ALE meta-analysis reveals dissociable networks for affective and discriminative aspects of touch

Abstract

Emotionally-laden tactile stimulation-such as a caress on the skin or the feel of velvet-may represent a functionally distinct domain of touch, underpinned by specific cortical pathways. In order to determine whether, and to what extent, cortical functional neuroanatomy supports a distinction between affective and discriminative touch, an activation likelihood estimate (ALE) meta-analysis was performed. This meta-analysis statistically mapped reported functional magnetic resonance imaging (fMRI) activations from 17 published affective touch studies in which tactile stimulation was associated with positive subjective evaluation (n = 291, 34 experimental contrasts). A separate ALE meta-analysis mapped regions most likely to be activated by tactile stimulation during detection and discrimination tasks (n = 1,075, 91 experimental contrasts). These meta-analyses revealed dissociable regions for affective and discriminative touch, with posterior insula (PI) more likely to be activated for affective touch, and primary somatosensory cortices (SI) more likely to be activated for discriminative touch. Secondary somatosensory cortex had a high likelihood of engagement by both affective and discriminative touch. Further, meta-analytic connectivity (MCAM) analyses investigated network-level co-activation likelihoods independent of task or stimulus, across a range of domains and paradigms. Affective-related PI and discriminative-related SI regions co-activated with different networks, implicated in dissociable functions, but sharing somatosensory co-activations. Taken together, these meta-analytic findings suggest that affective and discriminative touch are dissociable both on the regional and network levels. However, their degree of shared activation likelihood in somatosensory cortices indicates that this dissociation reflects functional biases within tactile processing networks, rather than functionally and anatomically distinct pathways.

Keywords: activation likelihood estimate; affective touch; discriminative touch; meta-analytic connectivity modeling; posterior insula; secondary somatosensory cortex.

Figure 1

Activation likelihood estimate (ALE) maps and contrasts for affective and discriminative touch. Upper left panel: Clusters in posterior insula (40, −14, 8) and parietal operculum (46, −26, 22; 46, −16, 10) with a significantly high likelihood of activation for touch stimulation associated with positive subjective ratings (“affective touch”). Map reflects reported activations across 17 studies (N = 291 unique subjects; see Table 1). Upper right panel: Clusters in primary (48, −38, 44) and secondary (52, −24, 20; −58, −20, 14) somatosensory cortices with a significantly high likelihood of activation for touch stimulation associated with tactile discrimination tasks (“discriminative touch”). Map reflects reported activations across 25 studies, N = 1075. Bottom left panel: A cluster in posterior insula (42, −14, 8) had a significantly higher specific activation likelihood for affective touch, as revealed by a contrast between affective and discriminative ALE maps. Bottom right panel: A cluster in primary somatosensory cortex (47,‐39, 46) had a significantly higher specific activation likelihood for discriminative touch, as revealed by a contrast between discriminative and affective ALE maps (see Table 2 for other clusters). All maps thresholded at FDR (pN) q < 0.001, minimum cluster size 200 mm. All coordinates reported in MNI space.

Figure 2

Selectivity and bias in somatosensory activation likelihood maps for aspects of affective touch. Right: Nonselective secondary somatosensory clusters (48, −26, 22; −54, −20, 18) significantly likely to be activated in both affective and discriminative touch paradigms, as revealed by a conjunction of affective and discriminative touch ALE maps. Left: Relative contributions of stimulated skin type (hairy, red; or glabrous, blue) to the affective touch ALE map. Despite an overall sampling bias toward hairy skin stimulation in affective touch studies (78%), 67% of the contributing foci in a PO cluster (46, −26, 22) reflect glabrous skin stimulation. All other clusters in the affective touch map reflected a 100% contribution of hairy skin stimulation. Contributions to the right PO cluster (52, −24, 20) from the discriminative touch map (overlaid in green) were exclusively from glabrous skin stimulation. All maps thresholded at FDR (pN) q < 0.001, minimum cluster size 200 mm. All coordinates reported in MNI space.

Figure 3

Task‐ and stimulus‐independent network co‐activation likelihoods as revealed by meta‐analytic connectivity modeling (MCAM) analysis. Left panel: Regions with a significant likelihood of co‐activation with the posterior insula seed region defined by the affective > discriminative touch ALE map, encompassing clusters in somatosensory regions and insula (red; see Table 3). Regions with a significant likelihood of co‐activation with the primary somatosensory seed region defined by the discriminative > affective touch ALE map, encompassing clusters in somatosensory and lateral premotor regions (green; see Table 3). Right panel: Regions with a significant likelihood of co‐activation in common between “affective” and “discriminative” seed regions, encompassing somatosensory cortices, anterior insula, and medial premotor regions. MCAM analysis included 406 fMRI contrasts (N = 4913). All maps thresholded at pN < 0.01, minimum cluster size 100 mm.