Elsevier

NeuroImage

Volume 57, Issue 2, 15 July 2011, Pages 462-475
NeuroImage

Dual pathways for haptic and visual perception of spatial and texture information

https://doi.org/10.1016/j.neuroimage.2011.05.001Get rights and content

Abstract

Segregation of information flow along a dorsally directed pathway for processing object location and a ventrally directed pathway for processing object identity is well established in the visual and auditory systems, but is less clear in the somatosensory system. We hypothesized that segregation of location vs. identity information in touch would be evident if texture is the relevant property for stimulus identity, given the salience of texture for touch. Here, we used functional magnetic resonance imaging (fMRI) to investigate whether the pathways for haptic and visual processing of location and texture are segregated, and the extent of bisensory convergence. Haptic texture-selectivity was found in the parietal operculum and posterior visual cortex bilaterally, and in parts of left inferior frontal cortex. There was bisensory texture-selectivity at some of these sites in posterior visual and left inferior frontal cortex. Connectivity analyses demonstrated, in each modality, flow of information from unisensory non-selective areas to modality-specific texture-selective areas and further to bisensory texture-selective areas. Location-selectivity was mostly bisensory, occurring in dorsal areas, including the frontal eye fields and multiple regions around the intraparietal sulcus bilaterally. Many of these regions received input from unisensory areas in both modalities. Together with earlier studies, the activation and connectivity analyses of the present study establish that somatosensory processing flows into segregated pathways for location and object identity information. The location-selective somatosensory pathway converges with its visual counterpart in dorsal frontoparietal cortex, while the texture-selective somatosensory pathway runs through the parietal operculum before converging with its visual counterpart in visual and frontal cortex. Both segregation of sensory processing according to object property and multisensory convergence appear to be universal organizing principles.

Research highlights

► Dual pathways for location and texture in somatosensory and visual systems. ► Somatosensory and visual location pathways converge in dorsal frontoparietal cortex. ► Somatosensory texture pathway runs through parietal operculum. ► Somatosensory and visual texture pathways converge in visual and frontal cortex.

Section snippets

Subjects

Eighteen subjects (eleven male, seven female) took part in the study after giving informed consent. All were right-handed as assessed by the high-validity subset of the Edinburgh handedness questionnaire (Raczkowski et al., 1974), were neurologically normal, and had vision that was normal or corrected to normal with contact lenses. Subjects with callused fingerpads or a history of injury to the upper extremity were excluded. Ages ranged from 18–23 years, with a mean age of 20.8.

Haptic

The haptic

Behavioral

Accuracy (mean % correct ± SEM) was 81.4 ± 2.8% in the VT task, 91.1 ± 1.9% in the visual location VL task, 87.7 ± 2.0% in the haptic texture HT task and 84.4 ± 1.9% in the haptic location HL task. An ANOVA showed no main effect of either modality (F1,17 = .01; p = .91) or task (F1,17 = 3.3; p = .09), but there was a significant interaction between these two factors (F1,17 = 761.2; p < .001). Paired t-tests (Bonferroni-corrected) showed significant differences between VT/VL (t17 =  3.8; p = 0.001) and between VL/HL (t17 =

Discussion

Analysis of the behavioral data obtained during scanning showed that subjects performed at a high level of accuracy, i.e. above 80% correct in all tasks. Although accuracy on the VL task was significantly higher than in either the VT or HL tasks, this did not impact the activations, since voxels independently identified as showing correlations (positive or negative) between activation magnitude and accuracy in each task were essentially non-overlapping with the corresponding activation maps.

Conclusions

The present study establishes the existence of dual pathways for processing location and texture in both the somatosensory and the visual system. The texture pathways proceed from modality-specific regions without task-selectivity through regions specific for both modality and texture to texture-selective bisensory regions. The location pathways also originate in modality-specific regions lacking task-selectivity, but project directly to location-selective unisensory and bisensory regions. Both

Acknowledgments

This work was supported by research grants from the NIH (R01 EY12440 and K24 EY17332 to K.S., and R01 EB002009 to X.H.). Support to K.S. from the Veterans Administration is also gratefully acknowledged.

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