Marc Himmelbach

Spatial awareness is a function of the temporal not the posterior parietal lobe

Our current understanding of spatial behaviour and parietal lobe function is largely based on the belief that spatial neglect in humans (a lack of awareness of space on the side of the body contralateral to a brain injury) is typically associated with lesions of the posterior parietal lobe. However, in monkeys, this disorder is observed after lesions of the superior temporal cortex, a puzzling discrepancy between the species. Here we show that, contrary to the widely accepted view, the superior temporal cortex is the neural substrate of spatial neglect in humans, as it is in monkeys. Unlike the monkey brain, spatial awareness in humans is a function largely confined to the right superior temporal cortex, a location topographically reminiscent of that for language on the left. Hence, the decisive phylogenetic transition from monkey to human brain seems to be a restriction of a formerly bilateral function to the right side, rather than a shift from the temporal to the parietal lobe. One may speculate that this lateralization of spatial awareness parallels the emergence of an elaborate representation for language on the left side.

Direct electrical stimulation of human cortex — the gold standard for mapping brain functions?

Despite its clinical relevance, direct electrical stimulation (DES) of the human brain is surprisingly poorly understood. Although we understand several aspects of electrical stimulation at the cellular level, surface DES evokes a complex summation effect in a large volume of brain tissue, and the effect is difficult to predict as it depends on many local and remote physiological and morphological factors. The complex stimulation effects are reflected in the heterogeneity of behavioural effects that are induced by DES, which range from evocation to inhibition of responses — sometimes even when DES is applied at the same cortical site. Thus, it is a misconception that DES — in contrast to other neuroscience techniques — allows us to draw unequivocal conclusions about the role of stimulated brain areas.

fMRI study of bimanual coordination.

Eleven right-handed subjects performed uni- and bimanual tapping tasks. Hemodynamic responses as measured with functional magnetic resonance imaging (fMRI) in the primary somato-motor cortex (SMC) showed that during bimanual activity the SMC contralateral to the hand taking the faster rate was more strongly activated than the SMC contralateral to hand taking the slower rate. There were no asymmetries, left SMC activation during the right fast/left slow tapping condition was comparable to the right SMC activation during the left fast/right slow condition. A given SMC showed similar activation levels for bimanual and unimanual activity (i.e. left SMC activation for right fast/left slow was similar to left SMC activation for the right fast unimanual condition). In contrast, a given supplementary motor area (SMA) showed significantly more activation for the bimanual than for the unimanual activity. In addition, an asymmetry was observed during bimanual activities: during the right fast/left slow activity, the left SMA showed more activation than the right SMA, but during the left fast/right slow activity, the right SMA was not significantly more activated than the left SMA. For unimanual activities, a clear rate effect (greater activation for faster rate) was seen in the SMC but not in the SMA.

A parametric analysis of the 'rate effect' in the sensorimotor cortex : a functional magnetic resonance imaging analysis in human subjects

We studied the effects of different movement speeds of unimanual right hand movements on functional magnetic resonance signal changes in the sensorimotor cortex using echo planar imaging (EPI). Six healthy right-handed subjects were scanned at rest and while executing a finger tapping task with their right index finger. Movement frequency was visually paced at rates ranging from 0.5 to 5 Hz, separated by 0.5 Hz steps. The blood oxygen level dependent (BOLD) response within the left sensorimotor cortex was linearly and positively related to movement frequency. However, this relation holds (r2 = 0.91) only for movement frequencies faster than 1 Hz (1.5-5 Hz). For the slower frequencies there was an initial sharp increase of the BOLD response from 0.5 to 1 Hz followed by an activity drop for 1.5 Hz. These results are compatible with the idea that two different motor control modes are operative during slow or fast movements. During slow movements a computational demanding on-line feedback control mode is operative resulting in strong BOLD signals indicating extensive neural activity. During faster movements on the other hand a program-like motor control mode is operative resulting in less demanding neural computations. The amount of neural computation for the latter control mode increases with increasing movement speed.

The Anatomy of Object Recognition—Visual Form Agnosia Caused by Medial Occipitotemporal Stroke

The influential model on visual information processing by Milner and Goodale (1995) has suggested a dissociation between action- and perception-related processing in a dorsal versus ventral stream projection. It was inspired substantially by the observation of a double dissociation of disturbed visual action versus perception in patients with optic ataxia on the one hand and patients with visual form agnosia (VFA) on the other. Unfortunately, almost all cases with VFA reported so far suffered from inhalational intoxication, the majority with carbon monoxide (CO). Since CO induces a diffuse and widespread pattern of neuronal and white matter damage throughout the whole brain, precise conclusions from these patients with VFA on the selective role of ventral stream structures for shape and orientation perception were difficult. Here, we report patient J.S., who demonstrated VFA after a well circumscribed brain lesion due to stroke etiology. Like the famous patient D.F. with VFA after CO intoxication studied by Milner, Goodale, and coworkers (Goodale et al., 1991, 1994; Milner et al., 1991; Servos et al., 1995; Mon-Williams et al., 2001a,b; Wann et al., 2001; Westwood et al., 2002; McIntosh et al., 2004; Schenk and Milner, 2006), J.S. showed an obvious dissociation between disturbed visual perception of shape and orientation information on the one side and preserved visuomotor abilities based on the same information on the other. In both hemispheres, damage primarily affected the fusiform and the lingual gyri as well as the adjacent posterior cingulate gyrus. We conclude that these medial structures of the ventral occipitotemporal cortex are integral for the normal flow of shape and of contour information into the ventral stream system allowing to recognize objects.

Exploring the visual world: The neural substrate of spatial orienting

Inspecting the visual environment, humans typically direct their attention across space by means of voluntary saccadic eye movements. Neuroimaging studies in healthy subjects have identified the superior parietal cortex and intraparietal sulcus as important structures involved in visual search. However, in apparent contrast, spatial disturbance of free exploration typically is observed after damage of brain structures located far more ventrally. Lesion studies in such patients disclosed the inferior parietal lobule (IPL) and temporo-parietal junction (TPJ), the superior temporal gyrus (STG) and insula, as well as the inferior frontal gyrus (IFG) of the right hemisphere. Here we used functional magnetic resonance imaging to investigate the involvement of these areas in active visual exploration in the intact brain. We conducted a region of interest analysis comparing free visual exploration of a dense stimulus array with the execution of stepwise horizontal and vertical saccades. The comparison of BOLD responses revealed significant signal increases during exploration in TPJ, STG, and IFG. This result calls for a reappraisal of the previous thinking on the function of these areas in visual search processes. In agreement with lesion studies, the data suggest that these areas are part of the network involved in human spatial orienting and exploration. The IPL dorsally of TPJ seem to be of minor importance for free visual exploration as these areas appear to be equally involved in the execution of spatially predetermined saccades.

Brain activation during immediate and delayed reaching in optic ataxia.

Patients with optic ataxia after lesions of the occipito-parietal cortex demonstrate gross deviations of movements to visual targets in their peripheral visual field. When the same patients point to remembered target locations their accuracy improves considerably. Taking into account opposite findings in a single patient suffering from visual form agnosia due to bilateral occipito-temporal lesions (D.F.), this paradoxical improvement was attributed to brain structures outside the dorsal stream, and supposed to be specifically associated with delayed movement execution. This conclusion was based on the still unverified assumption that the dorsal system is almost completely lacking any localization function in patients with optic ataxia who demonstrate the paradoxical delay effect. We thus investigated brain activity associated with immediately executed and delayed movements in a patient with optic ataxia due to extensive bilateral lesions (I.G.) and in 16 healthy subjects using functional magnetic resonance imaging. Our analysis revealed robust and indistinguishable activation of intact dorsal occipital and parietal areas adjacent to the patients lesions for both types of movements. In healthy subjects, we found the same visuomotor network activated during immediate and delayed movements as well as additionally higher signal increases for movements to visible targets than for delayed movements in bilateral occipito-parietal and occipito-temporal areas. Our results suggest that in healthy subjects as well as in the optic ataxia patient I.G. dorsal areas are not only involved in immediate but also in delayed reaching. This observation questions the hypothesis that residual visuospatial abilities in patients with optic ataxia could only be mediated by a system outside of the dorsal stream.

The Effect of Switching between Sequential and Repetitive Movements on Cortical Activation

We used whole-head functional magnetic resonance imaging (fMRI) to investigate the effect of switching between different sequential and repetitive movements in the context of conditional and fixed tasks. Four different movement tasks were applied: (1) unpredictable switching between two movement sequences comprising six submovements each according to visual cues (SEQ-VC); (2) unpredictable switching between repetitive movement of one finger according to visual cues (REP-VC); (3) performance of the same sequential movements used for SEQ-VC but in a fixed mode triggered by a visual stimulus (SEQ-FIX); (4) performance of the repetitive movements used for REP-FIX but in a fixed mode by a visual stimulus (REP-FIX). The statistical group analysis of the hemodynamic responses revealed the following results: (1) the SEQ-VC compared to the SEQ-FIX condition (switching between movement sequences) engendered stronger activations in the left rostral supplementary motor area (pre-SMA), bilaterally in the posterior parietal lobule, the left ventral premotor area, and the visual cortices; (2) the REP-VC compared to the REP-FIX condition (switching between repetitive movements) only revealed stronger activation in extra-striate areas. We hypothesize that during switching of movement sequences higher motor control aspects are involved including movement selection, updating of motor plans, as well as recalling and restoring motor plans. The repetitive movements are too simple in order to evoke additional activations in the medial and lateral premotor areas, as well as in parietal areas.

fMRI of global visual perception in simultanagnosia.

The integration of visual elements into global perception seems to be implemented separately to single object perception. This assumption is supported by the existence of patients with simultanagnosia who can identify single objects but are incapable of integrating multiple visual items. We investigated a case of simultanagnosia due to posterior cortical atrophy without structural brain damage who demonstrated an incomplete simultanagnosia. The patient successfully recognized a global stimulus in one trial but failed to do so just a few seconds later. Using event-related fMRI, we contrasted post hoc selected trials of successful global perception with trials of global recognition failure. We found circumscribed clusters of activity at the right and left primary intermediate sulci and a bilateral cluster at the ventral precuneus. The integration of multiple visual elements resulting in a conscious perception of their gestalt seems to rely on these bilateral structures in the human lateral and medial inferior parietal cortex.

Goal-Directed Hand Movements Are Not Affected by the Biased Space Representation in Spatial Neglect

Patients with spatial neglect exhibit a severe shift of spontaneous explorative movements to the right side, indicating a bias of long-living representations of space. Whether or not goal-directed movements likewise are affected by this rightward bias has been controversially discussed throughout the last decade. Unfortunately, substantial differences regarding patient selection and data analysis prevented a direct comparison of these results. We thus studied pointing movements in a new sample of subjects covering all different patient groups previously investigated on this issue. We analyzed all the different measures of hand path curvature used so far and, in addition, suggest a new measure that avoids the disadvantages of the previously used parameters. Despite their severe bias for exploratory movements, we did not find systematic, direction-specific deviations of goal-directed hand movements that were specific for the patients with spatial neglect. The results strongly suggest that the disturbance of long-living spatial representations underlying the bias of exploratory behavior in patients with neglect does not influence the performance of goal-directed movements. The data support the view of a dual mode of space representation in the posterior parietal and the superior temporal cortex.