Elsevier

NeuroImage

Volume 25, Issue 4, 1 May 2005, Pages 1292-1301
NeuroImage

Functional representation of the finger and face in the human somatosensory cortex: intraoperative intrinsic optical imaging

https://doi.org/10.1016/j.neuroimage.2004.12.049Get rights and content

Abstract

We applied the intrinsic optical imaging technique to the human primary somatosensory cortex during brain tumor/epilepsy surgery for nine patients. The cortical surface was illuminated with a Xenon light through an operating microscope, and the reflected light, which passed through a 605 nm bandpass filter, was detected by a CCD camera-based optical imaging system. Individual electrical stimulation of five digits induced changes in the reflected light intensities. Visualizing the intrinsic optical responses, we constructed maps of finger representation in Brodmann's area 1. In the maps, response areas of Digits I to V were sequentially aligned along the central sulcus in the crown of the postcentral gyrus from the latero-inferior region (Digit I) to the medio-superior region (Digit V). The neighboring response areas partially overlapped each other, as previously described in the monkey somatosensory cortex. Similar results were obtained in the face region with stimulation of the three branches of the trigeminal nerve. These results suggest that the overlap of the response areas is a common feature in the somatosensory cortex not only in monkeys, but also in humans.

Introduction

Intrinsic optical imaging is a useful technique for monitoring brain function with high spatial and temporal resolutions (Bonhoeffer and Grinvald, 1996). Since the pioneering work by Grinvald et al. (1986), it has been applied to the cat/monkey visual cortex (Bonhoeffer and Grinvald, 1993, Chapman et al., 1996, Gödecke and Bonhoeffer, 1996, Ts'o et al., 1990), the rodent somatosensory cortex (Dowling et al., 1996, Gochin et al., 1992, Masino et al., 1993, Tanaka et al., 2000, Yazawa et al., 2001), and the rodent spinal cord (Sasaki et al., 2002, Sasaki et al., 2003). The intrinsic optical signals (changes in reflected light intensity) are considered to consist of three different components: they originate from (1) activity-dependent changes in the oxygen saturation level of hemoglobin, (2) changes in blood volume in an area containing electrically active neurons, and (3) light-scattering changes that accompany cortical activation, which are caused by ion/water movement, expansion and contraction of extracellular spaces, capillary expansion, or neurotransmitter release (Bonhoeffer and Grinvald, 1996, Cohen, 1973, Frostig et al., 1990, Malonek and Grinvald, 1996).

The intrinsic optical imaging technique was also applied to the human cortex during neurosurgical operations. Haglund et al. (1992) first demonstrated the usefulness of this technique for monitoring stimulation-evoked epileptiform afterdischarges and cognitively-evoked functional activity. Subsequently, it was used to monitor brain functions related to sensation (Cannestra et al., 1998, Sato et al., 2002, Shoham and Grinvald, 2001, Toga et al., 1995) and language tasks (Cannestra et al., 2000, Pouratian et al., 2000). In most studies of sensation, optical signals were evoked by median/ulnar nerve stimulation or digit stimulation. Although these studies showed that different peripheral stimulation provided different functional maps, contiguous representation of fine receptive fields, such as response areas of the five digits, was not assessed.

The purpose of this study was to examine functional representation of the finger area in the human primary somatosensory cortex. In the human somatosensory cortex, Penfield and Boldray (1937) first described a somatosensory homunculus on the postcentral gyrus. In the monkey, using a micro-electrode recording technique, Kaas et al. (1979) showed that complete somatotopic maps also present in each Brodmann's area (3a, 3b, 1, and 2). In the monkey somatosensory cortex, significant overlaps of functional representation of the fingers were described in somatotopic maps, and we questioned whether similar overlaps exist in the human brain. In the present study, we also examined functional representation of the three branches of the trigeminal nerve, and compared the data between the finger and face regions.

Section snippets

Subjects

We measured intrinsic optical signals from the somatosensory cortex in nine anesthetized patients undergoing surgery for frontal, parietal, or temporal lobe brain tumors (eight patients) and temporal lobe epilepsy (one patient). The patient data are summarized in Table 1. The patients had no past history of neurosurgical operations. All the patients were right-handed. Informed consent was obtained from all patients prior to the surgery and intraoperative intrinsic optical imaging. The patients

Optical responses induced by Digits I–V stimulation

Fig. 1 shows intrinsic optical images obtained from a 47-year-old patient who suffered from an oligodendroglioma (Case 9 in Table 1). All of the right digits (Digits I–V) were stimulated individually by ring-like electrodes, and intrinsic optical signals (optical reflectance changes) were detected from the left somatosensory cortex. Prior to the intrinsic optical recording, we recorded cortical somatosensory-evoked potentials (SEPs) in response to right median nerve stimulation to identify the

Discussion

In the present study, we performed intraoperative intrinsic optical imaging for nine patients, and succeeded in recording optical responses from eight patients as shown in Table 1. From six patients, we could obtain clear functional maps of the finger or face area in the somatosensory cortex. We discuss here the functional representation of the finger and face in the somatosensory cortex, and also consider a limitation in the application of intraoperative intrinsic optical imaging.

Acknowledgments

We are grateful to Dr. Amiram Grinvald for generous help in constructing the optical recording apparatus, and to reviewers for their helpful comments about our manuscript. We also wish to express our gratitude to Drs. Kohtaro Kamino and Kimiyoshi Hirakawa for helpful discussions throughout the course of our work, and many medical doctors and nurses for their kind cooperation in the operating room. This research was supported by grants from the Monbu-Kagaku-Sho of Japan and research funds from

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