A response-locking protocol to boost sensitivity for fMRI-based neurochronometry.

The timeline of brain-wide neural activity relative to a behavioral event is crucial when decoding the neural implementation of a cognitive process. Yet, fMRI assesses neural processes indirectly via delayed and regionally variable hemodynamics. This method-inherent temporal distortion impacts the interpretation of behavior-linked neural timing. Here we describe a novel behavioral protocol that aims at disentangling the BOLD dynamics of the pre- and post-response periods in response time tasks. We tested this response-locking protocol in a perceptual decision-making (random dot) task. Increasing perceptual difficulty produced expected activity increases over a broad network involving the lateral/medial prefrontal cortex and the anterior insula. However, response-locking revealed a previously unreported functional dissociation within this network. preSMA and anterior premotor cortex (prePMV) showed post-response activity modulations while anterior insula and anterior cingulate cortex did not. Furthermore, post-response BOLD activity at preSMA showed a modulation in timing but not amplitude while this pattern was reversed at prePMV. These timeline dissociations with response-locking thus revealed three functionally distinct sub-networks in what was seemingly one shared distributed network modulated by perceptual difficulty. These findings suggest that our novel response-locked protocol could boost the timing-related sensitivity of fMRI.

Freely chosen and instructed actions are terminated by different neural mechanisms revealed by kinematics-informed EEG.

Neurophysiological accounts of human volition are dominated by debates on the origin of voluntary choices but the neural consequences that follow such choices remain poorly understood. For instance, could one predict whether or not an action was chosen voluntarily based only on how that action is motorically executed? We investigated this possibility by integrating scalp electroencephalograms and index-finger accelerometer recordings acquired while people chose between pressing a left or right button either freely or as instructed by a visual cue. Even though freely selected and instructed actions were executed with equal vigor, the timing of the movement to release the button was comparatively delayed for freely selected actions. This chronometric difference was six-times larger for the ß-oscillations over the sensorimotor cortex that characteristically accompany an action's termination. This surprising modulation of an action's termination by volition was traceable to volition-modulated differences in how the competing yet non-selected action was represented and regulated.

Motor and emotional behaviours elicited by electrical stimulation of the human cingulate cortex.

The cingulate cortex is a mosaic of different anatomical fields, whose functional characterization is still a matter of debate. In humans, one method that may provide useful insights on the role of the different cingulate regions, and to tackle the issue of the functional differences between its anterior, middle and posterior subsectors, is intracortical electrical stimulation. While previous reports showed that a variety of integrated behaviours could be elicited by stimulating the midcingulate cortex, little is known about the effects of the electrical stimulation of anterior and posterior cingulate regions. Moreover, the internal arrangement of different behaviours within the midcingulate cortex is still unknown. In the present study, we extended previous stimulation studies by retrospectively analysing all the clinical manifestations induced by intracerebral high frequency electrical stimulation (50 Hz, pulse width: 1 ms, 5 s, current intensity: average intensity of 2.7 ± 0.7 mA, biphasic) of the entire cingulate cortex in a cohort of 329 drug-resistant epileptic patients (1789 stimulation sites) undergoing stereo-electroencephalography for a presurgical evaluation. The large number of patients, on one hand, and the accurate multimodal image-based localization of stereo-electroencephalography electrodes, on the other hand, allowed us to assign specific functional properties to modern anatomical subdivisions of the cingulate cortex. Behavioural or subjective responses were elicited from the 32.3% of all cingulate sites, mainly located in the pregenual and midcingulate regions. We found clear functional differences between the pregenual part of the cingulate cortex, hosting the majority of emotional, interoceptive and autonomic responses, and the anterior midcingulate sector, controlling the majority of all complex motor behaviours. Particularly interesting was the 'actotopic' organization of the anterior midcingulate sector, arranged along the ventro-dorsal axis: (i) whole-body behaviours directed to the extra-personal space, such as getting-up impulses, were elicited ventrally, close to the corpus callosum; (ii) hand actions in the peripersonal space were evoked by the stimulation of the intermediate position; and (iii) body-directed actions were induced by the stimulation of the dorsal branch of the cingulate sulcus. The caudal part of the midcingulate cortex and the posterior cingulate cortex were, in contrast, poorly excitable, and mainly devoted to sensory modalities. In particular, the caudal part of the midcingulate cortex hosted the majority of vestibular responses, while posterior cingulate cortex was the principal recipient of visual effects. We will discuss our data in the light of current controversies on the role of the cingulate cortex in cognition and emotion.

Frequency-specific modulation of connectivity in the ipsilateral sensorimotor cortex by different forms of movement initiation.

A consistent finding in motor EEG research is a bilateral attenuation of oscillatory activity over sensorimotor regions close to the onset of an upcoming unilateral hand movement. In contrast, little is known about how movement initiation affects oscillatory activity, especially in the hemisphere ipsilateral to the moving hand. We here investigated the neural mechanisms modulating oscillatory activity in the ipsilateral motor cortex prior to movement onset under the control of two different initiating networks, namely, Self-initiated and Visually-cued actions. During motor preparation, a contralateral preponderance of power over sensorimotor cortex (SM) was observed in α and ß bands during Visually-cued movements, whereas power changes were more bilateral during Self-initiated movements. Coherence between ipsilateral SM (iSM) and contralateral SM (cSM) in the α-band was significantly increased compared to the respective baseline values, independent of the context of movement initiation. However, this context-independent cSM-iSM coherence modulated the power changes in iSM in a context-dependent manner, that is, a stronger cSM-iSM coherence correlated with a larger decrease in high-ß power over iSM in the Self-initiated condition, in contrast to a smaller decrease in α power in the Visually-cued condition. In addition, the context-dependent coherence between SMA and iSM in the α-band and δ-θ-band for the Self-initiated and Visually-cued condition, respectively, exhibited a similar context-dependent modulation for power changes. Our findings suggest that the initiation of regional oscillations over iSM reflects changes in the information flow with the contralateral sensorimotor and premotor areas dependent upon the context of movement initiation. Importantly, the interaction between regional oscillations and network-like oscillatory couplings indicates different frequency-specific inhibitory mechanisms that modulate the activity in the ipsilateral sensorimotor cortex dependent upon how the movement is initiated.

Spatiotopic Adaptation in Visual Areas.

UNLABELLED: The ability to perceive the visual world around us as spatially stable despite frequent eye movements is one of the long-standing mysteries of neuroscience. The existence of neural mechanisms processing spatiotopic information is indispensable for a successful interaction with the external world. However, how the brain handles spatiotopic information remains a matter of debate. We here combined behavioral and fMRI adaptation to investigate the coding of spatiotopic information in the human brain. Subjects were adapted by a prolonged presentation of a tilted grating. Thereafter, they performed a saccade followed by the brief presentation of a probe. This procedure allowed dissociating adaptation aftereffects at retinal and spatiotopic positions. We found significant behavioral and functional adaptation in both retinal and spatiotopic positions, indicating information transfer into a spatiotopic coordinate system. The brain regions involved were located in ventral visual areas V3, V4, and VO. Our findings suggest that spatiotopic representations involved in maintaining visual stability are constructed by dynamically remapping visual feature information between retinotopic regions within early visual areas. SIGNIFICANCE STATEMENT: Why do we perceive the visual world as stable, although we constantly perform saccadic eye movements? We investigated how the visual system codes object locations in spatiotopic (i.e., external world) coordinates. We combined visual adaptation, in which the prolonged exposure to a specific visual feature alters perception, with fMRI adaptation, where the repeated presentation of a stimulus leads to a reduction in the BOLD amplitude. Functionally, adaptation was found in visual areas representing the retinal location of an adaptor but also at representations corresponding to its spatiotopic position. The results suggest that an active dynamic shift transports information in visual cortex to counteract the retinal displacement associated with saccade eye movements.

Four-dimensional maps of the human somatosensory system.

A fine-grained description of the spatiotemporal dynamics of human brain activity is a major goal of neuroscientific research. Limitations in spatial and temporal resolution of available noninvasive recording and imaging techniques have hindered so far the acquisition of precise, comprehensive four-dimensional maps of human neural activity. The present study combines anatomical and functional data from intracerebral recordings of nearly 100 patients, to generate highly resolved four-dimensional maps of human cortical processing of nonpainful somatosensory stimuli. These maps indicate that the human somatosensory system devoted to the hand encompasses a widespread network covering more than 10% of the cortical surface of both hemispheres. This network includes phasic components, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, and tonic components, centered on opercular and insular areas, and involving human parietal rostroventral area and ventral medial-superior-temporal area. The technique described opens new avenues for investigating the neural basis of all levels of cortical processing in humans.

Seeing biological actions in 3D: An fMRI study.

Precise kinematics or body configuration cannot be recovered from visual input without disparity information. Yet, no imaging study has investigated the role of disparity on action observation. Here, we investigated the interaction between disparity and the main cues of biological motion, kinematics and configuration, in two fMRI experiments. Stimuli were presented as point-light figures, depicting complex action sequences lasting 21 s. We hypothesized that interactions could occur at any of the three levels of the action observation network, comprising occipitotemporal, parietal and premotor cortex, with premotor cortex being the most likely location. The main effects of kinematics and configuration confirmed that the biological motion sequences activated all three levels of the action observation network, validating our approach. The interaction between configuration and disparity activated only premotor cortex, whereas interactions between kinematics and disparity occurred at all levels of the action observation network but were strongest at the premotor level. Control experiments demonstrated that these interactions could not be accounted for by low level motion in depth, task effects, spatial attention, or eye movements, including vergence. These results underscore the role of premotor cortex in action observation, and in imitating others or responding to their actions.

Correspondences between retinotopic areas and myelin maps in human visual cortex.

We generated probabilistic area maps and maximum probability maps (MPMs) for a set of 18 retinotopic areas previously mapped in individual subjects (Georgieva et al., 2009 and Kolster et al., 2010) using four different inter-subject registration methods. The best results were obtained using a recently developed multimodal surface matching method. The best set of MPMs had relatively smooth borders between visual areas and group average area sizes that matched the typical size in individual subjects. Comparisons between retinotopic areas and maps of estimated cortical myelin content revealed the following correspondences: (i) areas V1, V2, and V3 are heavily myelinated; (ii) the MT cluster is heavily myelinated, with a peak near the MT/pMSTv border; (iii) a dorsal myelin density peak corresponds to area V3D; (iv) the phPIT cluster is lightly myelinated; and (v) myelin density differs across the four areas of the V3A complex. Comparison of the retinotopic MPM with cytoarchitectonic areas, including those previously mapped to the fs_LR cortical surface atlas, revealed a correspondence between areas V1-3 and hOc1-3, respectively, but little correspondence beyond V3. These results indicate that architectonic and retinotopic areal boundaries are in agreement in some regions, and that retinotopy provides a finer-grained parcellation in other regions. The atlas datasets from this analysis are freely available as a resource for other studies that will benefit from retinotopic and myelin density map landmarks in human visual cortex.

Common and segregated processing of observed actions in human SPL.

To clarify the functional organization of parietal cortex involved in action observation, we scanned subjects observing 3 widely different classes of actions: Manipulation with the hands, locomotion, and climbing. An effector-based organization predicts that parietal regions involved in the observation of climbing should not differ from those involved in observing manipulation and locomotion, opposite to the prediction of an organization based upon the action performed. Compared with individual controls, the observation of climbing evoked activity in dorsal superior parietal lobule (SPL), extending into precuneus and posterior cingulate sulcus. Observation of locomotion differentially activated similar regions less strongly. Observation of manipulation activated ventro-rostral SPL, including putative human AIP (phAIP). Using interaction testing and exclusive masking to directly compare the parietal regions involved in observing the 3 action classes, relative to the controls, revealed that the rostral part of dorsal SPL was specifically involved in observing climbing and phAIP in observing manipulation. Parietal regions common to observing all 3 action classes were restricted and likely reflected higher order visual processing of body posture and 3D structure from motion. These results support a functional organization of some parietal regions involved in action observation according to the type of action in the case of climbing and manipulation.

Acting alters visual processing: flexible recruitment of visual areas by one's own actions.

Using functional magnetic resonance imaging, we investigated the effect of motor preparation/execution on the activation of visual cortical areas by action observation. We presented videos of human actors performing several fine manipulative actions (e.g., grasping) with the hand or foot, together with appropriate control stimuli. Subjects either responded in a central fixation task with the hand (A) or foot (B) or viewed the stimuli passively (C). Experimental conditions were arranged according to a 2 × 2 × 3 factorial design with action, effector, and response as factors. Bilateral posterior parietal cortex was more strongly activated for action videos compared with controls during active runs (A or B) contrasted with passive runs (C). Two neighboring regions in the right fusiform gyrus (FG) were activated when the effector employed to respond in the task matched that displayed in the videos (A or B), independently of whether the stimulus was an action or a control. Neighboring regions in the right posterior middle temporal gyrus (MTG) were also activated when the effector observed and that used to respond matched (A or B), but only for action videos, not controls. Our results indicate flexible modulation of visual areas during concurrent action observation and action execution/preparation, which was effector specific in the FG and MTG.