Parkinson-Related Changes of Activation in Visuomotor Brain Regions during Perceived Forward Self-Motion

Radial expanding optic flow is a visual consequence of forward locomotion. Presented on screen, it generates illusionary forward self-motion, pointing at a close vision-gait interrelation. As particularly parkinsonian gait is vulnerable to external stimuli, effects of optic flow on motor-related cerebral circuitry were explored with functional magnetic resonance imaging in healthy controls (HC) and patients with Parkinson’s disease (PD). Fifteen HC and 22 PD patients, of which 7 experienced freezing of gait (FOG), watched wide-field flow, interruptions by narrowing or deceleration and equivalent control conditions with static dots. Statistical parametric mapping revealed that wide-field flow interruption evoked activation of the (pre-)supplementary motor area (SMA) in HC, which was decreased in PD. During wide-field flow, dorsal occipito-parietal activations were reduced in PD relative to HC, with stronger functional connectivity between right visual motion area V5, pre-SMA and cerebellum (in PD without FOG). Non-specific ‘changes’ in stimulus patterns activated dorsolateral fronto-parietal regions and the fusiform gyrus. This attention-associated network was stronger activated in HC than in PD. PD patients thus appeared compromised in recruiting medial frontal regions facilitating internally generated virtual locomotion when visual motion support falls away. Reduced dorsal visual and parietal activations during wide-field optic flow in PD were explained by impaired feedforward visual and visuomotor processing within a magnocellular (visual motion) functional chain. Compensation of impaired feedforward processing by distant fronto-cerebellar circuitry in PD is consistent with motor responses to visual motion stimuli being either too strong or too weak. The ‘change’-related activations pointed at covert (stimulus-driven) attention.     

Sequential neural processes in abacus mental addition: an EEG and FMRI case study

Abacus experts are able to mentally calculate multi-digit numbers rapidly. Some behavioral and neuroimaging studies have suggested a visuospatial and visuomotor strategy during abacus mental calculation. However, no study up to now has attempted to dissociate temporally the visuospatial neural process from the visuomotor neural process during abacus mental calculation. In the present study, an abacus expert performed the mental addition tasks (8-digit and 4-digit addends presented in visual or auditory modes) swiftly and accurately. The 100% correct rates in this expert's task performance were significantly higher than those of ordinary subjects performing 1-digit and 2-digit addition tasks. ERPs, EEG source localizations, and fMRI results taken together suggested visuospatial and visuomotor processes were sequentially arranged during the abacus mental addition with visual addends and could be dissociated from each other temporally. The visuospatial transformation of the numbers, in which the superior parietal lobule was most likely involved, might occur first (around 380 ms) after the onset of the stimuli. The visuomotor processing, in which the superior/middle frontal gyri were most likely involved, might occur later (around 440 ms). Meanwhile, fMRI results suggested that neural networks involved in the abacus mental addition with auditory stimuli were similar to those in the visual abacus mental addition. The most prominently activated brain areas in both conditions included the bilateral superior parietal lobules (BA 7) and bilateral middle frontal gyri (BA 6). These results suggest a supra-modal brain network in abacus mental addition, which may develop from normal mental calculation networks.     

Evidence for the lateral intraparietal area as the parietal eye field.

It has long been appreciated that the posterior parietal cortex plays a role in the processing of saccadic eye movements. Only recently has it been discovered that a small cortical area, the lateral intraparietal area, within this much larger area appears to be specialized for saccadic eye movements. Unlike other cortical areas in the posterior parietal cortex, the lateral intraparietal area has strong anatomical connections to other saccade centers, and its cells have saccade-related responses that begin before the saccades. The lateral intraparietal area appears to be neither a strictly visual nor strictly motor structure; rather it performs visuomotor integration functions including determining the spatial location of saccade targets and forming plans to make eye movements.     

Decoupled Visually-Guided Reaching in Optic Ataxia: Differences in Motor Control between Canonical and Non-Canonical Orientations in Space

Guiding a limb often involves situations in which the spatial location of the target for gaze and limb movement are not congruent (i.e. have been decoupled). Such decoupled situations involve both the implementation of a cognitive rule (i.e. strategic control) and the online monitoring of the limb position relative to gaze and target (i.e. sensorimotor recalibration). To further understand the neural mechanisms underlying these different types of visuomotor control, we tested patient IG who has bilateral caudal superior parietal lobule (SPL) damage resulting in optic ataxia (OA), and compared her performance with six age-matched controls on a series of center-out reaching tasks. The tasks comprised 1) directing a cursor that had been rotated (180° or 90°) within the same spatial plane as the visual display, or 2) moving the hand along a different spatial plane than the visual display (horizontal or para-sagittal). Importantly, all conditions were performed towards visual targets located along either the horizontal axis (left and right; which can be guided from strategic control) or the diagonal axes (top-left and top-right; which require on-line trajectory elaboration and updating by sensorimotor recalibration). The bilateral OA patient performed much better in decoupled visuomotor control towards the horizontal targets, a canonical situation in which well-categorized allocentric cues could be utilized (i.e. guiding cursor direction perpendicular to computer monitor border). Relative to neurologically intact adults, IG''s performance suffered towards diagonal targets, a non-canonical situation in which only less-categorized allocentric cues were available (i.e. guiding cursor direction at an off-axis angle to computer monitor border), and she was therefore required to rely on sensorimotor recalibration of her decoupled limb. We propose that an intact caudal SPL is crucial for any decoupled visuomotor control, particularly when relying on the realignment between vision and proprioception without reliable allocentric cues towards non-canonical orientations in space.     

The Role of the Caudal Superior Parietal Lobule in Updating Hand Location in Peripheral Vision: Further Evidence from Optic Ataxia

Patients with optic ataxia (OA), who are missing the caudal portion of their superior parietal lobule (SPL), have difficulty performing visually-guided reaches towards extra-foveal targets. Such gaze and hand decoupling also occurs in commonly performed non-standard visuomotor transformations such as the use of a computer mouse. In this study, we test two unilateral OA patients in conditions of 1) a change in the physical location of the visual stimulus relative to the plane of the limb movement, 2) a cue that signals a required limb movement 180° opposite to the cued visual target location, or 3) both of these situations combined. In these non-standard visuomotor transformations, the OA deficit is not observed as the well-documented field-dependent misreach. Instead, OA patients make additional eye movements to update hand and goal location during motor execution in order to complete these slow movements. Overall, the OA patients struggled when having to guide centrifugal movements in peripheral vision, even when they were instructed from visual stimuli that could be foveated. We propose that an intact caudal SPL is crucial for any visuomotor control that involves updating ongoing hand location in space without foveating it, i.e. from peripheral vision, proprioceptive or predictive information.     

Electrophysiological evidence for right frontal lobe dominance in spatial visuomotor learning

Slow negative potential shifts were recorded together with the error made in motor performance when two different groups of 14 students tracked visual stimuli with their right hand. Various visuomotor tasks were compared. A tracking task (T) in which subjects had to track the stimulus directly, showed no decrease of error in motor performance during the experiment. In a distorted tracking task (DT) a continuous horizontal distortion of the visual feedback had to be compensated. The additional demands of this task required visuomotor learning. Another learning condition was a mirrored-tracking task (horizontally inverted tracking, hIT), i.e. an elementary function, such as the concept of changing left and right was interposed between perception and action. In addition, subjects performed a no-tracking control task (NT) in which they started the visual stimulus without tracking it. A slow negative potential shift was associated with the visuomotor performance (TP: tracking potential). In the learning tasks (DT and hIT) this negativity was significantly enhanced over the anterior midline and in hIT frontally and precentrally over both hemispheres. Comparing hIT and T for every subject, the enhancement of the tracking potential in hIT was correlated with the success in motor learning in frontomedial and bilaterally in frontolateral recordings (r = 0.81-0.88). However, comparing DT and T, such a correlation was only found in frontomedial and right frontolateral electrodes (r = 0.5-0.61), but not at the left frontolateral electrode. These experiments are consistent with previous findings and give further neurophysiological evidence for frontal lobe activity in visuomotor learning. The hemispherical asymmetry is discussed in respect to hemispherical specialization (right frontal lobe dominance in spatial visuomotor learning).     

Mechanisms of neural integration in the parietal lobe for visual attention.

The impulse discharges of neurons in the inferior parietal association cortex (area 7) were studied in the alert, behaving rhesus monkey, trained to fixate and follow visual targets. Four classes of cells related to visual or visuomotor function were found. Cells of one of these are sensitive to visual stimuli and have large, contralateral receptive fields with maximal sensitivity in the far temporal quadrants. Cells of the other three classes are related to visuomotor functions: visual fixation, tracking, and saccades. They are neither sensory nor motor in the usual sense for they are activated only by interested fixation of gaze or tracking, or before visually evoked saccadic eye movements. They are not activated during the spontaneous saccades and fixations that the monkey makes while casually exploring his environment. It is hypothesized that the light-sensitive neurons provide the visual input to the visuomotor cells that, in turn, produce a command signal for the direction of visual attention and for shifting the focus of attention from one target to another.     

Seeing your error alters my pointing: observing systematic pointing errors induces sensori-motor after-effects

During the procedure of prism adaptation, subjects execute pointing movements to visual targets under a lateral optical displacement: as consequence of the discrepancy between visual and proprioceptive inputs, their visuo-motor activity is characterized by pointing errors. The perception of such final errors triggers error-correction processes that eventually result into sensori-motor compensation, opposite to the prismatic displacement (i.e., after-effects). Here we tested whether the mere observation of erroneous pointing movements, similar to those executed during prism adaptation, is sufficient to produce adaptation-like after-effects. Neurotypical participants observed, from a first-person perspective, the examiner's arm making incorrect pointing movements that systematically overshot visual targets location to the right, thus simulating a rightward optical deviation. Three classical after-effect measures (proprioceptive, visual and visual-proprioceptive shift) were recorded before and after first-person's perspective observation of pointing errors. Results showed that mere visual exposure to an arm that systematically points on the right-side of a target (i.e., without error correction) produces a leftward after-effect, which mostly affects the observer's proprioceptive estimation of her body midline. In addition, being exposed to such a constant visual error induced in the observer the illusion "to feel" the seen movement. These findings indicate that it is possible to elicit sensori-motor after-effects by mere observation of movement errors.     

The role of the posterior parietal cortex in coordinate transformations for visual-motor integration

Lesion to the posterior parietal cortex in monkeys and humans produces spatial deficits in movement and perception. In recording experiments from area 7a, a cortical subdivision in the posterior parietal cortex in monkeys, we have found neurons whose responses are a function of both the retinal location of visual stimuli and the position of the eyes in the orbits. By combining these signals area 7 a neurons code the location of visual stimuli with respect to the head. However, these cells respond over only limited ranges of eye positions (eye-position-dependent coding). To code location in craniotopic space at all eye positions (eye-position-independent coding) an additional step in neural processing is required that uses information distributed across populations of area 7a neurons. We describe here a neural network model, based on back-propagation learning, that both demonstrates how spatial location could be derived from the population response of area 7a neurons and accurately accounts for the observed response properties of these neurons.     

Monocular vision leads to a dissociation between grip force and grip aperture scaling during reach-to-grasp movements

It has been argued that visual perception and the visual control of action depend upon functionally distinct and anatomically separable brain systems. Electrophysiological evidence indicates that binocular vision may be particularly important for the visuomotor processing within the posterior parietal cortex, and neuropsychological and psychophysical studies confirm that binocular vision is crucial for the accurate planning and control of prehension movements. An unresolved issue concerns the consequences for visuomotor processing of removing binocular vision. By one account, monocular viewing leads to reliance upon pictorial visual cues to calibrate grasping and results in disruption to normal size-constancy mechanisms. This proposal is based on the finding that maximum grip apertures are reduced with monocular vision. By a second account, monocular viewing results in the loss of binocular visual cues and leads to strategic changes in visuomotor processing by way of altered safety margins. This proposal is based on the finding that maximum grip apertures are increased with monocular vision. We measured both grip aperture and grip force during prehension movements executed with binocular and monocular viewing. We demonstrate that each of the above accounts may be correct and can be observed within the same task. Specifically, we show that, while grip apertures increase with monocular vision, consistent with altered visuomotor safety margins, maximum grip force is nevertheless reduced, consistent with a misperception of object size. These results are related to differences in visual processing required for calibrating grip aperture and grip force during reaching.     

EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping

To identify subdivisions of the human parietal cortex, we collected fMRI data while ten subjects performed six tasks: grasping, pointing, saccades, attention, calculation, and phoneme detection. Examination of task intersections revealed a systematic anterior-to-posterior organization of activations associated with grasping only, grasping and pointing, all visuomotor tasks, attention and saccades, and saccades only. Calculation yielded two distinct activations: one unique to calculation in the bilateral anterior IPS mesial to the supramarginal gyrus and the other shared with phoneme detection in the left IPS mesial to the angular gyrus. These results suggest human homologs of the monkey areas AIP, MIP, V6A, and LIP and imply a large cortical expansion of the inferior parietal lobule correlated with the development of human language and calculation abilities.     

Neural Responses in Parietal and Occipital Areas in Response to Visual Events Are Modulated by Prior Multisensory Stimuli

The effect of multi-modal vs uni-modal prior stimuli on the subsequent processing of a simple flash stimulus was studied in the context of the audio-visual ‘flash-beep’ illusion, in which the number of flashes a person sees is influenced by accompanying beep stimuli. EEG recordings were made while combinations of simple visual and audio-visual stimuli were presented. The experiments found that the electric field strength related to a flash stimulus was stronger when it was preceded by a multi-modal flash/beep stimulus, compared to when it was preceded by another uni-modal flash stimulus. This difference was found to be significant in two distinct timeframes – an early timeframe, from 130–160 ms, and a late timeframe, from 300–320 ms. Source localisation analysis found that the increased activity in the early interval was localised to an area centred on the inferior and superior parietal lobes, whereas the later increase was associated with stronger activity in an area centred on primary and secondary visual cortex, in the occipital lobe. The results suggest that processing of a visual stimulus can be affected by the presence of an immediately prior multisensory event. Relatively long-lasting interactions generated by the initial auditory and visual stimuli altered the processing of a subsequent visual stimulus.     

Visuomotor synchronization: Analysis of the initiation and stable synchronization phases

The initiation phase of visuomotor synchronization and the phase of stable synchronization were studied in an experiment where eight adult subjects synchronized their motor responses with an isochronous sequence of visual stimuli. The period of the sequence varied in a wide range (from 500 to 2200 ms). Analysis of the statistical characteristics of synchronization errors (asynchronies) showed that the phase of stable visuomotor synchronization fit the model of current phase correction of a central timer; as in the case of audiomotor synchronization, the variability of the intervals of the central timer and the phase correction coefficient increased with increasing period of the stimulus sequence. The initiation phase of visuomotor synchronization was characterized by a considerable inter-and intraindividual variability of the form (exponential, linear, or step) and duration (from one to ten responses) of the transition from reacting to a sensory signal to synchronization. The shape and duration of the transitional region depend on the phase correction coefficient and the possibility of using an estimate of the sequence period stored in memory. The obtained data indicate that the initiation stage is not automatic throughout the studied range of periods of the visual stimulus sequence; in particular, working memory plays a substantial role in its organization.     

Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats

Animals can make faster behavioral responses to multisensory stimuli than to unisensory stimuli. The superior colliculus (SC), which receives multiple inputs from different sensory modalities, is considered to be involved in the initiation of motor responses. However, the mechanism by which multisensory information facilitates motor responses is not yet understood. Here, we demonstrate that multisensory information modulates competition among SC neurons to elicit faster responses. We conducted multiunit recordings from the SC of rats performing a two-alternative spatial discrimination task using auditory and/or visual stimuli. We found that a large population of SC neurons showed direction-selective activity before the onset of movement in response to the stimuli irrespective of stimulation modality. Trial-by-trial correlation analysis showed that the premovement activity of many SC neurons increased with faster reaction speed for the contraversive movement, whereas the premovement activity of another population of neurons decreased with faster reaction speed for the ipsiversive movement. When visual and auditory stimuli were presented simultaneously, the premovement activity of a population of neurons for the contraversive movement was enhanced, whereas the premovement activity of another population of neurons for the ipsiversive movement was depressed. Unilateral inactivation of SC using muscimol prolonged reaction times of contraversive movements, but it shortened those of ipsiversive movements. These findings suggest that the difference in activity between the SC hemispheres regulates the reaction speed of motor responses, and multisensory information enlarges the activity difference resulting in faster responses.     

Sensory and behavioral properties of neurons in posterior parietal cortex of the awake, trained monkey.

Neurons in posterior parietal cortex of the awake, trained monkey respond to passive visual and/or somatosensory stimuli. In general, the receptive fields of these cells are large and nonspecific. When these neurons are studied during visually guided hand movements and eye movements, most of their activity can be accounted for by passive sensory stimulation. However, for some visual cells, the response to a stimulus is enhanced when it is to be the target for a saccadic eye movement. This enhancement is selective for eye movements into the visual receptive field since it does not occur with eye movements to other parts of the visual field. Cells that discharge in association with a visual fixation task have foveal receptive fields and respond to the spots of light used as fixation targets. Cells discharging selectively in association with different directions of tracking eye movements have directionally selective responses to moving visual stimuli. Every cell in our sample discharging in association with movement could be driven by passive sensory stimuli. We conclude that the activity of neurons in posterior parietal cortex is dependent on and indicative of external stimuli but not predictive of movement.     

Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions

Visual processing is not determined solely by retinal inputs. Attentional modulation can arise when the internal attentional state (current task) of the observer alters visual processing of the same stimuli. This can influence visual cortex, boosting neural responses to an attended stimulus. Emotional modulation can also arise, when affective properties (emotional significance) of stimuli, rather than their strictly visual properties, influence processing. This too can boost responses in visual cortex, as for fear-associated stimuli. Both attentional and emotional modulation of visual processing may reflect distant influences upon visual cortex, exerted by brain structures outside the visual system per se. Hence, these modulations may provide windows onto causal interactions between distant but interconnected brain regions. We review recent evidence, noting both similarities and differences between attentional and emotional modulation. Both can affect visual cortex, but can reflect influences from different regions, such as fronto-parietal circuits versus the amygdala. Recent work on this has developed new approaches for studying causal influences between human brain regions that may be useful in other cognitive domains. The new methods include application of functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) measures in brain-damaged patients to study distant functional impacts of their focal lesions, and use of transcranial magnetic stimulation concurrently with fMRI or EEG in the normal brain. Cognitive neuroscience is now moving beyond considering the putative functions of particular brain regions, as if each operated in isolation, to consider, instead, how distinct brain regions (such as visual cortex, parietal or frontal regions, or amygdala) may mutually influence each other in a causal manner.     

Processing of complex stimuli and natural scenes in the visual cortex

A major part of vision research builds on the assumption that processing of visual stimuli can be understood on the basis of knowledge about the processing of simplified, artificial stimuli. Recent experimental advances, however, show that a combination of responses to simplified stimuli does not adequately describe responses to natural visual scenes. The systems performance exceeds the performance predicted from understanding its basic constituents. This highlights the fact that the visual system is specifically adapted to the properties of its everyday input and can only fully be understood when probed with naturalistic stimuli.     

Stimulus dependency of object-evoked responses in human visual cortex: an inverse problem for category specificity

Many studies have linked the processing of different object categories to specific event-related potentials (ERPs) such as the face-specific N170. Despite reports showing that object-related ERPs are influenced by visual stimulus features, there is consensus that these components primarily reflect categorical aspects of the stimuli. Here, we re-investigated this idea by systematically measuring the effects of visual feature manipulations on ERP responses elicited by both structure-from-motion (SFM)-defined and luminance-defined object stimuli. SFM objects elicited a novel component at 200-250 ms (N250) over parietal and posterior temporal sites. We found, however, that the N250 amplitude was unaffected by restructuring SFM stimuli into meaningless objects based on identical visual cues. This suggests that this N250 peak was not uniquely linked to categorical aspects of the objects, but is strongly determined by visual stimulus features. We provide strong support for this hypothesis by parametrically manipulating the depth range of both SFM- and luminance-defined object stimuli and showing that the N250 evoked by SFM stimuli as well as the well-known N170 to static faces were sensitive to this manipulation. Importantly, this effect could not be attributed to compromised object categorization in low depth stimuli, confirming a strong impact of visual stimulus features on object-related ERP signals. As ERP components linked with visual categorical object perception are likely determined by multiple stimulus features, this creates an interesting inverse problem when deriving specific perceptual processes from variations in ERP components.     

Human parieto-occipital visual cortex: lack of retinotopy and foveal magnification.

We studied visual representation in the parietal cortex by recording whole-scalp neuromagnetic responses to luminance stimuli of varying eccentricities. The stimuli were semicircles (5.5 degrees in radius) presented at horizontal eccentricities from 0 degree to 16 degrees, separately in the right and left hemifields. All stimuli evoked responses in the contralateral occipital and medial parietal areas. The waveforms and distributions of the occipital responses varied with stimulus side (left, right) and eccentricity, whereas the parietal responses were remarkably similar to all stimuli. The equivalent sources of the parietal signals clustered within 1 cm3 in the medial parieto-occipital sulcus and did not differ significantly between the stimuli. The strength of the parietal activation remained practically constant with increasing stimulus eccentricity, suggesting that the visual areas in the parieto-occipital sulcus lack the enhanced foveal representation typical of most other visual areas. This result strengthens our previous suggestion that the medial parieto-occipital sulcus is the human homologue of the monkey V6 complex, characterized by, for example, lack of retinotopy and the absence of relative foveal magnification.     

Different temporal structure for form versus surface cortical color systems--evidence from chromatic non-linear VEP

Physiological studies of color processing have typically measured responses to spatially varying chromatic stimuli such as gratings, while psychophysical studies of color include color naming, color and light, as well as spatial and temporal chromatic sensitivities. This raises the question of whether we have one or several cortical color processing systems. Here we show from non-linear analysis of human visual evoked potentials (VEP) the presence of distinct and independent temporal signatures for form and surface color processing. Surface color stimuli produced most power in the second order Wiener kernel, indicative of a slowly recovering neural system, while chromatic form stimulation produced most power in the first order kernel (showing rapid recovery). We find end-spectral saturation-dependent signals, easily separable from achromatic signals for surface color stimuli. However physiological responses to form color stimuli, though varying somewhat with saturation, showed similar waveform components. Lastly, the spectral dependence of surface and form color VEP was different, with the surface color responses almost vanishing with yellow-grey isoluminant stimulation whereas the form color VEP shows robust recordable signals across all hues. Thus, surface and form colored stimuli engage different neural systems within cortex, pointing to the need to establish their relative contributions under the diverse chromatic stimulus conditions used in the literature.