Transcranial Magnetic Stimulation applied to the primary motor cortex demonstrates involvement in mental rotation of Shepard figures and hands.

Abstract

Mental rotation (MR) assists individuals’ mind in visualizing object stimuli being rotated at a different orientation from their original position. The primary motor cortex (M1) was discovered to be activated in the mental rotation (MR) of Shepard figures, but the M1 displays its involvement in MR of hands to a lesser extent. This suggests that the M1 plays a complimentary part in facilitating MR, rather than orchestrating the entire process. Nonetheless, the direct comparison between Shepard figures and hands’ conditions has not yet been properly explored. In order to investigate the functional role of M1 in MR of hands and Shepard figures, 60 participants completed a MR task whilst transcranial magnetic stimulation (TMS) was delivered to the M1 region. There were two separate trials, where half of the participants performed a MR task with hands (M = 24.03, SD = 3.33) whereas the other half engaged in MR of objects (M = 23.60, SD = 2.87). Any performance disruption, as measured by reaction times (RTs) against a sham TMS condition, would be indicative of functional involvement in M1 in MR of hands and objects. A pair samples t-test displayed slight increase in RTs when real TMS was applied to M1 for both the hand (p = .003, d = .602) and Shepard figures (p < .001, d = .701) condition. These findings imply that the M1 has a contributory role in facilitating MR of hands and Shepard figures.

Keywords: Primary motor cortex, mental rotation, transcranial magnetic stimulation

Mental rotation (MR) is a motor imagery task that requires rotating visual stimuli to an orientation that is distinct from which they are presented (Hamada et al. 2018). Such ability enables people to undertake everyday tasks such as mapping the environment (Meneghetti et al. 2014) or specific tasks such as comparing the area of two different polygons in geometry (Hawes et al. 2015). Shepard et al. (1978) first investigated MR by asking participants to determine the congruence between pairs of three-dimensional, multi-armed cube figures, known as Shepard figures across different trajectories. Studies have since investigated the cognitive process underlying MR through transcranial magnetic stimulation (TMS), which disrupts continuous neural activity in a brain region to disclose when its activity occurs during a cognitive process (Eisenegger et al., 2007).

Eisenegger et al. (2007) discovered that the primary motor cortex (M1) was activated during MR. Their study applied the probing excitability approach, which delivers a single TMS pulse to the M1 to determine its Motor evoked potentials (MEPs), which measure M1’s electrical activity during MR. Participants completed the MR task by assessing whether two pictures of Shepard figures were identical or mirrored in two experiments. The first experiment required them to engage in MR, alongside an aloud reading and an inner reading task while the second experiment applied TMS as participants completed the MR task. The results demonstrated that MR of Shepard cubes obtained higher MEPs in M1, compared to reading aloud or silently. Despite M1’s activation in each task, it was unclear why the M1’s involvement was more inherent in MR, but not reading aloud or silently.

Additionally, Ganis et al. (2000) found that the M1 is also responsible for the MR of hand yet its involvement is still ambiguous. By applying single pulse TMS, Ganis et al. (2000) found TMS impaired the MR of hands more than that of feet indicating that the M1 contributes more to the hands’ task. However, the study required participants to deliver motor responses via feet, which compromised TMS’s impairment in M1 and thus obtained TMS effects at a later stage. In contrast, Sauner et al. (2006) did not find any disruption from single pulse TMS to the M1 when participants judged the laterality of hands’ stimuli. Because participants answered verbally, TMS pulses impacted the activity of M1’s region that is responsible for initiating vocal movement instead of hands. This could suggest that M1’s involvement in MR of hand demands further clarification because of feet and verbal response’s interferences.

Bode et al. (2008) considered perhaps that M1’s role in MR is dependent on strategic application in rotating visual stimuli. Their study speculated that in general, the MR involved either internal strategy, referring to MR of an object with hands, triggering M1 or external strategy, indicating a self-rotating object driven by an external force that may not require M1. The internal strategy is applied to simple stimuli, such as hands or tools whereas abstract figures, like houses or Shepard cubes, involve external strategy. Nonetheless, their study found TMS pulses applied to M1 evoke stronger MEPs during MR for every category of objects except for hands. Subjectively, most participants reported using the external strategy for Shepard figures, tools and 2-D figures, yet it was not widely applied to hands. Although the study pointed out that external strategy is not essential for M1 during MR, the M1’s causal role in MR of hands warrants further research.

The current study aimed to investigate whether M1 is causally involved in MR by focusing on testing MR with hand and Shepard cubes condition. If M1 is involved in MR of hands along with Shepard figures, then reaction time should be longer in both conditions when real TMS is applied as opposed to sham TMS. Therefore, it is hypothesized that participants will be slower to react under real TMS compared to sham TMS in MR of Shepard figures, mediated by longer reaction time (RT) in real TMS. It is additionally hypothesized that participants will be slower to respond, which is reflected in higher RT under real TMS compared to sham TMS in MR of hand.

Method

Participants

Sixty participants took part in the study, 30 of whom were allocated to the hands condition (16 female, 14 male; aged 18–30 years; M = 24.03, SD = 3.33) and 30 of whom were allocated to the Shepard figures condition (15 female, 15 male, aged 18–29 years; M = 23.60, SD = 2.87). All participants were right-handed, had normal or corrected-to-normal vision, and had no history of psychological or neurological disorders.

Materials and Measures

A transcranial magnetic stimulator (TMS) equipped with a figure-eight coil was used. This was placed tangentially over the hand area of the left primary motor cortex with the handle pointing backward and rotated 45 away from the midline. Stimuli were presented on the 21” flat screen of a Dell PC using the Presentation Software Package. Stimuli were either Shepard figures (Shepard & Metzler, 1971) or hands (Bode et al., 2007) which were approximately constant in size (maximum of 10cm).

Procedure and Design

Participants were seated approximately 70 cm (+/- 4) from the computer screen. Their task was to mentally rotate the left object to see if it could be made to match the object on the right. A positive match could be made in half of the trials, whereas in the other half, the object was mirrored. The degree of rotation necessary to come to either a “same” or “different” judgement ranged between 45 and 315 degrees. For each category, there were three objects, each presented at four different viewing angles. All stimuli were shown twice, once for “same” and once for “different”, leading to 24 trials in total per block for each condition which were randomized. Participants were instructed to mentally rotate each object in order to decide whether it was the same or different. They were asked to do this as quickly and accurately as possible, indicating their decision using one of two buttons with their left hand. There were six experimental blocks.

Results

Participants’ reaction times (RT) were measured for real TMS and sham TMS in both hand and Shepard conditions (see Figure 1). The mean RT was recorded when real TMS pulse was delivered to the hand area of the left M1 throughout the MR of Shepard figures (M = 2115, SD = 173.42) and in the sham TMS condition (M = 1950, SD = 152.25). The same occurred for MR of hands under real TMS (M = 1899, SD = 180) and sham TMS (M = 1774, SD = 143.51).

Figure 1

Mean Reaction Times for real Transcranial Magnetic Stimulation (TMS) and Sham trials

Note: RT was measured in millisecond (ms). Error bars represent standard errors.

A pair-samples t-test indicated that mentally rotating Shepard cubes in real TMS condition yielded slightly higher mean RT than the sham condition. This difference was statistically significant t(29) = 3.839, p < .001, d = .701, which constitutes a large effect, according to Cohen (1988). Similarly for the hands’ condition, real TMS applied to M1 increased RT relative to sham TMS, t(29) = 3.298, p = .002, d = .602, which also constitutes a large effect (Cohen 1988).

Discussion

This study aimed to extend our understanding of M1 influence in the MR of Shepard figures and hands. Significant differences between real TMS and sham TMS supported our first hypothesis that participants would be slower to react under the condition of real TMS compared to sham TMS when mentally rotating Shepard figures. Our results also support the second hypothesis that participants’ RT would be greater under the condition of real TMS relative to sham TMS when they mentally rotated their hand. Potentially, these findings suggest that real TMS impaired MR slightly less in hands’ condition than Shepard figures’ condition, which is suggestive of a less substantial association between M1 and MR of hands.

The finding that participants were slower to react under real TMS conditions in engaging in mental rotation is in line with Eissenegr et al. (2007) and Bode et al. (2008). Our research applied a different method from Eisseneger et al (2007) in which our study does not establish conditions where participants read aloud or silently, thus preventing both processes from influencing M1. Furthermore, our study narrows Bode et al. (2008) study’s stimuli used to test M1’s excitability down to hands and Shepard cubes. The primary focus of this research is to compare RT between sham TMS and real TMS in MR of hand and Shepard cubes. Our findings are similar to the two aforementioned studies, suggesting that M1 does play a role in mental rotation.

In particular, the finding that MR of hands required higher RT under real TMS applied to M1 is consistent with Ganis et al (2008) but contradicts Sauner et al. (2006). Our findings are similar to Ganis et al. (2008) in which both our studies discovered that impairing M1 during MR of hands results in higher RT. In contrast, Sauner et al. (2006) did not find evidence concerning M1’s involvement in ME even though their research and our research requires individuals to respond. While Sauner et al. (2006) requires participants to deliver their answer verbally, our participant pressed the response button with their hands. Perhaps utilization of hands’ response enabled us to observe more clearly M1’s response to MR.

The finding that M1 has a lower RT under the hand condition compared to Shepard cubes’ condition may be attributable to the coordination in brain areas adjacent to M1. Specifically, Wraga et al. (2003) discovered that the premotor cortex (Area 6) and M1 was activated in preparatory hand movements, suggesting that M1 may receive anticipatory signals from area 6 to prepare for hand rotation. Cona et al. (2017) proposed that the dorsal premotor cortex mediate the comprehension of the similarity or differences between stimuli and process the concluding information for M1 to response. Since multiple brain regions including M1 facilitate MR of hand, the area’s strategic role in hand rotation can be an avenue for future research.

Nevertheless, one limitation of the study is that the study’s measure of RTs does not explain why M1 was involved in Shepard cubes and hands’ condition. The result mainly demonstrated that MR of Shepard cubes and hand retained a higher RT in real TMS than sham TMS applied to M1. Although it suggests that M1 contributed to MR, it is unable to reveal the cognitive process that underlies M1’s functionality. Another limitation is that the study considers primarily M1 instead of proximal brain regions. It is reasonable to suppose that M1 did not entirely contribute to hands’ rotation, which may explain why the effect size in M1 activation in hands’ condition is moderative compared to Shepard figures. Hamada et al. (2018) observed that MR of hand stimulated M1, area 6 and the posterior motor cortex under fMRI which measures brain activity during MR. Further studies can compare between MR of hands and Shepard Cubes through fMRI.

In conclusion, our study found that the MR of Shepard cubes was slower than that of hands when TMS was applied to the M1. Our results indicate that M1 contributed to MR of abstract figures but was less engaged in rotating hands. As the results revealed the function of M1, and how involved the area is with distinct stimuli, they expanded the knowledge regarding M1’s functionality in helping humans utilize motor imagery skill in everyday life.

References

Bode, S., Koenecke, S., & Jäncke, L. (2007). Different strategies do not moderate primary motor cortex involvement in mental rotation: A TMS study. Behavioral and Brain Functions, 3(38), 1–9, https://doi.org/10.1186/1744- 9081–3–38

Cohen, J. (1988) Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Erlbaum Associate.

Cona, G., Panozzo, G., & Semenza, C. (2017). The role of dorsal premotor cortex in mental rotation: A transcranial magnetic stimulation study. Brain and cognition, 116, 71–78.

Eisenegger, C., Herwig, U., & Jäncke, L. (2007). The involvement of primary motor cortex in mental rotation revealed by transcranial magnetic stimulation. European Journal of Neuroscience, 25(4), 1240–1244. https://doi.org/10.1111/j.1460-9568.2007.05354.x

Giorgio Ganis, Julian P. Keenan, Stephen M. Kosslyn, Alvaro Pascual-Leone (2000). Transcranial Magnetic Stimulation of Primary Motor Cortex Affects Mental Rotation, Cerebral Cortex, 10(2), February 2000, 175–180, https://doi.org/10.1093/cercor/10.2.175

Hamada, H., Matsuzawa, D., Sutoh, C., Hirano, Y., Chakraborty, S., Ito, H., … & Shimizu, E. (2018). Comparison of brain activity between motor imagery and mental rotation of the hand tasks: a functional magnetic resonance imaging study. Brain imaging and behavior, 12(6), 1596–1606.

Hawes, Z., Moss, J., Caswell, B., & Poliszczuk, D. (2015). Effects of mental rotation training on children’s spatial and mathematics performance: A randomized controlled study. Trends in Neuroscience and Education, 4(3), 60–68.

Meneghetti, C., Borella, E., & Pazzaglia, F. (2016). Mental rotation training: transfer and maintenance effects on spatial abilities. Psychological Research, 80(1), 113–127. doi:10.1007/s00426–014–0644–7

Sauner, D., Bestmann, S., Siebner, H. R., & Rothwell, J. C. (2006). No evidence for a substantial involvement of primary motor hand area in handedness judgements: a transcranial magnetic stimulation study. European Journal of Neuroscience, 23(8), 2215–2224. doi:10.1111/j.1460–9568.2006.04731.x

Shepard, R. N., & Metzler, J. (1971). Mental rotation of three-dimensional objects. Science, 171(3972), 701–703.

Wraga, M., Thompson, W. L., Alpert, N. M., & Kosslyn, S. M. (2003). Implicit transfer of motor strategies in mental rotation. Brain and cognition, 52(2), 135–143.