Mapping quantal touch using 7 Tesla functional magnetic resonance imaging and single-unit intraneural microstimulation

Panchuelo, Rosa M. Sanchez; Ackerley, Rochelle; Glover, Paul; Bowtell, Richard; Wessberg, Johan; Francis, Susan T.; McGlone, Francis

doi:10.7554/elife.12812

Cited by 38 publications

(56 citation statements)

References 46 publications

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“…Functional MRI signal changes in S1 show a linear arrangement of individual digits ( Fig. 1) as previously described in high-resolution fMRI (Olman 2012;Panchuelo 2016;Kolasinsky 2016;Schluppeck 2017;Siero 2014;Ejaz 2015). The distance between the representations of the thumb and the little finger in S1 is 16 ± 4 mm.…”

Section: Resultssupporting

confidence: 74%

Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex

Huber¹,

Finn²,

Handwerker³

et al. 2018

Preprint

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The human brain coordinates a wide variety of motor activities. On a large scale, the cortical motor system is topographically organized such that neighboring body parts are represented by neighboring brain areas. This homunculus-like somatotopic organization along the central sulcus has been observed using neuroimaging for large body parts such as the face, hands and feet. However, on a finer scale, invasive electrical stimulation studies show deviations from this somatotopic organization that suggest an organizing principle based on motor actions rather than body part moved. It has not been clear how the action-map organization principle of the motor cortex in the mesoscopic (sub-millimeter) regime integrates into a body map organization principle on a macroscopic scale (cm). Here we developed and applied advanced mesoscopic (sub-millimeter) fMRI and analysis methodology to non-invasively investigate the functional organization topography across columnar and laminar structures in humans. We find that individual fingers have multiple mirrored representations in the primary motor cortex depending on the movements they are involved in. We find that individual digits have cortical representations up to 3 mm apart from each other arranged in a column-like fashion. These representations are differentially engaged depending on whether the digits' muscles are used for different motor actions such as flexion movements like grasping a ball or retraction movements like releasing a ball. This research provides a starting point for noninvasive investigation of mesoscale topography across layers and columns of the human cortex and bridges the gap between invasive electrophysiological investigations and large coverage noninvasive neuroimaging. high-resolution fMRI | motor cortex | cortical layers | cortical columns | VASO

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Section: Resultssupporting

confidence: 74%

Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex

Huber¹,

Finn²,

Handwerker³

et al. 2018

Preprint

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“…Without spatial smoothing, methods to best deal with differences in brain anatomy become vital to minimise inter‐subject spatial variability, especially for higher‐order cognitive areas for which anatomical variability is greater than for primary sensory areas (Turner & Geyer, ). Minimal anatomical variability in primary sensory cortex may, in part, explain the successes of UHF high spatial resolution studies of sensorimotor and visual cortex (Goncalves et al, ; Kemper et al, ; Poltoratski et al, ; Rua et al, ; Sanchez Panchuelo et al, ; Sanchez Panchuelo et al, ; Sanchez‐Panchuelo et al, ). Indeed, our data confirmed this observation, showing good inter‐subject correspondence of V1 (Figure b) and excellent correspondence of the anatomical and functional boundaries of V1–V3 (Figure c).…”

Section: Discussionmentioning

confidence: 99%

“…Minimal anatomical variability in primary sensory cortex may, in part, explain the successes of UHF high spatial resolution studies of sensorimotor and visual cortex (Goncalves et al, 2015;Kemper et al, 2017;Poltoratski et al, 2017;Rua et al, 2017;Sanchez Panchuelo et al, 2015;Sanchez Panchuelo et al, 2016;Sanchez-Panchuelo et al, 2012).…”

Section: Spatial Smoothingmentioning

confidence: 99%

“…To date, the majority of UHF fMRI studies have used reduced field‐of‐view (FOV) 2D‐and 3D echo planar imaging (EPI) acquisitions to study chosen primary sensory areas, such as the visual and sensorimotor cortices (Fracasso, Luijten, Dumoulin, & Petridou, ; Puckett, Bollmann, Barth, & Cunnington, ; Reithler, Peters, & Goebel, ; Schluppeck, Sanchez‐Panchuelo, & Francis, ), thus overcoming a number of challenges of B 0 and B 1 inhomogeneities associated with larger FOV acquisitions (Polimeni, Renvall, Zaretskaya, & Fischl, ; Uludag & Blinder, ). For example, the increase in BOLD CNR of UHF experiments has been used to provide detailed maps of individual subjects’ visual (Goncalves et al, ; Kemper, De Martino, Emmerling, Yacoub, & Goebel, ; Poltoratski, Ling, McCormack, & Tong, ; Rua et al, ) and somatosensory functional responses (Puckett et al, ; Sanchez Panchuelo et al, ; Sanchez Panchuelo, Schluppeck, Harmer, Bowtell, & Francis, ) and how these relate to individual brain anatomy (Besle, Sanchez‐Panchuelo, Bowtell, Francis, & Schluppeck, ; Sanchez‐Panchuelo et al, ; Sanchez‐Panchuelo et al, ). These functional maps have been shown to spatially vary across subjects, highlighting inter‐subject variability, whilst the reproducibility of these maps has been shown to be high within subjects across sessions (Goncalves et al, ; Sanchez‐Panchuelo et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Addressing challenges of high spatial resolution UHF fMRI for group analysis of higher‐order cognitive tasks: An inter‐sensory task directing attention between visual and somatosensory domains

Aquino

Sokoliuk

Pakenham

et al. 2018

Human Brain Mapping

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Functional MRI at ultra‐high field (UHF, ≥7 T) provides significant increases in BOLD contrast‐to‐noise ratio (CNR) compared with conventional field strength (3 T), and has been exploited for reduced field‐of‐view, high spatial resolution mapping of primary sensory areas. Applying these high spatial resolution methods to investigate whole brain functional responses to higher‐order cognitive tasks leads to a number of challenges, in particular how to perform robust group‐level statistical analyses. This study addresses these challenges using an inter‐sensory cognitive task which modulates top‐down attention at graded levels between the visual and somatosensory domains. At the individual level, highly focal functional activation to the task and task difficulty (modulated by attention levels) were detectable due to the high CNR at UHF. However, to assess group level effects, both anatomical and functional variability must be considered during analysis. We demonstrate the importance of surface over volume normalisation and the requirement of no spatial smoothing when assessing highly focal activity. Using novel group analysis on anatomically parcellated brain regions, we show that in higher cognitive areas (parietal and dorsal‐lateral‐prefrontal cortex) fMRI responses to graded attention levels were modulated quadratically, whilst in visual cortex and VIP, responses were modulated linearly. These group fMRI responses were not seen clearly using conventional second‐level GLM analyses, illustrating the limitations of a conventional approach when investigating such focal responses in higher cognitive regions which are more anatomically variable. The approaches demonstrated here complement other advanced analysis methods such as multivariate pattern analysis, allowing UHF to be fully exploited in cognitive neuroscience.

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“…A study by Kelly et al, (1997) used high density electroencephalography (EEG) over the primary somatosensory cortex (S1) and showed that stimulating single FA1 or SA1 units projecting to the hand gave characteristic peaks in power at the same frequency at which the units were stimulated. Only two studies have been performed using functional magnetic resonance imaging (fMRI) to map the spatial profile of the cortical responses to single-unit INMS (Sanchez Panchuelo et al, 2016;Trulsson et al, 2001). The earlier study, performed at 3.0 T, showed that individual type I units have corresponding neural activations in S1 and the 90 secondary somatosensory cortex (S2), and the responses were in good spatial agreement with activations from vibrotactile stimulation (Trulsson et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Imaging human cortical responses to intraneural microstimulation using magnetoencephalography

O'Neill¹,

Watkins²,

Ackerley

et al. 2018

Preprint

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10The sensation of touch in the glabrous skin of the human hand is conveyed by thousands of fast-conducting mechanoreceptive afferents, which can be categorised into four distinct types. The spiking properties of these afferents in the periphery in response to varied tactile stimuli are well-characterised, but relatively little is known about the spatiotemporal properties of the neural representations of these different receptor types in the human cortex. Here, we use the novel methodological combination of single-unit intraneural microstimulation (INMS) with magnetoencephalography (MEG) to localise cortical representations of individual touch afferents in humans, by measuring the extracranial magnetic fields from neural currents. We found that by assessing the modulation of the beta (13-30 Hz) rhythm during single-unit INMS, significant changes in oscillatory amplitude occur in the contralateral primary somatosensory cortex within and across a group of fast adapting type I mechanoreceptive afferents, which corresponded well to the induced response from matched vibrotactile stimulation. Combining the 20 spatiotemporal specificity of MEG with the selective single-unit stimulation of INMS enables the interrogation of the central representations of different aspects of tactile afferent signalling within the human cortices. The fundamental finding that single-unit INMS ERD responses are robust and consistent with natural somatosensory stimuli will permit us to more dynamically probe the central nervo us system responses in humans, to address questions about the processing of touch from the different classes of mechanoreceptive afferent s and the effects of varying the stimulus frequency and patterning.

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Mapping quantal touch using 7 Tesla functional magnetic resonance imaging and single-unit intraneural microstimulation

Cited by 38 publications

References 46 publications

Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex

Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex

Addressing challenges of high spatial resolution UHF fMRI for group analysis of higher‐order cognitive tasks: An inter‐sensory task directing attention between visual and somatosensory domains

Imaging human cortical responses to intraneural microstimulation using magnetoencephalography

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