolution in normal postures

When two touches are delivered one to each hand with the arms in a normal posture (uncrossed), 75% correct judgment can be achieved with a stimulation interval of 20-60 ms (Shore et al., 2002b; Roder et al., 2004; Wada et al., 2004; Shore et al., 2005; Craig and Belser, 2006; Kobor et al., 2006; Schicke and Roder, 2006; Azanon and Soto-Faraco, 2007b; Roberts and Humphreys, 2008; Fujisaki and Nishida, 2009; Heed et al., 2012). To be more precise, the stimulation interval may be replaced with the stimulus onset asynchrony (SOA), which refers to the interval between the onsets of the two stimuli. The just noticeable difference (JND) is a measure of temporal resolution, which is defined as half of the difference between two SOAs that yield the “right hand first” judgment in 75% and 25% of the trials (Figure 1B).

Figure 1: A general model (A) and an ordinary psychometric function (B) of temporal order judgment. Sternberg and Knoll (1973) hypothesized that there is a decision mechanism that receives signals A and B through independent channels and yields an “A-first-then-B” judgment according to the difference in the arrival times (TB-TA). The probability function G was hypothesized to be a non-decreasing (monotonous) function of the time difference. SOA: stimulus onset asynchrony, JND: just noticeable difference, PSS: point of subjective simultaneity.

Hirsh (1961) reported that a JND of approximately 20 ms was shared across 6 combinations of the 3 different sensory modalities (visual, auditory, tactile, audio-tactile, visuo-tactile, and audio-visual temporal order judgment, TOJ). However, a recent study (Fujisaki and Nishida, 2009) reported that the JND was smallest in tactile TOJ (19 ms) followed by the JNDs in audio-tactile (23 ms) and visuo-tactile (30 ms) TOJs and was largest in audio-visual TOJs (37 ms).

Sambo et al. (2013) recently reported that the JND with nociceptive stimuli increased to 80 ms as compared to 49 ms with tactile stimuli. This may be attributed to a larger variance in conduction latency with Aδ fibers that convey nociception than that with Aβ fibers that convey the sense of touch.

Judgment reversal in tactile temporal order due to arm crossing

Figure 2: Reversal of subjective temporal order due to arm (A, B) and stick (C) crossing. A: The judgment probability that the right hand was stimulated earlier than the left hand is plotted against the stimulation interval. A positive SOA indicates that the right hand was stimulated first. The response curve was a classical sigmoid when the arms were uncrossed (black circles and curves), whereas it became N-shaped in the exemplified subject when the arms were crossed (red dots and curves). B: Pooled data from eight naive subjects who crossed the left hand over the right hand in the crossed-arm condition (red dots and curves). The N-shape is still apparent. C: Data from a subject with an apparent judgment reversal when the sticks were crossed without crossing the arms (red dots and curve). Stimulation was delivered to the tip of each stick, and the subject was required to judge which of the two tips was stimulated first. Panel A was reproduced from Yamamoto and Kitazawa (2001a). Panels A-C were reproduced from Kitazawa et al. (2008) with permission from Oxford University Press (In: Sensorimotor Foundations of Higher Cognition, page 76).

Tactile temporal order is dramatically altered simply by crossing the hands (Yamamoto and Kitazawa, 2001a; Shore et al., 2002b). When participants judged the order of two tactile stimuli with their arms crossed, the JND increased to 124 ms from 34 ms (Shore et al., 2002b). The effect was beyond the mere increase in the JND (Yamamoto and Kitazawa, 2001a). In some participants, the subjective temporal order was inverted at SOAs of 100-200 ms but was corrected at longer SOAs (1500 ms). As a result, the psychometric function was no longer monotonic but N-shaped (Figure 2A, B). The effect of arm crossing on tactile TOJ has now been replicated in many studies (Yamamoto and Kitazawa, 2001a; Shore et al., 2002a; Roder et al., 2004; Wada et al., 2004; Craig and Belser, 2006; Kobor et al., 2006; Schicke and Roder, 2006; Azanon and Soto-Faraco, 2007a; Roberts and Humphreys, 2008; Pagel et al., 2009; Heed et al., 2012; Cadieux and Shore, 2013), and the mean JND in the arms-uncrossed posture was in the range of 18-58 ms but increased to 91-447 ms. It is worth noting that the JND, which implicitly assumes a monotonic function, is not useful for quantifying N-shaped responses because it yields a negative value. Instead, Yamamoto and Kitazawa (Yamamoto and Kitazawa, 2001a) introduced a quantitative model with a probability of judgment reversal from the right-hand first to the left-hand first (Al) or vice versa (Ar), which can be fit to N-shaped or S-shaped responses. The peak probability of judgment reversal varied across participants and ranged from 0.1 to 1 with an average of ~0.3 (Yamamoto and Kitazawa, 2001a; Wada et al., 2004).

A reversal of tactile temporal order also occurs when two legs are crossed (with foot stimulation) or when one arm and the contralateral leg are crossed (Schicke and Roder, 2006). It even occurs without crossing the arms when crossing two drumsticks (one held in each hand (Figure 2C)) when participants are required to judge the order of stimuli that were delivered to the tips of the sticks with their eyes closed (Yamamoto and Kitazawa, 2001b). Straight sticks can be replaced with L-shaped (Yamamoto et al., 2005) or virtual tools in virtual reality (Moizumi et al., 2007).

These reversals in tactile temporal order occur when participants respond with their hand with their eyes closed. Under these conditions, it is reasonable to base their judgments simply on the locations of the stimuli on the body surface. Nonetheless, tactile temporal order was reversed. This indicates that tactile signals are not ordered in time while the signals are represented somatotopically. Tactile temporal order is determined only after the tactile signals are referred to a relevant location in space, which could be the hand itself or the tip of a tool in the hand.

Other evidence for the involvement of spatial coordinates

The perceived hand positions in space affect tactile temporal order even when the arms are not crossed. The JND decreases as the distance of two hands increase (Shore et al., 2005; Kuroki et al., 2010). The JND increases when the two hands are virtually placed close together with a mirror (Gallace and Spence, 2005). Hermosillo (2011) demonstrated that the planning of arm movements from uncrossed to crossed impairs tactile TOJ, even when the stimuli are delivered prior to the onset of actual arm-crossing movements. The subjective temporal order is affected by future (planned) arm configuration.

Involvement of local motion and global “apparent motion”

Craig (2003) and Craig and Busey (2003) examined TOJs of two tactile stimuli presented to two finger pads when each of the two stimuli simulated a local motion of the skin. They found that the judgments were affected by the local tactile motions. The judgments were biased toward the correct judgment, (or toward the incorrect judgment) according to whether the direction of the local motions were consistent (or inconsistent) with the global “apparent motion” defined by the two successive stimuli across the finger pads. These results clearly demonstrate that local tactile motions, which should be represented in the somatotopic coordinates in the initial stage, interact with the direction of the global motion vector between the two hands defined in the external coordinates. Another study (Kitazawa et al., 2008) reported that tactile TOJ was affected by visual distractors that defined a global motion vector between the two hands. By using visual distractors that participants were told to ignore, some participants yielded N-shaped response curves even when the arms were not crossed. Takahashi et al. (2013) reported that the participants felt a sense of “motion” in > 70% of trials when the two stimuli were delivered one to each hand with SOAs of 50-200 ms. The sense of “motion” occurred irrespective of whether the arms were crossed or uncrossed even though the participants closed their eyes.

Altogether, we can speculate that tactile TOJ involves signals regarding a global motion vector defined between the spatial locations of tactile stimuli in the external coordinates.

Spatial remapping of tactile stimuli implicated for judgment reversal

It is now generally accepted that the judgment reversal due to arm crossing occurs because of an initial erroneous remapping of the tactile signal to the spatial position of the wrong (contralateral) hand (Yamamoto and Kitazawa, 2001a; Kitazawa, 2002; Fujisaki et al., 2012; Heed and Azanon, 2014). The tactile signal, initially remapped to the wrong position (1’ in Figure 4A), is then remapped to the correct hand thereafter (1’’ in Figure 4A). The dynamic process of remapping is supported by several findings as follows. Groh and Sparks (1996) reported that some trajectories of saccadic eye movements in response to a touch to the crossed hand began in the direction of the wrong hand, curved toward the correct hand, and reached the correct hand approximately 400 ms after the delivery of the stimulus. A recent study examined the finding in more detail (Overvliet et al., 2011). By using a cross-modal cueing paradigm, Azanon & Soto-Faraco (Azanon and Soto-Faraco, 2008; Azanon et al., 2010b) demonstrated that a touch to a crossed hand initially facilitated a response to a visual stimulus to the wrong hand but then facilitated a response to a visual stimulus to the correct hand 180-360 ms after the touch.

What happens when two stimuli are delivered one to each of the crossed hands (1 and 2 in Figure 4) before the first stimulus is remapped to the correct hand? We may speculate that both stimuli are mapped to the wrong hand (1’ and 2’ in Figure 4). That is, tactile temporal order is inverted in the space represented in the brain. By contrast, when the second stimulus is delivered with an interval greater than 500 ms, after the first stimulus is remapped to the correct hand, the second stimulus is also remapped to the correct hand after an interval, and the correct judgment can be recovered.

Recent studies using functional imaging (Wada et al., 2012), electroencephalography (Heed and Roder, 2010; Soto-Faraco and Azanon, 2013) and transcranial magnetic stimulation (Azanon et al., 2010a) suggested that the posterior parietal cortex is involved in the process of tactile remapping.

Figure 3: Two steps in spatial remapping. It is now generally accepted that a stimulus to a crossed hand (1) is initially remapped to the wrong hand (1’) but remapped further to the correct hand thereafter (1’’). When the second stimulus (2) is delivered before the first stimulus is correctly remapped, the second stimulus is also remapped to the wrong hand (2’). Tactile temporal order is then inverted in the space coordinates in the brain. The figure was reproduced from Kitazawa et al. (2008) with permission from Oxford University Press (In: Sensorimotor Foundations of Higher Cognition, page 91).

Congenitally (early) blind people do not demonstrate reversals in tactile TOJ even when their arms are crossed but late blind participants (aged 12 years and above) do (Roder et al., 2004; Collignon et al., 2009). Pagel et al. (2009) demonstrated that the crossing effect on tactile TOJ was not observed before the age of 5 years but is observed after the age of 5 1/2 years. Those data suggest that the use of external coordinates for tactile localization is acquired by the age of 5 years and requires normal vision. Notably, the crossing effect is smaller when the normal sighted cross the hands in the back than when they cross their hands in front (Kobor et al., 2006). These findings further suggest that the development of the crossing effect requires experience to direct the eyes to the position of touch on the skin.

A model of tactile TOJ

A model of tactile TOJ (a motion projection hypothesis) that accounts for all of the findings explained above has been proposed (Figure 4) (Kitazawa et al., 2008; Fujisaki et al., 2012; Takahashi et al., 2013). In the model, two successive tactile signals to both hands are initially represented in somatotopic coordinates (such as in the primary sensory cortex) but are then remapped to spatial coordinates (such as in the parietal cortex). These signals also evoke a global motion signal in the perisylvian areas. The separate information regarding “what happened where” and the motion vector is finally integrated to construct a perception regarding “what happened in which order”.

Figure 4: Motion-projection hypothesis. Tactile events are hypothesized to be ordered in time by combining information regarding “what happened where” represented in external spatial coordinates and information regarding “when”. The “when” information is hypothesized to be captured in a motion vector. Illustrations show the process of correct judgment in the arms-uncrossed condition (A) and inverted judgment in the arms-crossed condition (B). The same networks are hypothesized to be activated in both cases. Adapted from Takahashi et al. (2013) with permission from Oxford University Press.

However, it is worth noting that the model does not apply to all cases in tactile TOJ. For example, Roberts and Humphrey (2008) reported that crossing the arms had no effect on tactile TOJ when order was judged by the frequency or duration of the tactile stimuli. The underlying mechanisms should be different in those tasks that do not require the discrimination of one hand from the other.

Neuroimaging

A functional imaging study (Takahashi et al., 2013) examined the brain regions involved in judgments of the temporal order of successive taps delivered to both hands. A numerosity judgment task of similar difficulty with identical tactile stimulation was used as a control. In both arm postures (arms crossed and uncrossed) the following regions were activated: the bilateral premotor cortices, the bilateral middle frontal gyri, the bilateral inferior parietal cortices and supramarginal gyri, and the bilateral posterior part of the superior and middle temporal gyri.

Activation in the premotor and inferior parietal areas agrees with the involvement of spatial coordinates. Stronger activation was found in the parietal region, which is implicated in the process of remapping tactile stimuli to spatial coordinates when the participants crossed their arms.

The activation in the perisylvian areas was close to (and partially overlapped with) the visual-motion–sensitive areas. This was also in good agreement with the suggested involvement of the motion vector defined between the two hands. Activation close to the perisylvian area was also reported during a visual TOJ task (Davis et al., 2009).

Temporal order judgments and simultaneity judgments

Simultaneity judgment (SJ) refers to a judgment of whether two signals are simultaneous or not. The probability of the judgment that two signals are simultaneous is generally approximated by a Gaussian function of the SOA with a peak at approximately zero (e.g., Fujisaki and Nishida, 2009). The SOA that yields the peak probability of simultaneity judgment is generally close to the point of subjective simultaneity (PSS) during TOJ, which is defined as an SOA where the order judgment probability is 0.5 (Figure 1B). This may yield the impression that the two stimuli are perceived as simultaneous at the PSS during TOJ. However, this is not necessarily true (Weiss and Scharlau, 2011). Even if we are totally uncertain about the temporal order of two stimuli, we can still perceive them as not being simultaneous. This point is clearly demonstrated in the participant illustrated in Figure 2A. The participant’s N-shaped response curve cut the level of 0.5 at 3 points; one near zero; and the others at -600 and +400 ms. At the two points with SOAs of ~500 ms, the stimuli cannot be perceived as simultaneous, though the order was totally ambiguous for the participant. Indeed, it has been repeatedly shown that crossing the arms does not impair SJ at all (Axelrod et al., 1968; Geffen et al., 2000; Fujisaki and Nishida, 2009). We are not necessarily able to judge the temporal order even if we are certain that they are not simultaneous. That is, some mechanisms for TOJ do not overlap with those for SJ (Hirsh and Sherrick, 1961; Ulrich, 1987; Jaśkowski, 1991; Yamamoto and Kitazawa, 2001a; Shore et al., 2005; Fujisaki and Nishida, 2009).

Patients with Parkinson’s disease (PD), a neurodegenerative disease strongly associated with basal ganglia dysfunction, demonstrate deficits in temporal processing when performing temporal reproduction tasks (Pastor et al., 1992a; O'Boyle et al., 1996; Harrington et al., 1998), perceptual timing tasks (Pastor et al., 1992b; Malapani et al., 1998), SJs, and temporal discrimination between two stimuli (Artieda et al., 1992; Fiorio et al., 2008; Conte et al., 2010). A neuroimaging study of healthy participants confirmed that the basal ganglia and the substantia nigra pars compacta are involved in the reproduction of short and long time intervals (Jahanshahi et al., 2006). These previous findings suggest that dopaminergic transmission in the basal ganglia and related cortical structures play an important role in interval timing tasks, including SJ (for review see Buhusi and Meck, 2005; Merchant et al., 2013). However, patients with PD do not necessarily demonstrate deficits in TOJ compared with their age-matched controls (Nelson et al., 2012; Nishikawa et al., in press). It is possible that SJ may depend more critically on dopaminergic transmission in the basal ganglia than TOJ.

Taken together, the mechanisms underlying tactile TOJ are not identical to SJ, though some overlap may exist.

Effects of past experiences on tactile temporal order

After repeated exposures to a constant time lag of audiovisual stimulus pairs, the lag tends to be ignored to make participants perceive the audiovisual stimuli as being simultaneous (Figure 5B) (Fujisaki et al., 2004; Vroomen et al., 2004). This is called lag adaptation, which is considered to be helpful for binding two signals that have arrived in the brain with a certain delay but actually originated from a single event. Due to the difference between the conduction velocity of light (3 x 1010 m/s) and sound (3 x 102 m/s), the light and sound that occurred simultaneously from a single event arrive at the sensory organs with some delay (light then sound) depending on the distance between the event location and the head. Thus, it is reasonable to ignore the constant lag. However, it is less likely that two tactile stimuli to both hands originated from a single event because the spatial locations of the two hands are not always identical. In fact, lag adaptation is not observed in tactile temporal order judgment when stimuli are delivered one to each hand. Instead, the opposite phenomenon is observed. When the right (left) hand is stimulated earlier than the left (right) hand, subjects tend to have more judgments of right-hand-first (left-hand-first) (Figure 5C). Since it conforms to Bayesian integration theory, the phenomenon is referred to as “Bayesian calibration” (Miyazaki et al., 2006). More specifically, this type of perceptual change can be considered as a learning of “prior” probability in the Bayesian terminology. By contrast, the lag adaptation can be considered as a learning of “likelihood” (Sato and Aihara, 2011; Fujisaki et al., 2012). How these two types of perceptual changes are implemented in the brain should be the focus of future studies.

Figure 5: Two opposing calibrations observed in audiovisual (B) and tactile (C) TOJs. (A) Biased distributions of SOAs with positive (blue) and negative (red) peaks. Positive SOA indicates “auditory first” in audiovisual TOJ and “right hand first” in tactile TOJ. (B-C) Opposite types of temporal calibration: lag adaptation (B) and Bayesian calibration (C). The probability of ‘‘auditory first’’ (B) and ‘‘right hand first’’ (C) judgments (ordinate) is plotted against the SOAs. The psychometric function shifts toward the peak of each distribution of SOAs in audiovisual TOJs (B, lag adaptation), while it shifts away from the peak in tactile TOJs (C, Bayesian calibration). The figure was reproduced from Miyazaki et al. (2006).

Future directions

N-shaped response curves (Figure 2A), discovered by crossing the arms, cannot be explained by the long-held decision center model with two independent channels (Figure 1A). The discovery unique to tactile temporal order revealed that the process of TOJ is more complex than had once been believed. A proposed model hypothesizes that spatial information (what happened where) and temporal information (direction of motion vector) are combined, and the most likely scenario on what happened where in which order is constructed (Figure 4). The validity of the hypothesis in other sensory modalities and its neural correlates warrant further investigation.

Another line of studies in tactile temporal order have revealed that repeated exposure to stimuli with a certain order results in a calibration of PSS in the opposite direction (Bayesian calibration) compared to the lag adaptation discovered during audiovisual TOJ (Figure 5). The new finding in tactile temporal order has already been tested with audiovisual TOJ, and it was confirmed that Bayesian calibration occurs even in the audiovisual TOJ (Yamamoto et al., 2012). Generalizing the discoveries in tactile temporal order to other modalities will provide important hints to uncover the mechanisms of temporal order information processing in general.

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Sponsored by: Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

Reviewed by: Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

Reviewed by: Prof. Ehud Ahissar, Department of Neurobiology, The Weizmann Institute, Rehovot

Accepted on: 2015-03-23 06:37:56 GMT