Sensory gating, inhibition control and gamma oscillations in the human somatosensory cortex

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Abstract

Inhibiting the responses to irrelevant stimuli is an essential component of human cognitive function. Pre-attentive auditory sensory gating (SG), an attenuated neural activation to the second identical stimulus, has been found to be related to the performance of higher-hierarchical brain function. However, it remains unclear whether other cortical regions, such as somatosensory cortex, also possess similar characteristics, or if such a relationship is modality-specific. This study used magnetoencephalography to record neuromagnetic responses to paired-pulse electrical stimulation to median nerve in 22 healthy participants. Somatosensory SG ratio and cortical brain oscillations were obtained and compared with the behavioral performance of inhibition control, as evaluated by somatosensory and auditory Go-Nogo tasks. The results showed that somatosensory P35m SG ratio correlated with behavioral performance of inhibition control. Such relationship was also established in relation to the auditory Go-Nogo task. Finally, a higher frequency value of evoked gamma oscillations was found to relate to a better somatosensory SG ability. In conclusion, our data provided an empirical link between automatic cortical inhibition and behavioral performance of attentive inhibition control. This study invites further research on the relationships among gamma oscillations, neurophysiological indices, and behavioral performance in clinical populations in terms of SG or cortical inhibition.

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Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks.

Marlene Bartos, Imre Vida, Peter Jonas (2007)

Gamma frequency oscillations are thought to provide a temporal structure for information processing in the brain. They contribute to cognitive functions, such as memory formation and sensory processing, and are disturbed in some psychiatric disorders. Fast-spiking, parvalbumin-expressing, soma-inhibiting interneurons have a key role in the generation of these oscillations. Experimental analysis in the hippocampus and the neocortex reveals that synapses among these interneurons are highly specialized. Computational analysis further suggests that synaptic specialization turns interneuron networks into robust gamma frequency oscillators.

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Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans.

Suresh D. Muthukumaraswamy, Richard A. E. Edden, Derek K Jones … (2009)

Functional imaging of the human brain is an increasingly important technique for clinical and cognitive neuroscience research, with functional MRI (fMRI) of the blood oxygen level-dependent (BOLD) response and electroencephalography or magnetoencephalography (MEG) recordings of neural oscillations being 2 of the most popular approaches. However, the neural and physiological mechanisms that generate these responses are only partially understood and sources of interparticipant variability in these measures are rarely investigated. Here, we test the hypothesis that the properties of these neuroimaging metrics are related to individual levels of cortical inhibition by combining magnetic resonance spectroscopy to quantify resting GABA concentration in the visual cortex, MEG to measure stimulus-induced visual gamma oscillations and fMRI to measure the BOLD response to a simple visual grating stimulus. Our results demonstrate that across individuals gamma oscillation frequency is positively correlated with resting GABA concentration in visual cortex (R = 0.68; P < 0.02), BOLD magnitude is inversely correlated with resting GABA (R = -0.64; P < 0.05) and that gamma oscillation frequency is strongly inversely correlated with the magnitude of the BOLD response (R = -0.88; P < 0.001). Our results are therefore supportive of recent theories suggesting that these functional neuroimaging metrics are dependent on the excitation/inhibition balance in an individual's cortex and have important implications for the interpretation of functional imaging results, particularly when making between-group comparisons in clinical research.

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Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex.

Richard A. E. Edden, Suresh D. Muthukumaraswamy, Tom Freeman … (2009)

Neuronal orientation selectivity has been shown in animal models to require corticocortical network cooperation and to be dependent on the presence of GABAergic inhibition. However, it is not known whether variability in these fundamental neurophysiological parameters leads to variability in behavioral performance. Here, using a combination of magnetic resonance spectroscopy, magnetoencephalography, and visual psychophysics, we show that individual performance on a visual orientation discrimination task is correlated with both the resting concentration of GABA and the frequency of stimulus-induced gamma oscillations in human visual cortex. Behaviorally, a strong oblique effect was found, with the mean angular threshold for oblique discrimination being five times higher than that for vertically oriented stimuli. Similarly, we found an oblique effect for the dependency of performance on neurophysiological parameters. Orientation detection thresholds were significantly negatively correlated with visual cortex GABA concentration for obliquely oriented patterns (r = -0.65, p < 0.015) but did not reach significance for vertically oriented stimuli (r = -0.39, p = 0.2). Similarly, thresholds for obliquely oriented stimuli were negatively correlated with gamma oscillation frequency (r = -0.65, p < 0.017), but thresholds for vertical orientations were not (r = -0.02, p = 0.9). Gamma oscillation frequency was positively correlated with GABA concentration in primary visual cortex (r = 0.67, p < 0.013). These results confirm the importance of GABAergic inhibition in orientation selectivity and demonstrate, for the first time, that interindividual performance on a simple visual task is linked to neurotransmitter concentration. The results also suggest a key role for GABAergic gamma oscillations in visual discrimination tasks.

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Author and article information

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group

ISSN (Electronic): 2045-2322

Publication date (Electronic): 04 February 2016

Publication date Collection: 2016

Volume: 6

Electronic Location Identifier: 20437

Affiliations

[1 ]Department of Occupational Therapy and Graduate Institute of Behavioral Sciences, Chang Gung University , Taoyuan, Taiwan

[2 ]Healthy Aging Research Center, Chang Gung University , Taoyuan, Taiwan

[3 ]Department of Psychiatry, Chang Gung Memorial Hospital , Taoyuan, Taiwan

[4 ]Institute of Brain Science, National Yang-Ming University , Taipei, Taiwan

[5 ]Brain Research Center, National Yang-Ming University , Taipei, Taiwan

[6 ]Graduate Institute of Applied Physics, National Chengchi University , Taipei, Taiwan

[7 ]Mind, Brain and Learning Center, National Chengchi University , Taipei, Taiwan

[8 ]Department of Medicine, Chang Gung University , Taoyuan, Taiwan

[9 ]Department of Traditional Chinese Medicine, Chang Gung University , Taoyuan, Taiwan

Author notes

[a ] ch.cheng@ 123456mail.cgu.edu.tw or chiahsiung.cheng@ 123456gmail.com

Article

Publisher Item ID: srep20437

DOI: 10.1038/srep20437

PMC ID: 4740805

PubMed ID: 26843358

SO-VID: e7e53e3a-d49a-40c4-ae6b-2dc604c3aaa8

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Sensory gating, inhibition control and gamma oscillations in the human somatosensory cortex

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Gamma Delta T cells

Most cited references 41

Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks.

Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans.

Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex.

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