High-resolution fMRI investigations of the fingertip somatotopy and variability in BA3b and BA1 of the primary somatosensory cortex

doi:10.1016/j.neuroscience.2016.10.036

Neuroscience

Volume 339, 17 December 2016, Pages 667-677

https://doi.org/10.1016/j.neuroscience.2016.10.036 Get rights and content

Highlights

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Differences in the functional maps of the fingertip somatotopy in BA1 and BA3b.
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Analysis of the functional and anatomical contribution to the variability in the somatotopy.
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Evaluation of left-right symmetry in the fingertip somatotopy.
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Group analysis of the fingertip somatotopy in BA3b and BA1.
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Maximization of fine-scale mapping and statistical sensitivity in group comparisons.

Abstract

The fingertip somatotopy in BA1 and BA3b of monkeys exhibits characteristic differences with a more discrete separation of the body parts in BA3b and a continuous orientation column-like structure in BA1. We present evidence for similar differences in the human somatotopy using BOLD fMRI for the investigations. Though the variability between the individual maps was large, we found a group-wide somatotopic representation in BA3b and BA1. The variability due to anatomical differences was small in our sample. This was demonstrated by comparing exact shortest distances in the individual brains and after nonlinear normalization to the group space template, for the removal of the individual anatomical variability. Distance mapping along Dijkstra paths was found to be a valid approximation to exact shortest paths only in the individual brains. The degree of fine-scale detail mapping was improved if valid surface distances instead of 3D Euclidean distances were applied. A further improvement was achieved by mapping the distances between all neighboring fingertips instead of only the outer fingertips. Taking into account all optimizations we found mirror symmetry of the somatotopy with respect to the interhemispheric gap.

Introduction

S1 consists of four BAs which differ in their cytoarchitectonic properties (Brodmann, 1909). The cortical sensory representation areas of the stimulated body surface were defined as the regions with the largest electrical response amplitude, based on the investigation of single neurons with electrophysiological methods. A separate somatotopic arrangement of the contralateral representation areas was found in BA1 and BA3b, the fingertips lined up sequentially along the postcentral gyrus, with D1 (thumb) located most inferior (Kaas et al., 1979). Optical BOLD imaging was used to reveal the large-scale structure of the activation pattern in monkey cortices invasively based on the hemodynamic coupling to neural activity, exhibiting a modular structure of the representation areas in BA3b (Chen et al., 2001); a structure similar to the continuous V1 visual orientation maps in BA1 (Friedman et al., 2004), where the frequency of the stimulation is the analogous property to the orientation. This corresponds to larger fingertip representations areas in BA1 with a higher overlap compared to BA3b and a more frequent response to multiple fingers of the fingertip areas in BA1, as found in electrophysiological studies (Iwamura et al., 1980, Iwamura et al., 1983b).

fMRI investigations of the human S1 fingertip somatotopy are also based on the BOLD effect and the hemodynamic coupling. The distances between the fingertip positions revealed important associations to behavioral properties in healthy participants and patients. Examples are the associations with the tactile hyper acuity thresholds in healthy participants (Duncan and Boynton, 2007) and CRPS in patients (Di Pietro et al., 2015). In those studies S1 was often not separated into BAs. Recent 7-Tesla fMRI examinations (Besle et al., 2014, Martuzzi et al., 2014) found separate fingertip representations across the BAs in S1 and raised the question whether analogous examinations are possible with 3-Tesla MRI. The cortex in S1 possesses a complex folding pattern (Hopkins et al., 2014). However, the inter finger distances were in most examinations determined using 3D Euclidean distances, which neglect the cortical folding and may obscure fine-scale details. Virtually all fMRI studies on the fingertip somatotopy observed a large inter individual variability. However, whether the observed variability is due to anatomical or functional differences between the participants has not been clarified.

Our examinations address those issues using an automated approach for investigations of the human fingertip somatotopy in BA3b (Pfannmöller et al., 2016) and extended the approach to include BA1. We investigate differences between the fingertip representation in BA1 and BA3b, using cytoarchitectonic probability maps for separation of S1 into BAs (Fischl et al., 2008). In order to maximize the mapping of fine-scale details and to include the cortical anatomy into the distance determination, we compare three different methods for the determination of cortical distances. Exact shortest distances are applied as a gold standard method for the determination of distances along the cortical surface (Balasubramanian et al., 2009). We assess whether Dijkstra (Dijkstra, 1959) or 3D Euclidean distances are valid approximations. Furthermore, we use the nonlinear surface-based FreeSurfer normalization (Fischl et al., 1999) to investigate the relative contribution of the anatomical variability to the total variability of the fingertip distances. This allows us to make inferences about the functional origin of the variability in the somatotopy between participants and on its left- and right-hand symmetry, a central quantity in examinations involving the fingertip somatotopy.

Section snippets

Participants and tactile stimulation

We investigated 18 healthy participants [mean age: 30 ± 11 years; 11 women; average handedness score of 92; range 77–100 (Oldfield, 1971)]. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee, and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The authors declare that they have no actual or potential conflicts of interest with this work. Informed consent

Fingertip representation in BA3b and BA1

Concerning the peak value approach: As shown in Table 1, at least 78% of the participants exhibited artifact-free cortical maps in BA3b, while only 56% of the participants revealed artifact-free maps in BA1. In more than 80% of the valid BA3b maps the fingertips revealed a sequential arrangement along the postcentral gyrus, while there were less than 30% for BA1. The fingertip positions in BA3b were confined to a specific sub region after nonlinear normalization to FSaverage, as depicted in Fig.

Fingertip representation in BA3b and BA1

Previous fMRI investigations focused on the BA-specific somatotopies (Besle et al., 2014, Martuzzi et al., 2014) and noticed a difference between the maps for the fingertip representation across the BAs in S1. We investigated the human fingertip somatotopy of D1, D2 and D3 in BA3b and BA1. An excellent agreement with the expected pattern for the fingertip representations was found in BA3b applying the peak value approach and a good agreement in BA1 in the center of mass approach. Although the

Conclusion

Our results provide support for a modular functional structure in BA3b and an orientation column-like structure analogous to V1 in BA1, as found in monkey cortices. Valid surface distances were found to improve the fine-scale feature mapping in the somatotopy considerably. Application of exact shortest distances and nonlinear normalization allowed disentangling anatomical and functional contributions to the variability in the somatotopy. We found a dominant contribution of functional

Acknowledgements

M. Lotze was funded by a grant from the German Research Community (DFG Lo795/7-1). Markus Oelschläger is acknowledged for assistance during data acquisition. J. P. Pfannmöller participated in data acquisition, data evaluation and preparation of the examinations. M. Greiner and M. Balasubramanian participated in data evaluation. M. Lotze participated in the preparation of the examinations. All authors contributed to the preparation of the manuscript.

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High-resolution fMRI investigations of the fingertip somatotopy and variability in BA3b and BA1 of the primary somatosensory cortex

Highlights

Abstract

Introduction

Section snippets

Participants and tactile stimulation

Fingertip representation in BA3b and BA1

Fingertip representation in BA3b and BA1

Conclusion

Acknowledgements

Clin Neurophysiol

NeuroImage

NeuroImage

NeuroImage

Brain Res

NeuroImage

Neurosci Biobehav R

NeuroImage

Neuropsychologia

NeuroImage

NeuroImage

NeuroImage

NeuroImage

NeuroImage

Magn Reson Imaging

Neuroscience

Exact geodesics and shortest paths on polyhedral surfaces

IEEE T Pattern Anal

Controlling the false discovery rate – a practical and powerful approach to multiple testing

J Roy Stat Soc B Met

Event-related fMRI at 7T reveals overlapping cortical representations for adjacent fingertips in S1 of individual subjects

Hum. Brain Mapp.

Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues

Fine-scale organization of SI (Area 3b) in the squirrel monkey revealed with intrinsic optical imaging

J Neurophysiol