J. D. Crawford

Visuospatial updating of reaching targets in near and far space.

&NA; The brain constructs multiple representations of near and far space but it is unclear which spatial mechanism guides reaching across eye movements in near space. Retinocentric reaching representations are known to exist in parietal cortex, but must be updated during eye movements, in order to remain accurate. In contrast, non‐retinal (e.g. muscle‐centered) reaching plans in motor cortex do not require updating, and so may provide a more stable encoding mechanism. To test between these, we employed a behavioral test. Subjects briefly foveated a target (located at various depths in near and far space) looked peripherally, then reached toward its remembered location. Surprisingly, subjects did not use the stable non‐retinal reaching plan (compared to controls without eye movements). Instead, the intervening eye movements induced a systematic pattern of reaching errors for targets at all depths consistent with updating in a retinal frame. We conclude that a common eye‐centered updating mechanism prevails in programming arm movements in both near and far space.

Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties

Grasping behaviors require the selection of grasp-relevant object dimensions, independent of overall object size. Previous neuroimaging studies found that the intraparietal cortex processes object size, but it is unknown whether the graspable dimension (i.e., grasp axis between selected points on the object) or the overall size of objects triggers activation in that region. We used functional magnetic resonance imaging adaptation to investigate human brain areas involved in processing the grasp-relevant dimension of real 3-dimensional objects in grasping and viewing tasks. Trials consisted of 2 sequential stimuli in which the objects grasp-relevant dimension, its global size, or both were novel or repeated. We found that calcarine and extrastriate visual areas adapted to object size regardless of the grasp-relevant dimension during viewing tasks. In contrast, the superior parietal occipital cortex (SPOC) and lateral occipital complex of the left hemisphere adapted to the grasp-relevant dimension regardless of object size and task. Finally, the dorsal premotor cortex adapted to the grasp-relevant dimension in grasping, but not in viewing, tasks, suggesting that motor processing was complete at this stage. Taken together, our results provide a complete cortical circuit for progressive transformation of general object properties into grasp-related responses.

Spatial updating across saccades during manual interception

We studied the effect of intervening saccades on the manual interception of a moving target. Previous studies suggest that stationary reach goals are coded and updated across saccades in gaze-centered coordinates, but whether this generalizes to interception is unknown. Subjects (n = 9) reached to manually intercept a moving target after it was rendered invisible. Subjects either fixated throughout the trial or made a saccade before reaching (both fixation points were in the range of -10° to 10°). Consistent with previous findings and our control experiment with stationary targets, the interception errors depended on the direction of the remembered moving goal relative to the new eye position, as if the target is coded and updated across the saccade in gaze-centered coordinates. However, our results were also more variable in that the interception errors for more than half of our subjects also depended on the goal direction relative to the initial gaze direction. This suggests that the feedforward transformations for interception differ from those for stationary targets. Our analyses show that the interception errors reflect a combination of biases in the (gaze-centered) representation of target motion and in the transformation of goal information into body-centered coordinates for action.

3-DIMENSIONAL EYE-HEAD COORDINATION IN GAZE SHIFTS EVOKED DURING STIMULATION OF THE LATERAL INTRAPARIETAL CORTEX

Coordinated eye-head gaze shifts have been evoked during electrical stimulation of the frontal cortex (supplementary eye field (SEF) and frontal eye field (FEF)) and superior colliculus (SC), but less is known about the role of lateral intraparietal cortex (LIP) in head-unrestrained gaze shifts. To explore this, two monkeys (M1 and M2) were implanted with recording chambers and 3-D eye+ head search coils. Tungsten electrodes delivered trains of electrical pulses (usually 200 ms duration) to and around area LIP during head-unrestrained gaze fixations. A current of 200 muA consistently evoked small, short-latency contralateral gaze shifts from 152 sites in M1 and 243 sites in M2 (Constantin et al., 2007). Gaze kinematics were independent of stimulus amplitude and duration, except that subsequent saccades were suppressed. The average amplitude of the evoked gaze shifts was 8.46 degrees for M1 and 8.25 degrees for M2, with average head components of only 0.36 and 0.62 degrees respectively. The heads amplitude contribution to these movements was significantly smaller than in normal gaze shifts, and did not increase with behavioral adaptation. Stimulation-evoked gaze, eye and head movements qualitatively obeyed normal 3-D constraints (Donders law and Listings law), but with less precision. As in normal behavior, when the head was restrained LIP stimulation evoked eye-only saccades in Listings plane, whereas when the head was not restrained, stimulation evoked saccades with position-dependent torsional components (driving the eye out of Listings plane). In behavioral gaze-shifts, the vestibuloocular reflex (VOR) then drives torsion back into Listings plane, but in the absence of subsequent head movement the stimulation-induced torsion was left hanging. This suggests that the position-dependent torsional saccade components are preprogrammed, and that the oculomotor system was expecting a head movement command to follow the saccade. These data show that, unlike SEF, FEF, and SC stimulation in nearly identical conditions, LIP stimulation fails to produce normally-coordinated eye-head gaze shifts.

The effects of TMS over dorsolateral prefrontal cortex on trans-saccadic memory of multiple objects

Humans typically make several rapid eye movements (saccades) per second. It is thought that visual working memory can retain and spatially integrate three to four objects or features across each saccade but little is known about this neural mechanism. Previously we showed that transcranial magnetic stimulation (TMS) to the posterior parietal cortex and frontal eye fields degrade trans-saccadic memory of multiple object features (Prime, Vesia, & Crawford, 2008, Journal of Neuroscience, 28(27), 6938-6949; Prime, Vesia, & Crawford, 2010, Cerebral Cortex, 20(4), 759-772.). Here, we used a similar protocol to investigate whether dorsolateral prefrontal cortex (DLPFC), an area involved in spatial working memory, is also involved in trans-saccadic memory. Subjects were required to report changes in stimulus orientation with (saccade task) or without (fixation task) an eye movement in the intervening memory interval. We applied single-pulse TMS to left and right DLPFC during the memory delay, timed at three intervals to arrive approximately 100 ms before, 100 ms after, or at saccade onset. In the fixation task, left DLPFC TMS produced inconsistent results, whereas right DLPFC TMS disrupted performance at all three intervals (significantly for presaccadic TMS). In contrast, in the saccade task, TMS consistently facilitated performance (significantly for left DLPFC/perisaccadic TMS and right DLPFC/postsaccadic TMS) suggesting a dis-inhibition of trans-saccadic processing. These results are consistent with a neural circuit of trans-saccadic memory that overlaps and interacts with, but is partially separate from the circuit for visual working memory during sustained fixation.

A computational model to study the dynamics of updating of remembered visual targets during rapid and slow eye movements

After an intervening eye movement, or saccade, humans and animals are able to localize previously perceived visual targets (spatial updating). Although efforts have been made to discover the mechanism underlying spatial updating, there are still many unanswered questions about the neuronal mechanism of this phenomenon. State space model is an effective method for modeling dynamical systems and it can represent the internal behaviour of these systems. Therefore, we developed a state space model for updating target-related spatial information in gaze-centered coordinates. We considered three types of input in our proposed model: 1) an efference copy signal, inspired by motor burst in SC, 2) an eye position signal, found in LIP, VIP, MT and MST areas and 3) visual topographic maps of visual stimuli, located in SC. To model the internal neuronal behaviour of the system, we developed a radial basis function neural network (RBFNN) which can be trained with an Extended Kalman filter method. This RBFNN represents the state space and we can obtain a topographic map of the remembered target in its hidden layer. From our proposed model, the output obtained is the decoded location of the remembered target. To explore the internal mechanism underlying the updating process, we trained this model on a double-step saccade-saccade or pursuit-saccade task. After training, the receptive fields of state-space units replicated both predictive remapping during saccades (Duhamel et al. Science 1992) and continuous eye-centered updating during smooth pursuit (Dash et al. Current Biology, in press). In addition, during trans-saccadic remapping, receptive fields also expanded (to our knowledge, this predicted expansion has not yet been reported in the published literature). In the future, we plan to incorporate this framework within a more comprehensive model of trans-saccadic integration of both spatial and feature information, and use this framework to construct a physiologically plausible model. Meeting abstract presented at VSS 2015.

Characteristics of remembered saccades in Parkinson's disease

Saccades to a remembered target use non-visual feedback and rely on a normal functioning of the projection from the caudate nucleus to the substantia nigra pars reticulata. The latter projection is known to be defective in Parkinsons disease and it seems therefore likely that remembered saccades are abnormal in such patients. In a series of three studies the characteristics of remembered saccades were compared with those of reflex saccades in patients with Parkinsons disease and normals. It was found that the remembered saccades of the patients were more hypometric than those of normals but that the final eye position was normal. Latency and peak velocity were normal as well. The patients exhibited an increased incidence of multistepping (“staircase saccades”). Using an inverse reconstruction technique, evidence was obtained for the presence of pulse doublets at the input of the oculomotor plant in such cases.

Transsaccadic feature interactions in multiple reference frames: an fMRIa study

Transsaccadic integration of visual features can operate in various frames of reference, but the corresponding neural mechanisms have not been differentiated. A recent fMRIa (adaptation) study identified two cortical regions in supramarginal gyrus (SMG) and extrastriate cortex that were sensitive to transsaccadic changes in stimulus orientation (Dunkley et al., 2016). Here, we modified this paradigm to identify the neural correlates for transsaccadic comparison of object orientations in: 1) Spatially Congruent (SC), 2) Retinally Congruent (RC) or 3) Spatially Incongruent (SI)) coordinates. Functional data were recorded from 12 human participants while they observed a grating (oriented 45° or 135°) before a saccade, and then judged whether a post-saccadic grating (in SC, RC, or SI configuration) had the same or different orientation. Our analysis focused on areas that showed a significant repetition suppression (Different > Same) or repetition enhancement (Same > Different) BOLD responses. Several cortical areas were significantly modulated in all three conditions: premotor/motor cortex (likely related to the manual response), and posterior-middle intraparietal sulcus. In the SC condition, uniquely activated areas included left SMG and left lateral occipitotemporal gyrus (LOtG). In the RC condition, unique areas included inferior frontal gyrus and the left lateral BA 7. In the SI condition, uniquely activated areas included the frontal eye field, medial BA 7, and right LOtG. Overall, the SC results were significantly different from both RC and SI. These data suggest that different cortical networks are used to compare pre- and post-saccadic orientation information, depending on the spatial nature of the task. Significance Statement Every time one makes a saccade, the brain must compare and integrate stored visual information with new information. It has recently been shown that ‘transsaccadic integration’ of visual object orientation involves specific areas within parietal and occipital cortex (Dunkley et al., 2016). Here, we show that this pattern of cortical activation also depends on the spatial nature of the task: when the visual object is fixed relative to space, the eye, or relative to neither space nor the eye, different frontal, parietal, and occipital regions are engaged. More generally, these findings suggest that different aspects of trans-saccadic integration flexibly employ different cortical networks.

Space-fixed, retina-fixed, and frame-independent mechanisms of trans-saccadic feature integration: repetition suppression and enhancement in an fMRIa paradigm.

To date, the neural mechanisms of feature information integration across saccades, also known as trans-saccadic integration (TSI), of low-level object features are relatively unknown. Using fMRI adaptation (fMRIa), we found that the right inferior parietal lobule (IPL; specifically, SMG) and extrastriate cortex (putative V4) are sensitive to stimulus orientation in a space-fixed reference frame (Dunkley & Crawford, Society for Neuroscience Abstracts, 2012). To identify the neural mechanisms of underlying TSI in multiple reference frames, we employed fMRIa to probe three spatial conditions: 1) Space-fixed, 2) Retina-fixed and 3) Frame-independent (neither Space-fixed, nor Retina-fixed). Functional data were collected across 12 participants while they observed an obliquely oriented grating (45° or 135°), followed by a grating at the same (Repeat condition) or different angle (Novel condition). Participants were instructed to decide via 2AFC if the subsequent grating was repeated or novel. Repeat vs. Novel contrasts showed repetition suppression (RS) and enhancement (RE). RS showed condition-specific patterns within a parieto-frontal network. Distinct areas of activation were identified for the three conditions (i.e., SMG for Condition 1; middle and inferior frontal gyri (MFG, IFG) for Condition 2; and FEF and area 7 for Condition 3) as well as common clusters (i.e., posterior middle intraparietal sulcus, M1 and pre-supplementary area). RE was observed in occipito-temporal areas. Specifically, RE in Condition 1 was observed in cuneus, inferior occipital gyrus, medial occipitotemporal gyrus (MOtG), lateral occipitotemporal gyrus (LOtG) and MFG. RE in Condition 2 was observed in lingual gyrus (LG) and MOtG. In Condition 3, RE was found in cuneus, LOtG, middle occipital gyrus and LG. Shared RE areas included cuneus, LG and MOtG. Overall, TSI of orientation activated different cortical patterns (with some parietal overlap) in the three frames. Further, suppression occurred in a cognitive-sensorimotor, parieto-frontal network, whereas enhancement occurred in an early visual, occipital network. Meeting abstract presented at VSS 2015.