Eye-centered Representation Research Articles

Sounds are remapped across saccades

To achieve visual space constancy, our brain remaps eye-centered projections of visual objects across saccades. Here, we measured saccade trajectory curvature following the presentation of visual, auditory, and audiovisual distractors in a double-step saccade task to investigate if this stability mechanism also accounts for localized sounds. We found that saccade trajectories systematically curved away from the position at which either a light or a sound was presented, suggesting that both modalities are represented in eye-centered oculomotor centers. Importantly, the same effect was observed when the distractor preceded the execution of the first saccade. These results suggest that oculomotor centers keep track of visual, auditory and audiovisual objects by remapping their eye-centered representations across saccades. Furthermore, they argue for the existence of a supra-modal map which keeps track of multi-sensory object locations across our movements to create an impression of space constancy.

Multiple Coordinate Systems and Motor Strategies for Reaching Movements When Eye and Hand Are Dissociated in Depth and Direction

Reaching behavior represents one of the basic aspects of human cognitive abilities important for the interaction with the environment. Reaching movements towards visual objects are controlled by mechanisms based on coordinate systems that transform the spatial information of target location into appropriate motor response. Although recent works have extensively studied the encoding of target position for reaching in three-dimensional space at behavioral level, the combined analysis of reach errors and movement variability has so far been investigated by few studies. Here we did so by testing 12 healthy participants in an experiment where reaching targets were presented at different depths and directions in foveal and peripheral viewing conditions. Each participant executed a memory-guided task in which he/she had to reach the memorized position of the target. A combination of vector and gradient analysis, novel for behavioral data, was applied to analyze patterns of reach errors for different combinations of eye/target positions. The results showed reach error patterns based on both eye- and space-centered coordinate systems: in depth more biased towards a space-centered representation and in direction mixed between space- and eye-centered representation. We calculated movement variability to describe different trajectory strategies adopted by participants while reaching to the different eye/target configurations tested. In direction, the distribution of variability between configurations that shared the same eye/target relative configuration was different, whereas in configurations that shared the same spatial position of targets, it was similar. In depth, the variability showed more similar distributions in both pairs of eye/target configurations tested. These results suggest that reaching movements executed in geometries that require hand and eye dissociations in direction and depth showed multiple coordinate systems and different trajectory strategies according to eye/target configurations and the two dimensions of space.

Visual Targets Aren’t Irreversibly Converted to Motor Coordinates: Eye-Centered Updating of Visuospatial Memory in Online Reach Control

Counter to current and widely accepted hypotheses that sensorimotor transformations involve converting target locations in spatial memory from an eye-fixed reference frame into a more stable motor-based reference frame, we show that this is not strictly the case. Eye-centered representations continue to dominate reach control even during movement execution; the eye-centered target representation persists after conversion to a motor-based frame and is continuously updated as the eyes move during reach, and is used to modify the reach plan accordingly during online control. While reaches are known to be adjusted online when targets physically shift, our results are the first to show that similar adjustments occur in response to changes in representations of remembered target locations. Specifically, we find that shifts in gaze direction, which produce predictable changes in the internal (specifically eye-centered) representation of remembered target locations also produce mid-transport changes in reach kinematics. This indicates that representations of remembered reach targets (and visuospatial memory in general) continue to be updated relative to gaze even after reach onset. Thus, online motor control is influenced dynamically by both the external and internal updating mechanisms.

Eye-Centered Representation of Optic Flow Tuning in the Ventral Intraparietal Area

Reference frames are important for understanding sensory processing in the cortex. Previous work showed that vestibular heading signals in the ventral intraparietal area (VIP) are represented in body-centered coordinates. In contrast, vestibular heading tuning in the medial superior temporal area (MSTd) is approximately head centered. We considered the hypothesis that visual heading signals (from optic flow) in VIP might also be transformed into a body-centered representation, unlike visual heading tuning in MSTd, which is approximately eye centered. We distinguished among eye-centered, head-centered, and body-centered spatial reference frames by systematically varying both eye and head positions while rhesus monkeys viewed optic flow stimuli depicting various headings. We found that heading tuning of VIP neurons based on optic flow generally shifted with eye position, indicating an eye-centered spatial reference frame. This is similar to the representation of visual heading signals in MSTd, but contrasts sharply with the body-centered representation of vestibular heading signals in VIP. These findings demonstrate a clear dissociation between the spatial reference frames of visual and vestibular signals in VIP, and emphasize that frames of reference for neurons in parietal cortex can depend on the type of sensory stimulation.

Heterogeneous Representations in the Superior Parietal Lobule Are Common across Reaches to Visual and Proprioceptive Targets

The planning and control of sensory-guided movements requires the integration of multiple sensory streams. Although the information conveyed by different sensory modalities is often overlapping, the shared information is represented differently across modalities during the early stages of cortical processing. We ask how these diverse sensory signals are represented in multimodal sensorimotor areas of cortex in macaque monkeys. Although a common modality-independent representation might facilitate downstream readout, previous studies have found that modality-specific representations in multimodal cortex reflect upstream spatial representations. For example, visual signals have a more eye-centered representation. We recorded neural activity from two parietal areas involved in reach planning, area 5 and the medial intraparietal area (MIP), as animals reached to visual, combined visual and proprioceptive, and proprioceptive targets while fixing their gaze on another location. In contrast to other multimodal cortical areas, the same spatial representations are used to represent visual and proprioceptive signals in both area 5 and MIP. However, these representations are heterogeneous. Although we observed a posterior-to-anterior gradient in population responses in parietal cortex, from more eye-centered to more hand- or body-centered representations, we do not observe the simple and discrete reference frame representations suggested by studies that focused on identifying the "best-match" reference frame for a given cortical area. In summary, we find modality-independent representations of spatial information in parietal cortex, although these representations are complex and heterogeneous.

Eye-movement-driven changes in the perception of auditory space

The perceptual localization of sensory stimuli often depends on body position, and, when action is required, sensory coordinates must be transformed into a motor reference frame. We investigated the role of such a reference frame change on visual and auditory spatial cognition. Participants had to make a saccade to a visual or auditory target and subsequently compare the location of a visual or auditory probe to the remembered location of the target. Neither visual nor auditory localization depended on trial-by-trial variability in saccade endpoint, suggesting that target locations are remapped across saccades in a manner allowing for oculomotor noise. We also compared visual and auditory localization performance before and after the systematic modification of saccade metrics by saccadic adaptation. Adaptation introduced systematic biases into transsaccadic visual and auditory localization behavior. These results show that information about eye movements is taken into account in both visual and auditory spatial cognition. We propose that auditory stimuli are remapped across saccades and that this eye-centered representation contributes to normal auditory localization.

Multisensory guidance of orienting behavior

We use both vision and audition when localizing objects and events in our environment. However, these sensory systems receive spatial information in different coordinate systems: sounds are localized using inter-aural and spectral cues, yielding a head-centered representation of space, whereas the visual system uses an eye-centered representation of space, based on the site of activation on the retina. In addition, the visual system employs a place-coded, retinotopic map of space, whereas the auditory system’s representational format is characterized by broad spatial tuning and a lack of topographical organization. A common view is that the brain needs to reconcile these differences in order to control behavior, such as orienting gaze to the location of a sound source. To accomplish this, it seems that either auditory spatial information must be transformed from a head-centered rate code to an eye-centered map to match the frame of reference used by the visual system, or vice versa. Here, we review a number of studies that have focused on the neural basis underlying such transformations in the primate auditory system. Although, these studies have found some evidence for such transformations, many differences in the way the auditory and visual system encode space exist throughout the auditory pathway. We will review these differences at the neural level, and will discuss them in relation to differences in the way auditory and visual information is used in guiding orienting movements.

Different Learned Coordinate Frames for Planning Trajectories and Final Positions in Reaching

We previously reported that the kinematics of reaching movements reflect the superimposition of two separate control mechanisms specifying the hand's spatial trajectory and its final equilibrium position. We now asked whether the brain maintains separate representations of the spatial goals for planning hand trajectory and final position. One group of subjects learned a 30 degrees visuomotor rotation about the hand's starting point while performing a movement reversal task ("slicing") in which they reversed direction at one target and terminated movement at another. This task required accuracy in acquiring a target mid-movement. A second group adapted while moving to -- and stabilizing at -- a single target ("reaching"). This task required accuracy in specifying an intended final position. We examined how learning in the two tasks generalized both to movements made from untrained initial positions and to movements directed toward untrained targets. Shifting initial hand position had differential effects on the location of reversals and final positions: Trajectory directions remained unchanged and reversal locations were displaced in slicing whereas final positions of both reaches and slices were relatively unchanged. Generalization across directions in slicing was consistent with a hand-centered representation of desired reversal point as demonstrated previously for this task whereas the distributions of final positions were consistent with an eye-centered representation as found previously in studies of pointing in three-dimensional space. Our findings indicate that the intended trajectory and final position are represented in different coordinate frames, reconciling previous conflicting claims of hand-centered (vectorial) and eye-centered representations in reach planning.

Is reaching eye-centered, body-centered, hand-centered, or a combination?

There are currently three main views on the neural basis of visually guided reaching: 1) neurons in the superior parietal lobe guide arm movements in a spatial framework that is centered on the body; 2) neurons in the intraparietal sulcus guide arm movements in a spatial framework that is centered on the eye; 3) neurons in the caudal part of premotor cortex guide arm movements in a spatial framework that is centered on the arm and hand. The three viewpoints are mutually compatible and may fit into a larger pattern. Eye-centered representations of target position, and body-centered representations of arm and hand position, may be integrated to form a hand-centered representation close to the output stage in caudal premotor and primary motor cortex.

Reaches to Sounds Encoded in an Eye-Centered Reference Frame

A recent hypothesis suggests that neurons in the lateral intraparietal area (LIP) and the parietal reach region (PRR) encode movement plans in a common eye-centered reference frame. To test this hypothesis further, we examined how PRR neurons encode reach plans to auditory stimuli. We found that PRR activity was affected by eye and initial hand position. Population analyses, however, indicated that PRR neurons were affected more strongly by eye position than by initial hand position. These eye position effects were appropriate to maintain coding in eye coordinates. Indeed, a significant population of PRR neurons encoded reaches to auditory stimuli in an eye-centered reference frame. These results extend the hypothesis that, regardless of the modality of the sensory input or the eventual action, PRR and LIP neurons represent movement plans in a common, eye-centered representation.

Saccade-related activity in the parietal reach region.

In previous experiments, we showed that cells in the parietal reach region (PRR) in monkey posterior parietal cortex code intended reaching movements in an eye-centered frame of reference. These cells are more active when an arm compared with an eye movement is being planned. Despite this clear preference for arm movements, we now report that PRR neurons also fire around the time of a saccade. Of 206 cells tested, 29% had perisaccadic activity in a delayed-saccade task. Two findings indicate that saccade-related activity does not reflect saccade planning or execution. First, activity is often peri- or postsaccadic but seldom presaccadic. Second, cells with saccade-related activity were no more likely to show strong saccadic delay period activity than cells without saccade-related activity. These findings indicate that PRR cells do not take part in saccade planning. Instead, the saccade-related activity in PRR may reflect cross-coupling between reach and saccade pathways that may be used to facilitate eye-hand coordination. Alternatively, saccade-related activity may reflect eye position information that could be used to maintain an eye-centered representation of intended reach targets across eye movements.

Effects of eye position on saccadic eye movements and on the neuronal responses to auditory and visual stimuli in cat superior colliculus.

Many neurons in the deeper layers of the superior colliculus (SC) respond to multiple sensory inputs--visual, auditory, and somatic--as well as provide signals essential for saccadic eye movements to targets in different modalities. When the eyes and pinnae are in primary position, the neural map of auditory space is in rough topographic alignment with the map of visual space, and if the auditory map is based solely on headpinna coordinates, any changes in eye position in the orbit will cause misalignment of the maps. We investigated the effects of eye position on the response of sound-sensitive neurons in the SC of cats because previous work on cats and on monkeys had suggested the possibility of species differences in the representation of auditory signals in the SC. We also investigated the effects of eye position on the accuracy of saccades to auditory, visual, and bimodal stimuli. All studies were conducted in alert, trained cats with the head restrained in a fixed position. Neuronal and behavioral responses were studied during periods when the eyes were steadily directed to different positions relative to the position of the sound. Cats showed partial compensation for eye position in making saccades, regardless of the modality of the target, and they showed similar patterns of error in saccades to auditory and visual targets. These behavioral data are consistent with coding the location of visual and auditory targets in the same coordinate system. In the vast majority of intermediate-layer neurons, eye position significantly affected the number of spikes evoked by sound stimuli. For most of these neurons, changes in eye position produced significant shifts in the speaker location producing maximal response. In some neurons, eye position significantly facilitated the magnitude of neuronal response evoked by sounds from a variety of speaker locations. Because few pinna movements could be detected, in is unlikely that these changes in neuronal response could be due to changes in the position of the pinnae. Our results indicate that the deep layers of the SC contain an eye-centered representation of sound location. Because eye position did not affect the percentage of neurons exhibiting multimodal integration, visual and auditory maps appear to remain integrated in the SC even when the eyes are directed eccentrically.(ABSTRACT TRUNCATED AT 400 WORDS)