Functional characterization of human second somatosensory cortex by magnetoencephalography

doi:10.1016/S0166-4328(02)00143-2

Behavioural Brain Research

Volume 135, Issues 1–2, 20 September 2002, Pages 141-145

https://doi.org/10.1016/S0166-4328(02)00143-2 Get rights and content

Abstract

Magnetoencephalographic (MEG) recordings allow noninvasive monitoring of simultaneously active brain areas with reasonable spatial and excellent temporal resolution. Whole-scalp neuromagnetic recordings show activation of contralateral primary (SI) and bilateral second (SII) somatosensory cortices to unilateral median nerve stimulation. Recent MEG studies on healthy and diseased human subjects have shown some functional characteristics of SII cortex. Besides tactile input, the SII cortex also responds to nociceptive afferents. The SII activation is differentially modulated by isometric muscle contraction of various body parts. Lesions in the SII cortex may disturb the self-perception of body scheme. Moreover, the SI and SII cortices may be sequentially activated within one hemisphere, but the SII cortex may also receive direct peripheral input on the ipsilateral side.

Introduction

In magnetoencephalographic (MEG) measurements, weak magnetic fields generated by cerebral currents can be detected outside the head with superconducting sensors [9], [10]. The spatial resolution of MEG for cortical sources is a few millimeters under favourable conditions, and the temporal resolution is better than a millisecond. MEG is well suited for exploration of various brain regions embedded within cortical sulci and, thus, complements the study of somatosensory cortical functions by other methods. The second somatosensory cortex (SII) is located deep in the Sylvian fissure, and its function is not completely understood.

In this article, we focused on functional characterization of SII cortex studied with a whole-scalp 122-channel-Neuromag-122™ [6], [7], [15], [16] or a 306-channel Vectorview™ [20]. During the recording, the subject was sitting comfortably in a magnetically shielded room with the head leaning against the helmet-shaped neuromagnetometer. The exact location of the head with respect to the sensors was measured with the aid of 3–4 head indicator coils placed at known sites on the scalp. The locations of the coils with respect to anatomical landmarks on the head were determined with a 3-D digitizer to allow alignment of the MEG and magnetic resonance (MR) image coordinate systems. MR images of the subject's brain were acquired with a 1.5-T Siemens Magnetom™ scanner.

Section snippets

Somatosensory evoked fields from the SII cortex

Figure 1 shows somatosensory evoked fields of one healthy subject to electric stimuli presented to the right median nerve at the wrist with a 2 s interstimulus interval (ISI). The signal distribution indicates that the stimuli activate several source areas. In line with previous MEG studies [2], [6], [13], [20], [28], the earliest deflection N20m occurs over the left anterior parietal cortex, followed by P30m at 31 ms. Longer-latency responses peak at 86 and 110 ms over the left and right

Sensorimotor integration

Monkey studies have shown that SII cortex may play a role in the learning of manual skills [25]. In humans, electrical stimulation of the cortex close to SII area may disturb motor activity [22]. SII cortex has been suggested to provide an important link between sensory inputs and motor cortex [3].

Figure 3 shows that SII responses are differently affected by isometric contraction of various body parts [20]. In agreement with a previous study [6], SII responses were enlarged during isometric

Perception of unified body image

Unitary bodily awareness depends on a stable body scheme. Brain insults may change the normal perception of unified body image. A recent paper from our laboratory [16] described a 37-year-old female who developed a right frontal lobe lesion and fragmented awareness of body image after operation of a ruptured aneurysm of left pericallosal artery. Several times a day, she sensed a third arm on the left side of her body. Repeated MEG recordings showed that the SII responses were dampened 50%

Processing of noxious information

The roles of SII cortex in pain perception have been explored with MEG recordings by various nociceptive stimuli: electric stimulation of the dental pulp, CO₂ pulses delivered to the nasal mucosa and painful CO₂ laser of the skin [12], [15], [17], [19]. Nonpainful stimulation of visceral esophageal afferents can elicit SII responses bilaterally, but there is no clear SI activation. It seems that both noxious and visceral stimuli may activate the SII cortices directly (for a review see ref [11]).

Serial versus parallel processing of tactile information

The somatosensory cortical areas form a complex network. Serial versus parallel processing of somatosensory inputs between SI and SII cortices has been under debate [23], [24], [26]. In human MEG studies, the earliest SI response to median nerve stimulation peaks at 20 ms and may continue for 100–180 ms. Activation of SII usually peaks at 70–100 ms and may continue long up to 200 ms. The temporal characteristics would be compatible with serial processing of somatosensory information from SI to

Conclusion

Excellent temporal resolution combined with the ability to detect activity of fissural cortex makes MEG a suitable tool for studies of the somatosensory network. Recent MEG studies have shown that SII cortex plays an important role in sensorimotor integration, maintenance of body image and processing of noxious and visceral input. MEG recordings on stroke patients also imply that the SII cortex may receive direct input from the periphery. In the future, further MEG studies will bring a better

Acknowledgements

This work was supported in part by the Academy of Finland (N.F.), and research grants VGH-90-443-(3) from Taipei Veterans General Hospital (Y.Y.L.), Taipei, Taiwan. We thank Professor Riitta Hari for valuable comments on the manuscript.

References (28)

N. Forss et al.
Comparison of somatosensory evoked fields to airpuff and electric stimuli
Electroencephalogr. Clin. Neurophysiol.
(1994)
N. Forss et al.
Sensorimotor integration in human primary and secondary somatosensory cortices
Brain Res.
(1998)
R. Hari et al.
Neuromagnetic localization of cortical activity evoked by painful dental stimulation in man
Neurosci. Lett.
(1983)
R. Hari et al.
Somatosensory evoked cerebral magnetic fields from SI and SII in man
Electroencephalogr. Clin. Neurophysiol.
(1984)
R. Hari et al.
Separate finger representations at the human second somatosensory cortex
Neuroscience
(1990)
R. Hari et al.
Right-hemisphere preponderance of responses to painful CO₂ stimulation of the human nasal mucosa
Pain
(1997)
R. Hari et al.
Three hands: Fragmentation of human bodily awareness
Neurosci. Lett.
(1998)
J. Huttunen et al.
Cortical responses to painful CO₂ stimulation of nasal mucosa; a magnetoencephalographic study in man
Electroencephalogr. Clin. Neurophysiol.
(1986)
R. Kakigi et al.
Pain-related magnetic fields following painful CO₂ laser stimulation in man
Neurosci. Lett.
(1995)
Y.-Y. Lin et al.
Differential effects of muscle contraction from various body parts on neuromagnetic somatosensory responses
Neuroimage
(2000)

F. Mauguière et al.

Activation of a distributed somatosensory cortical network in the human brain. A dipole modeling study of magnetic fields evoked by median nerve stimulation. Part I: Location and activation timing of SEF sources

Electroencephalogr. Clin. Neurophysiol.

(1997)

R.M. Ridley et al.

Impaired tactile learning and retention after removals of the second somatic sensory projection cortex (SII) in the monkey

Brain Res.

(1976)

C. Simões et al.

Relationship between responses to contra- and ispilateral stimuli in the human second somatosensory cortex SII

Neuroimage

(1999)

J. Tiihonen et al.

Early deflections of cerebral magnetic responses to median nerve stimulation

Electroencephalogr. Clin. Neurophysiol.

(1989)

Cited by (62)

Neuromagnetic oscillations in the human sensory systems: A mini review of our series and literature
2020, Neuroscience Research
Oscillatory neuronal (electrical) activity in defined frequency ranges supports synchronous interactions between anatomically distinct regions of the human brain during cognitive tasks. Here, the author reviews our previous studies that focused on the neuromagnetic oscillations in the sensory systems in response to the external stimuli in normal healthy subjects and neurological disorders. A magnetoencephalography was applied to evaluate the neuromagnetic oscillations in humans. We have demonstrated that the oscillatory gamma synchronization binds the primary and secondary somatosensory areas (S1 and S2) in humans. This functional coupling is modulated by aging. In people who stutter, functional and structural reorganization of the right auditory cortex appears to be a compensatory mechanism for impaired left auditory cortex function. This may be partly caused by increased right hemispheric local phase synchronization and increased inter-hemispheric phase synchronization. We have also found that the hippocampus modulates auditory processing differently under normal conditions and in epileptic patients with hippocampal sclerosis. This indicates that altered neural synchronization may provide useful information about possible functional deterioration in patients with unilateral mesial temporal lobe epilepsy. Finally, supraspinal (cortical) mechanism is responsible for pain perception and pain relief via neural oscillations. Together, neuronal synchronization plays an important role in distributed cortico-cortical processing.
The motor engram as a dynamic change of the cortical network during early sequence learning: An fMRI study
2020, Neuroscience Research
Citation Excerpt :
Seed-based functional connectivity analysis of the resting epoch of the maximum blocks revealed that the connectivity between left aIPS and IPL was enhanced as learning proceeded. The IPL (BA 40) has been linked to the sensorimotor integration processes (Caminiti et al., 1996; Rizzolatti et al., 1997; for a review see Wise et al., 1997; Huttunen et al., 1996; Forss and Jousmakï, 1998; Lin and Forss, 2002), as well as encoding of sequence-specific information (Honda et al., 1998; Rauch et al., 1995; Sakai et al., 1998). Parietal lesions, particularly on the left side, are implicated in apraxia, the inability to execute previously learned movements (Halsband and Lange, 2006; Wheaton and Hallett, 2007; Halsband et al., 2001).
Neural substrates of motor engrams in the human brain are hard to identify because their dormant states are difficult to discriminate. We utilized eigenvector centrality (EC) to measure the network information that accumulates as an engram during learning. To discriminate engrams formed by emphasis on speed or accuracy, we conducted functional MRI on 58 normal volunteers as they performed a sequential finger-tapping task with the non-dominant left hand. Participants alternated between performing a tapping sequence as quickly as possible (maximum mode) or at a constant speed of 2 Hz, paced by a sequence-specifying visual cue (constant mode). We depicted the formation of the motor engram by characterizing the dormant state as the increase in EC of the resting epoch throughout the training course, and the ecphory, or activated state, as the increment in EC during the task epoch relative to the alternated resting epoch. We found that a network covering the left anterior intraparietal sulcus and inferior parietal lobule represented the engram for the speed of execution, whereas bilateral premotor cortex and right primary motor cortex represented the sequential order of movements. This constitutes the first demonstration of learning-mode specific motor engrams formed by only 30 min of training.
Altered functional connectivity between primary and secondary somatosensory areas in panic disorder
2020, Psychiatry Research
Disturbance in the interpretation of bodily sensation has been widely reported in patients with panic disorder (PD). However, it remains substantially unknown whether patients with PD exhibit any defect in cortical somatosensory processing of non-threatening stimuli. Thus, the present study aimed to examine the functional integrity of the cortical somatosensory system in patients with PD using neurophysiological recordings. A total of 20 patients with PD and 20 healthy controls (HC) were recruited to investigate the cortical responses to median nerve stimulation through whole-head magnetoencephalographic (MEG) imaging. To comprehensively investigate all somatosensory functioning, we studied the regional activation of the primary somatosensory cortex (SI), contralateral (SIIc), and ipsilateral (SIIi) secondary somatosensory cortices, as well as functional connectivity among the SI, SIIc, and SIIi in alpha, beta, and gamma frequency bands. We found that patients with PD demonstrated a reduction in SI activity compared with those in the HC group. Furthermore, a significantly weaker gamma-band functional connectivity between SI and SIIc was found in the PD group relative to the HC group. Our data suggest that patients with PD exhibit abnormal responses to non-threatening (i.e., pain-free) stimuli in the cortical somatosensory system.
Maladaptive change of body representation in the brain after damage to central or peripheral nervous system
2016, Neuroscience Research
Our brain has great flexibility to cope with various changes in the environment. Use-dependent plasticity, a kind of functional plasticity, plays the most important role in this ability to cope. For example, the functional recovery of paretic limb motor movement during post-stroke rehabilitation depends mainly on how much it is used. Patients with hemiparesis, however, tend to gradually disuse the paretic limb because of its motor impairment. Decreased use of the paretic hand then leads to further functional decline brought by use-dependent plasticity. To break this negative loop, body representation, which is the conscious and unconscious information regarding body state stored in the brain, is key for using the paretic limb because it plays an important role in selecting an effector while a motor program is generated. In an attempt to understand body representation in the brain, we reviewed animal and human literature mainly on the alterations of the sensory maps in the primary somatosensory cortex corresponding to the changes in limb usage caused by peripheral or central nervous system damage.
Age-related changes across the primary and secondary somatosensory areas: An analysis of neuromagnetic oscillatory activities
2014, Clinical Neurophysiology
Citation Excerpt :
In addition, it has been suggested that SII is unique in having dual afferent pathways. Several neurophysiological and anatomical studies have reported that SII receives input from SI as well as the thalamus (Karhu and Tesche, 1999; Lin and Forss, 2002; Raij et al., 2008; Zhang et al., 1996, 2001a, 2001b). A previous SEF study demonstrated an age-related reduction in source-wave amplitudes of SII using multi-dipole analysis (Stephen et al., 2006).
Age-related changes are well documented in the primary somatosensory cortex (SI). Based on previous somatosensory evoked potential studies, the amplitude of N20 typically increases with age probably due to cortical disinhibition. However, less is known about age-related change in the secondary somatosensory cortex (SII). The current study quantified age-related changes across SI and SII mainly based on oscillatory activity indices measured with magnetoencephalography.
We recorded somatosensory evoked magnetic fields (SEFs) to right median nerve stimulation in healthy young and old subjects and assessed major SEF components. Then, we evaluated the phase-locking factor (PLF) for local field synchrony on neural oscillations and the weighted phase-lag index (wPLI) for cortico-cortical synchrony between SI and SII.
PLF was significantly increased in SI along with the increased amplitude of N20m in the old subjects. PLF was also increased in SII associated with a shortened peak latency of SEFs. wPLI analysis revealed the increased coherent activity between SI and SII.
Our results suggest that the functional coupling between SI and SII is influenced by the cortical disinhibition due to normal aging.
We provide the first electrophysiological evidence for age-related changes in oscillatory neural activities across the somatosensory areas.
Neural Coordination of Cooperative Hand Movements: Implications for Rehabilitation Technology
2022, Neurorehabilitation Technology, Third Edition

View all citing articles on Scopus

View full text

Research reportFunctional characterization of human second somatosensory cortex by magnetoencephalography

Abstract

Introduction

Section snippets

Somatosensory evoked fields from the SII cortex

Sensorimotor integration

Perception of unified body image

Processing of noxious information

Serial versus parallel processing of tactile information

Conclusion

Acknowledgements

Electroencephalogr. Clin. Neurophysiol.

Brain Res.

Neurosci. Lett.

Electroencephalogr. Clin. Neurophysiol.

Neuroscience

Pain

Neurosci. Lett.

Electroencephalogr. Clin. Neurophysiol.

Neurosci. Lett.

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

Brain Res.

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

Research report
Functional characterization of human second somatosensory cortex by magnetoencephalography