The Somatotopy of Mental Tactile Imagery

Abstract

To what degree mental imagery (MI) bears on the same neuronal processes as perception has been a central question in the neurophysiological study of imagery. Sensory-recruitment models suggest that imagery of sensory material heavily relies on the involvement of sensory cortices. Empirical evidence mainly stems from the study of visual imagery and suggests that it depends on the mentally imagined material whether hierarchically lower regions are recruited. However, evidence from other modalities is necessary to infer generalized principles. In this fMRI study we used the somatotopic organization of the primary somatosensory cortex (SI) to test in how far MI of tactile sensations activates topographically sensory brain areas. Participants (N = 19) either perceived or imagined vibrotactile stimuli on their left or right thumbs or big toes. The direct comparison to a corresponding perception condition revealed that SI was somatotopically recruited during imagery. While stimulus driven bottom-up processing induced activity throughout all SI subareas, i.e., BA1, BA3a, BA3b, and BA2 defined by probabilistic cytoarchitectonic maps, top-down recruitment during imagery was limited to the hierarchically highest subarea BA2.

Keywords: fMRI; imagery debate; mental codes; mental imagery; somatosensory; tactile; tactospatial sketchpad.

FIGURE 1

Experimental Design. (A) Vibrotactile stimuli were presented on a 2 x 4 pin Braille-like display. (B) Stimulation modules were attached to four body locations: right hand thumb (rH), left hand thumb (lH), right foot big toe (rF), and left foot big toe (lF). (C) The experimental paradigm constituted a block design where a visual color cue indicated where to imagine vibration in the four IMAGERY conditions. For the PERCEPTION condition the visual display was matched, where blue/green indicated PERCEPTION/IMAGERY (randomized across subjects). Each trial lasted 8 s and was followed by a 12 s inter-trial interval. Each condition was repeated three times in each of the three experimental runs, supplemented with six null-events (8 s fixation) per run.

FIGURE 2

General imagery related brain activity. To depict the network of brain regions that support tactile imagery independent of content, we computed the main effect of IMAGERY > PERCEPTION. The identified network is composed of areas that are known to be modulated by general task demands such as the SMA and the preMC, which were recently associated with rehearsal processes (Fegen et al., 2015) and the medial frontal gyrus. Furthermore, activity in bilateral IFG was found, which is well known for its involvement in the processing of vibrotactile stimuli. Finally, we found left-lateralized activation in the IPS.

FIGURE 3

Somatotopic activation in SI and SII during (A) perception (p < 0.05 FWE corrected at the voxel level) and (B) imagery (p < 0.01 uncorrected), revealed by the contrasts of individual stimulation conditions against the three other PERCEPTION/IMAGERY conditions. As expected, the activation strength in somatosensory cortices during IMAGERY was lower than during PERCEPTION and was therefore tested on an uncorrected level following the a priori hypothesis of somatotopic activation in SI/SII. (C) Overlap of somatotopic activation in SI between PERCEPTION > other PERCEPTION conditions and IMAGERY > other IMAGERY conditions contrasts. Results displayed at p < 0.001 uncorrected within a SI/SII mask generated with the Anatomy Toolbox.

FIGURE 4

Comparison of perception and imagery. (A) Overlap in activation between perception and imagery identified by body-locus-specific conjunction analyses against conjunction null hypothesis (Friston et al., 2005), confirming that MI indeed recruits SI content-specifically. All results displayed at p < 0.05 FWE corrected at the voxel level, cluster extend threshold of 22 voxel; Note: The conjunction analysis for the right foot toe displayed also SI and SII activation however only at a threshold of p < 0.001 uncorrected, corresponding activation clusters are reported in Table 1. (B) To test what areas activate more during the PERCEPTION than during the IMAGERY condition, we computed the corresponding contrast for the left and right hand conditions and identified the hierarchically lower SI subregions (BA3b and BA1) to be stronger activated during PERCEPTION. Those SI areas that are activated in both conditions – as depicted by the conjunction analysis – are the more posterior portions of SI, corresponding to the hierarchically higher subarea BA2. To display the differences in activation level across SI subregions, we extracted first-level contrast estimates for the PERCEPTION and IMAGERY conditions contrasted against implicit baseline. These demonstrate that BA3b and BA1 do not show activation levels exceeding baseline, and that activation levels in BA2 are higher in the PERCEPTION condition than in the IMAGERY condition.