Elsevier

Brain Research Bulletin

Volume 83, Issue 5, 30 October 2010, Pages 223-231
Brain Research Bulletin

Research report
Passive tactile recognition of geometrical shape in humans: An fMRI study

https://doi.org/10.1016/j.brainresbull.2010.08.001Get rights and content

Abstract

Tactile shape discrimination involves frontal other than somatosensory cortex (Palva et al., 2005 [48]), but it is unclear if this frontal activity is related to exploratory concomitants. In this study, we investigated topographical details of prefrontal, premotor, and parietal areas during passive tactile recognition of 2D geometrical shapes in conditions avoiding exploratory movements. Functional magnetic resonance imaging (fMRI) was performed while the same wooden 2D geometrical shapes were blindly pressed on subjects’ passive right palm in three conditions. In the RAW condition, shapes were pressed while subjects were asked to attend to the stimuli but were not trained to recognize them. After a brief training, in the SHAPE condition subjects were asked to covertly recognize shapes. In the RECOGNITION condition, they were asked to overtly recognize shapes, using response buttons with their opposite hand. Results showed that somatosensory cortex including contralateral SII, contralateral SI, and left insula was active in all conditions, confirming its importance in processing tactile shapes. In the RAW vs. SHAPE contrast, bilateral posterior parietal, insular, premotor, prefrontal, and (left) Broca's areas were more active in the latter. In the RECOGNITION, activation of (left) Broca's area correlated with correct responses. These results suggest that, even without exploratory movements, passive recognition of tactile geometrical shapes involves prefrontal and premotor as well as somatosensory regions. In this framework, Broca's area might be involved in a successful selection and/or execution of the correct responses.

Introduction

Object recognition by touch is a complex and poorly understood process. It involves (i) encoding of elementary microgeometric (roughness, surface texture) and macrogeometric (edges, shape) features, (ii) integration of sensorimotor information, and (iii) association with other multimodal sensory information to create a tactile representation of a semantically defined object [5], [15], [47], [66].

Previous studies have investigated the role of somatosensory systems in the process of tactile object recognition [12], [17], [21], [49], [64]. It has been shown that primary somatosensory cortex (SI) is involved in initial encoding of elementary microgeometric features (roughness, surface texture), by means of low-level shape feature extraction and coding [4], [47]. Bilateral secondary somatosensory cortex (SII) and inferior parietal lobule (IPL) [56], [68], [78] are crucial for the processing of macrogeometric features, e.g. edges, shape [52], [60], integration of sensorimotor information [38], [45], and coordination of sensorimotor information from the two body halves [33]. Insular cortex plays a key role not only in pain and thermal discrimination [8], [71], but also in the memorization, recognition, and recall of tactile information [1], [26], [63].

Previous studies have also shown that a frontal–parietal network including dorso-lateral prefrontal (BA9\46), intraparietal sulcus (IPS; BA5), and IPL (BA40) is involved in the visual [22], [23] and tactile recognition of geometric shapes [2], [5], [40], [56], [67]. In this network, IPS would perform a high-level processing of somatosensory and sensorimotor information [39], [66], and dorso-lateral prefrontal cortex would perform tactile object identification during sequential discrimination based on short-term information storage, retrieval comparison, and decision making [67]. Further evidence that frontal cortex is involved in the recognition of somatosensory stimuli has been provided by magnetoencephalographic techniques [48]. This evidence complements previous findings showing that in a patient with a stroke in right parietal cortex, recognition of somatosensory stimuli was related to the activation of spared parietal and frontal regions of the contralateral side [62]. Furthermore, neural activity of premotor cortex did covary with animals perceptual reports [19]. However, it is unclear to what extent this frontal activity is related to exploratory concomitants of the sensory experience. In the present study, we explored topographical details of prefrontal, premotor, and parietal areas during a passive tactile recognition of 2D geometrical shapes in conditions avoiding exploratory movements. Functional magnetic resonance imaging (fMRI) was performed while wooden 2D geometrical shapes (square, circle, ellipse and triangle) were blindly pressed on subjects’ passive right hand palm in three conditions. In the RAW condition, the shapes were pressed while subjects were asked to attend to the stimuli but were not trained to recognize them. After a brief training session, in the SHAPE condition subjects were asked to covertly recognize the shape without exploratory movements of the hand. In the RECOGNITION condition, the subjects were asked to overtly recognize the shapes by pressing buttons with their opposite hand. It was expected that the contrast RAW vs. SHAPE unveiled the spatial details of the cortical (even frontal?) activation related to the passive recognition of tactile shapes. Furthermore, in the RECOGNITION condition correlation analysis between the cortical activation and correct behavioral responses showed the neural correlates of attentional processes speeding the performance.

Section snippets

Subjects and stimulation procedures

A first group of 30 subjects, 21 males, 9 females, ranging in age from 23 to 38 years (mean age 27.4 ± 4.2 standard deviation, SD), was recruited for behavioral data collection, in order to validate the tactile stimuli used during the fMRI recordings. The stimuli were delivered to the subjects right hand palm by means of four wooden pieces, each having one face with a geometrical shape: a circle (area = 3.14 cm2), a square (area = 2.89 cm2), a triangle (area = 2.71 cm2) and an ellipse (area = 3.07 cm2) (Fig.

Behavioral data

In the pilot experiment, the mean reaction time was 1.7 s (±0.4 SD) s, and the mean percentage of correct response (hit rate) was 67.5% (±23.9% SD). A negative correlation was observed between hit rate and reaction time (r = −0.49, p = 0.005; Pearson's product moment test, N = 30), indicating that the execution of a correct performance occurs with a short reaction time.

In the main experiment, assessment of attentional processes yielded the following results. In the RAW condition all subjects reported

Discussion

As a novelty, the present fMRI study aimed at clarifying the topographic details of the activation of premotor and prefrontal other than somatosensory areas during the passive recognition of 2D geometrical tactile shapes when no exploratory movements are involved. fMRI was performed while wooden 2D geometrical shapes were blindly pressed on subjects’ passive right hand palm in three presentation conditions. In the RAW condition, subjects attended to the somatosensory stimuli (i.e. elementary

Conclusions

In this fMRI study, we explored topographical details of prefrontal and premotor other than parietal areas during a passive recognition of 2D geometrical shapes when no exploratory movements are involved. Results showed that somatosensory cortex including contralateral SII, contralateral SI, and left insula was active in all conditions, confirming its importance in the processing of tactile shape. In the contrast RAW vs. SHAPE, bilateral posterior parietal, insular, premotor, prefrontal, and

Conflict of interest

The authors declare that they have no competing financial interests.

Acknowledgements

We want to thank Prof. Maurizio Corbetta for his valuable suggestions and Mr. Mario Savini for wooden objects realization.

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