The importance of the negative blood-oxygenation-level-dependent (BOLD) response in the somatosensory cortex

Klingner, Carsten M.; Brodoehl, Stefan; Witte, Otto W.

doi:10.1515/revneuro-2015-0002

Cited by 13 publications

(8 citation statements)

References 51 publications

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“…This is consistent with previous results showing that the topographically organized finger representations in S1 are subject to complex lateral, mainly inhibitory, intra-areal interactions (Ruben et al, 2006;Lipton et al, 2010;Reed et al, 2010;Thakur et al, 2012;Martuzzi et al, 2014). For the controls, the BOLD activity in these representations also showed negative values when the fingers of the right hand received the tactile stimuli ( Figure 4A, filled gray bars representing Ind R and Litt R stimulation), which is consistent with previous observations on BOLD responses in S1 during ipsilateral hand stimulations in healthy adults (Hlushchuk and Hari, 2006;Klingner et al, 2015;Tal et al, 2017). A dominant explanation is that signals from S1 contralateral to a stimulated hand are transmitted to the ipsilateral hemisphere via callosal connections between higher order somatosensory areas (BA 1, 2 and secondary somatosensory cortex) and feedback connections to area 3b mediate the suppressive effects through local activation of inhibitory neurons (Tommerdahl et al, 2006;Reed et al, 2011;Klingner et al, 2015).…”

Section: Effect Of Injury In the Primary Somatosensory Cortex (S1)supporting

confidence: 92%

“…However, injury related changes in cortical responses to tactile input from non-median innervated skin areas within the affected hand can be expected since the activity within S1's finger representations dynamically interact under normal conditions (Ruben et al, 2006;Lipton et al, 2010;Reed et al, 2010;Thakur et al, 2012;Martuzzi et al, 2014). Likewise, effect of injury on responses to inputs from the hand of the non-injured arm can be expected since stimulation of one hand can not only give rise to contralateral cortical responses, but also to ipsilateral activity changes in healthy individuals, including within S1 (Hlushchuk and Hari, 2006;Klingner et al, 2015;Tamè et al, 2016;Tal et al, 2017). We tested these propositions by tactile stimulation targeting the tip of the index finger innervated by the reinnervated median nerve, but also the tip of the little finger of the same hand innervated by the uninjured ulnar nerve and the tips of the index and little fingers of the other unaffected hand.…”

Section: Introductionmentioning

confidence: 99%

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Disinhibition of Human Primary Somatosensory Cortex After Median Nerve Transection and Reinnervation

Nordmark

Johansson

2020

Front. Hum. Neurosci.

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Despite state-of-the-art surgical and postoperative treatment, median nerve transection causes lasting impaired hand function due to limitations in the nerve's reinnervation ability. The defective innervation and thus controllability of the affected hand can shape the brain's control of manual behaviors. Earlier studies of changes in the processing of tactile stimuli have focused mainly on stimulation of the reinnervated hand and lack sufficient control over the brain's use of the tactile input in perceptual terms. Here we used fMRI to measure brain activity (BOLD-signal) in 11 people with median nerve injury and healthy controls (N = 11) when performing demanding tactile tasks using the tip of either the index or little finger of either hand. For the nerve-injured group, the left median nerve had been traumatically transected in the distal forearm and surgically repaired on average 8 years before the study. The hand representation of their contralesional (right) primary somatosensory cortex (S1) showed greater activity compared to controls when the left reinnervated index finger was used, but also when the left-hand little finger and the fingers of the right hand innervated by uninjured nerves were used. We argue that the overall increase in activity reflects a general disinhibition of contralesional S1 consistent with an augmented functional reorganizational plasticity being an ongoing feature of chronic recovery from nerve injury. Also, the nerve-injured showed increased activity within three prefrontal cortical areas implicated in higher-level behavioral processing (dorsal anterior cingulate cortex, left ventrolateral prefrontal and right dorsolateral prefrontal cortex), suggesting that processes supporting decisionmaking and response-selection were computationally more demanding due to the compromised tactile sensibility.

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Section: Effect Of Injury In the Primary Somatosensory Cortex (S1)supporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Disinhibition of Human Primary Somatosensory Cortex After Median Nerve Transection and Reinnervation

Nordmark

Johansson

2020

Front. Hum. Neurosci.

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“…Ipsilateral SM1 deactivation has been reported during a unimanual motor task in younger adults (Allison et al , ; Newton et al , ; Marchand et al , ; Hayashi et al , ). Similarly, electrical stimulation of the right median nerve may also cause ipsilateral deactivation in the primary somatosensory cortex, which has been proposed to reflect functional inhibition in the somatosensory system (Kastrup et al , ; Klingner et al , ; ; Schäfer et al , ; Gröschel et al , ).…”

Section: Discussionmentioning

confidence: 99%

Developmental Changes in Task‐Induced Brain Deactivation in Humans Revealed by a Motor Task

Morita

Asada

Naito

2019

Developmental Neurobiology

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Performing tasks activates relevant brain regions in adults while deactivating task‐irrelevant regions. Here, using a well‐controlled motor task, we explored how deactivation is shaped during typical human development and whether deactivation is related to task performance. Healthy right‐handed children (8–11 years), adolescents (12–15 years), and young adults (20–24 years; 20 per group) underwent functional magnetic resonance imaging with their eyes closed while performing a repetitive button‐press task with their right index finger in synchronization with a 1‐Hz sound. Deactivation in the ipsilateral sensorimotor cortex (SM1), bilateral visual and auditory (cross‐modal) areas, and bilateral default mode network (DMN) progressed with development. Specifically, ipsilateral SM1 and lateral occipital deactivation progressed prominently between childhood and adolescence, while medial occipital (including primary visual) and DMN deactivation progressed from adolescence to adulthood. In adults, greater cross‐modal deactivation in the bilateral primary visual cortices was associated with higher button‐press timing accuracy relative to the sound. The region‐specific deactivation progression in a developmental period may underlie the gradual promotion of sensorimotor function segregation required in the task. Task‐induced deactivation might have physiological significance regarding suppressed activity in task‐irrelevant regions. Furthermore, cross‐modal deactivation develops to benefit some aspects of task performance in adults.

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“…In the POR region, the overshoot part following the initial dip in oximetric signal is considered as an equivalence to the positive BOLD response 38 43 44 . In the NOR region, The undershoot part following the initial transient increase is relevant to the negative BOLD response 45 and may be caused by an overcompensation of decreased CBV and CBF for the reduction in energy consumption due to suppressed neuronal activity 19 20 21 45 . Decreases in CBV and CBF had been confirmed in our study.…”

Section: Discussionmentioning

confidence: 99%

“…Inhibition is ubiquitous in visual cortical neurons and stimulus-evoked hemodynamic signals are dependent on the interactions between neuronal excitation and inhibition 2 . Compared to the POR region, the greater inhibitory activity in the NOR region may change the balance between excitatory and inhibitory effects and produce a net inhibition 2 45 55 . The cortical depth of 500–600 μm belongs to the layer 4 which has the most dense vascularization 56 .…”

Section: Discussionmentioning

confidence: 99%

Inverted optical intrinsic response accompanied by decreased cerebral blood flow are related to both neuronal inhibition and excitation

Cao

Sun

et al. 2016

Sci Rep

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Negative hemodynamic response has been widely reported in blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging studies, however its origin is still controversial. Optical intrinsic signal (OIS) imaging can be used to study brain activity by simultaneously recording hemodynamic signals at different wavelengths with high spatial resolution. In this study, we found transcorneal electrical stimulation (TcES) could elicit both positive OIS response (POR) and negative OIS response (NOR) in cats’ visual cortex. We then investigated the property of this negative response to TcES and its relationship with cerebral blood flow (CBF) and neuronal activity. Results from laser speckle contrast imaging showed decreased CBF in the NOR region while increased CBF in the POR region. Both planar and laminar electrophysiological recordings in the middle (500–700 μm) cortical layers demonstrated that decreased and increased neuronal activities were coexisted in the NOR region. Furthermore, decreased neuronal activity was also detected in the deep cortical layers in the NOR region. This work provides evidence that the negative OIS together with the decreased CBF should be explained by mechanisms of both neuronal inhibition and excitation within middle cortical layers. Our results would be important for interpreting neurophysiological mechanisms underlying the negative BOLD signals.

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The importance of the negative blood-oxygenation-level-dependent (BOLD) response in the somatosensory cortex

Cited by 13 publications

References 51 publications

Disinhibition of Human Primary Somatosensory Cortex After Median Nerve Transection and Reinnervation

Disinhibition of Human Primary Somatosensory Cortex After Median Nerve Transection and Reinnervation

Developmental Changes in Task‐Induced Brain Deactivation in Humans Revealed by a Motor Task

Inverted optical intrinsic response accompanied by decreased cerebral blood flow are related to both neuronal inhibition and excitation

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