Michael Vesia

Specificity of Human Parietal Saccade and Reach Regions during Transcranial Magnetic Stimulation

Single-unit recordings in macaque monkeys have identified effector-specific regions in posterior parietal cortex (PPC), but functional neuroimaging in the human has yielded controversial results. Here we used on-line repetitive transcranial magnetic stimulation (rTMS) to determine saccade and reach specificity in human PPC. A short train of three TMS pulses (separated by an interval of 100 ms) was delivered to superior parieto-occipital cortex (SPOC), a region over the midposterior intraparietal sulcus (mIPS), and a site close to caudal IPS situated over the angular gyrus (AG) during a brief memory interval while subjects planned either a saccade or reach with the left or right hand. Behavioral measures then were compared to controls without rTMS. Stimulation of mIPS and AG produced similar patterns: increased end-point variability for reaches and decreased saccade accuracy for contralateral targets. In contrast, stimulation of SPOC deviated reach end points toward visual fixation and had no effect on saccades. Contralateral-limb specificity was highest for AG and lowest for SPOC. Visual feedback of the hand negated rTMS-induced disruptions of the reach plan for mIPS and AG, but not SPOC. These results suggest that human SPOC is specialized for encoding retinally peripheral reach goals, whereas more anterior-lateral regions (mIPS and AG) along the IPS possess overlapping maps for saccade and reach planning and are more closely involved in motor details (i.e., planning the reach vector for a specific hand). This work provides the first causal evidence for functional specificity of these parietal regions in healthy humans.

Specialization of reach function in human posterior parietal cortex

Posterior parietal cortex (PPC) plays an important role in the planning and control of goal-directed action. Single-unit studies in monkeys have identified reach-specific areas in the PPC, but the degree of effector and computational specificity for reach in the corresponding human regions is still under debate. Here, we review converging evidence spanning functional neuroimaging, parietal patient and transcranial magnetic stimulation studies in humans that suggests a functional topography for reach within human PPC. We contrast reach to saccade and grasp regions to distinguish functional specificity and also to understand how these different goal-directed actions might be coordinated at the cortical level. First, we present the current evidence for reach specificity in distinct modules in PPC, namely superior parietal occipital cortex, midposterior intraparietal cortex and angular gyrus, compared to saccade and grasp. Second, we review the evidence for hemispheric lateralization (both for hand and visual hemifield) in these reach representations. Third, we review evidence for computational reach specificity in these regions and finally propose a functional framework for these human PPC reach modules that includes (1) a distinction between the encoding of reach goals in posterior–medial PPC as opposed to reach movement vectors in more anterior–lateral PPC regions, and (2) their integration within a broader cortical framework for reach, grasp and eye–hand coordination. These findings represent both a confirmation and extension of findings that were previously reported for the monkey.

Transcranial Magnetic Stimulation over Posterior Parietal Cortex Disrupts Transsaccadic Memory of Multiple Objects

The posterior parietal cortex (PPC) plays a role in spatial updating of goals for eye and arm movements across saccades, but less is known about its role in updating perceptual memory. We reported previously that transsaccadic memory has a capacity for storing the orientations of three to four Gabor patches either within a single fixation (fixation task) or between separate fixations (saccade task). Here, we tested the role of the PPC in transsaccadic memory in eight subjects by simultaneously applying single-pulse transcranial magnetic stimulation (TMS) over the right and left PPC, over several control sites, and comparing these to behavioral controls with no TMS. In TMS trials, we randomly delivered pulses at one of three different time intervals around the time of the saccade, or at an equivalent time in the fixation task. Controls confirmed that subjects could normally retain at least three visual features. TMS over the left PPC and a control site had no significant effect on this performance. However, TMS over the right PPC disrupted memory performance in both tasks. This TMS-induced effect was most disruptive in the saccade task, in particular when stimulation coincided more closely with saccade timing. Here, the capacity to compare presaccadic and postsaccadic features was reduced to one object, as expected if the spatial aspect of memory was disrupted. This finding suggests that right PPC plays a role in the spatial processing involved in transsaccadic memory of visual features. We propose that this process uses saccade-related feedback signals similar to those observed in spatial updating.

Cortical mechanisms for trans-saccadic memory and integration of multiple object features

Constructing an internal representation of the world from successive visual fixations, i.e. separated by saccadic eye movements, is known as trans-saccadic perception. Research on trans-saccadic perception (TSP) has been traditionally aimed at resolving the problems of memory capacity and visual integration across saccades. In this paper, we review this literature on TSP with a focus on research showing that egocentric measures of the saccadic eye movement can be used to integrate simple object features across saccades, and that the memory capacity for items retained across saccades, like visual working memory, is restricted to about three to four items. We also review recent transcranial magnetic stimulation experiments which suggest that the right parietal eye field and frontal eye fields play a key functional role in spatial updating of objects in TSP. We conclude by speculating on possible cortical mechanisms for governing egocentric spatial updating of multiple objects in TSP.

Transcranial magnetic stimulation over human dorsal-lateral posterior parietal cortex disrupts integration of hand position signals into the reach plan.

Posterior parietal cortex (PPC) has been implicated in the integration of visual and proprioceptive information for the planning of action. We previously reported that single-pulse transcranial magnetic stimulation (TMS) over dorsal-lateral PPC perturbs the early stages of spatial processing for memory-guided reaching. However, our data did not distinguish whether TMS disrupted the reach goal or the internal estimate of initial hand position needed to calculate the reach vector. To test between these hypotheses, we investigated reaching in six healthy humans during left and right parietal TMS while varying visual feedback of the movement. We reasoned that if TMS were disrupting the internal representation of hand position, visual feedback from the hand might still recalibrate this signal. We tested four viewing conditions: 1) final vision of hand position; 2) full vision of hand position; 3) initial and final vision of hand position; and 4) middle and final vision of hand position. During the final vision condition, left parietal stimulation significantly increased endpoint variability, whereas right parietal stimulation produced a significant leftward shift in both visual fields. However, these errors significantly decreased with visual feedback of the hand during both planning and control stages of the reach movement. These new findings demonstrate that 1) visual feedback of hand position during the planning and early execution of the reach can recalibrate the perturbed signal and, importantly, and 2) TMS over dorsal-lateral PPC does not disrupt the internal representation of the visual goal, but rather the reach vector, or more likely the sense of initial hand position that is used to calculate this vector.

Human parietal and primary motor cortical interactions are selectively modulated during the transport and grip formation of goal-directed hand actions

Posterior parietal cortex (PPC) constitutes a critical cortical node in the sensorimotor system in which goal-directed actions are computed. This information then must be transferred into commands suitable for hand movements to the primary motor cortex (M1). Complexity arises because reach-to-grasp actions not only require directing the hand towards the object (transport component), but also preshaping the hand according to the features of the object (grip component). Yet, the functional influence that specific PPC regions exert over ipsilateral M1 during the planning of different hand movements remains unclear in humans. Here we manipulated transport and grip components of goal-directed hand movements and exploited paired-pulse transcranial magnetic stimulation ((pp)TMS) to probe the functional interactions between M1 and two different PPC regions, namely superior parieto-occipital cortex (SPOC) and the anterior region of the intraparietal sulcus (aIPS), in the left hemisphere. We show that when the extension of the arm is required to contact a target object, SPOC selectively facilitates motor evoked potentials, suggesting that SPOC-M1 interactions are functionally specific to arm transport. In contrast, a different pathway, linking the aIPS and ipsilateral M1, shows enhanced functional connections during the sensorimotor planning of grip. These results support recent human neuroimaging findings arguing for specialized human parietal regions for the planning of arm transport and hand grip during goal-directed actions. Importantly, they provide new insight into the causal influences these different parietal regions exert over ipsilateral motor cortex for specific types of planned hand movements.

TMS Over Human Frontal Eye Fields Disrupts Trans-saccadic Memory of Multiple Objects

We recently showed that transcranial magnetic stimulation (TMS) over the right parietal eye fields disrupts memory of object features and locations across saccades. We applied TMS over the frontal eye fields (FEF) as subjects compared the feature details of visual targets presented either within a single eye fixation (Fixation Task) or across a saccade (Saccade Task). TMS pulses were randomly delivered at one of 3 time intervals around the time of the saccade, or at equivalent times in the Fixation Task. A No-TMS control confirmed that subjects could normally retain approximately 3 visual features. TMS in the Fixation Task had no effect compared with No-TMS, but differences among TMS times were found during right FEF stimulation. TMS over either the right or left FEF disrupted memory performance in the Saccade Task when stimulation coincided most closely with the saccade. The capacity to compare pre-and postsaccadic features was reduced to 1-2 objects, as expected if the spatial aspect of memory was disrupted. These findings suggest that the FEF plays a role in the spatial processing involved in trans-saccadic memory of visual features. We propose that this process employs saccade-related feedback signals similar to those observed in spatial updating.

Correlations of Selected Psychomotor and Visuomotor Tests with Initial Dynavision Performance

The current study investigated the relationship between Dynavision scores for 36 men and 52 women (M age = 20.5 yr.) and performance on six conventional psychomotor tests which presumably tap similar psychomotor abilities and visuomotor skills. Analysis indicated that initial Dynavision performance was significantly correlated with performance on these common psychomotor tests. These data extend findings that propose the effectiveness of the Dynavision apparatus to assess performance on basic visual-motor and visual-cognitive functions. Taken together with these new results, findings suggest that this apparatus might contribute to psychomotor assessment and may be potentially useful for effective selection and identification of individual differences in human behavioral performance.

Modulation of left primary motor cortex excitability after bimanual training and intermittent theta burst stimulation to left dorsal premotor cortex

Bimanual visuomotor movement training (BMT) enhances the excitability of human preparatory premotor and primary motor (M1) cortices compared to unimanual movement. This occurs when BMT involves mirror symmetrical movements of both upper-limbs (in-phase) but not with non-symmetrical movements (anti-phase). The neural mechanisms mediating the effect of BMT is unclear, but may involve interhemispheric connections between homologous M1 representations as well as the dorsal premotor cortices (PMd). The purpose of this study is to assess how intermittent theta burst stimulation (iTBS) of the left PMd affects left M1 excitability, and the possible combined effects of iTBS to left PMd applied before a single session of BMT. Left M1 excitability was quantified using transcranial magnetic stimulation (TMS) in terms of both the amplitudes and spatial extent of motor evoked potentials (MEPs) for the extensor carpi radialis (ECR) before and multiple time points following (1) BMT, (2) iTBS to left PMd or (3) iTBS to left PMd and BMT. Although there was not a greater increase in either specific measure of M1 excitability due to the combination of the interventions, iTBS applied before BMT showed that both the spatial extent and global MEP amplitude for the ECR became larger in parallel, whereas the spatial extent was enhanced with BMT alone and global MEP amplitude was enhanced with iTBS to left PMd alone. These results suggest that the modulation of rapid functional M1 excitability associated with BMT and iTBS of the left PMd could operate under related early markers of neuro-plastic mechanisms, which may be expressed in concurrent and distinct patterns of M1 excitability. Critically, this work may guide rehabilitation training and stimulation techniques that modulate cortical excitability after brain injury.

The role of areas MT+/V5 and SPOC in spatial and temporal control of manual interception: an rTMS study

Manual interception, such as catching or hitting an approaching ball, requires the hand to contact a moving object at the right location and at the right time. Many studies have examined the neural mechanisms underlying the spatial aspects of goal-directed reaching, but the neural basis of the spatial and temporal aspects of manual interception are largely unknown. Here, we used repetitive transcranial magnetic stimulation (rTMS) to investigate the role of the human middle temporal visual motion area (MT+/V5) and superior parieto-occipital cortex (SPOC) in the spatial and temporal control of manual interception. Participants were required to reach-to-intercept a downward moving visual target that followed an unpredictably curved trajectory, presented on a screen in the vertical plane. We found that rTMS to MT+/V5 influenced interceptive timing and positioning, whereas rTMS to SPOC only tended to increase the spatial variance in reach end points for selected target trajectories. These findings are consistent with theories arguing that distinct neural mechanisms contribute to spatial, temporal, and spatiotemporal control of manual interception.