Dynamic Circuitry for Updating Spatial Representations. I. Behavioral Evidence for Interhemispheric Transfer in the Split-Brain Macaque

2005 ◽  
Vol 94 (5) ◽  
pp. 3228-3248 ◽  
Author(s):  
Rebecca A. Berman ◽  
Laura M. Heiser ◽  
Richard C. Saunders ◽  
Carol L. Colby
Keyword(s):  
Visual Representations ◽  
Visual Space ◽  
Spatial Updating ◽  
Spatial Representations ◽  
Double Step ◽  
Split Brain ◽  
Stable Representation ◽  
Accurate Performance ◽  
Behavioral Evidence ◽  
Visual Hemifields

Internal representations of the sensory world must be constantly adjusted to take movements into account. In the visual system, spatial updating provides a mechanism for maintaining a coherent map of salient locations as the eyes move. Little is known, however, about the pathways that produce updated spatial representations. In the present study, we asked whether direct cortico-cortical links are required for spatial updating. We addressed this question by investigating whether the forebrain commissures—the direct path between the two cortical hemispheres—are necessary for updating visual representations from one hemifield to the other. We assessed spatial updating in two split-brain monkeys using the double-step task, which involves saccades to two sequentially appearing targets. Accurate performance requires that the representation of the second target be updated to take the first saccade into account. We made two central discoveries regarding the pathways that underlie spatial updating. First, we found that split-brain monkeys exhibited a selective initial impairment on double-step sequences that required updating across visual hemifields. Second, and most surprisingly, these impairments were neither universal nor permanent: the monkeys were ultimately able to perform the across-hemifield sequences and, in some cases, this ability emerged rapidly. These findings indicate that direct cortical links provide the main substrate for updating visual representations, but they are not the sole substrate. Rather, a unified and stable representation of visual space is supported by a redundant cortico-subcortical network with a striking capacity for reorganization.

scholarly journals Dynamic Circuitry for Updating Spatial Representations. III. From Neurons to Behavior

2007 ◽  
Vol 98 (1) ◽  
pp. 105-121 ◽  
Author(s):  
Rebecca A. Berman ◽  
Laura M. Heiser ◽  
Catherine A. Dunn ◽  
Richard C. Saunders ◽  
Carol L. Colby
Keyword(s):  
Spatial Behavior ◽  
Neuron Activity ◽  
Spatial Representations ◽  
Behavioral Performance ◽  
Double Step ◽  
Population Activity ◽  
Extensive Experience ◽  
Split Brain ◽  
Lateral Intraparietal Cortex ◽  
The Difference

Each time the eyes move, the visual system must adjust internal representations to account for the accompanying shift in the retinal image. In the lateral intraparietal cortex (LIP), neurons update the spatial representations of salient stimuli when the eyes move. In previous experiments, we found that split-brain monkeys were impaired on double-step saccade sequences that required updating across visual hemifields, as compared to within hemifield. Here we describe a subsequent experiment to characterize the relationship between behavioral performance and neural activity in LIP in the split-brain monkey. We recorded from single LIP neurons while split-brain and intact monkeys performed two conditions of the double-step saccade task: one required across-hemifield updating and the other required within-hemifield updating. We found that, despite extensive experience with the task, the split-brain monkeys were significantly more accurate for within-hemifield than for across-hemifield sequences. In parallel, we found that population activity in LIP of the split-brain monkeys was significantly stronger for the within-hemifield than for the across-hemifield condition of the double-step task. In contrast, in the normal monkey, both the average behavioral performance and population activity showed no bias toward the within-hemifield condition. Finally, we found that the difference between within-hemifield and across-hemifield performance in the split-brain monkeys was reflected at the level of single-neuron activity in LIP. These findings indicate that remapping activity in area LIP is present in the split-brain monkey for the double-step task and covaries with spatial behavior on within-hemifield compared to across-hemifield sequences.

Dynamic Circuitry for Updating Spatial Representations. II. Physiological Evidence for Interhemispheric Transfer in Area LIP of the Split-Brain Macaque

2005 ◽  
Vol 94 (5) ◽  
pp. 3249-3258 ◽  
Author(s):  
Laura M. Heiser ◽  
Rebecca A. Berman ◽  
Richard C. Saunders ◽  
Carol L. Colby
Keyword(s):  
Eye Movements ◽  
Visual Representations ◽  
The Other ◽  
Spatial Representations ◽  
Lateral Intraparietal Area ◽  
Split Brain ◽  
Perceptual Stability ◽  
Visual Hemifield ◽  
Principal Finding ◽  
The Brain

With each eye movement, a new image impinges on the retina, yet we do not notice any shift in visual perception. This perceptual stability indicates that the brain must be able to update visual representations to take our eye movements into account. Neurons in the lateral intraparietal area (LIP) update visual representations when the eyes move. The circuitry that supports these updated representations remains unknown, however. In this experiment, we asked whether the forebrain commissures are necessary for updating in area LIP when stimulus representations must be updated from one visual hemifield to the other. We addressed this question by recording from LIP neurons in split-brain monkeys during two conditions: stimulus traces were updated either across or within hemifields. Our expectation was that across-hemifield updating activity in LIP would be reduced or abolished after transection of the forebrain commissures. Our principal finding is that LIP neurons can update stimulus traces from one hemifield to the other even in the absence of the forebrain commissures. This finding provides the first evidence that representations in parietal cortex can be updated without the use of direct cortico-cortical links. The second main finding is that updating activity in LIP is modified in the split-brain monkey: across-hemifield signals are reduced in magnitude and delayed in onset compared with within-hemifield signals, which indicates that the pathways for across-hemifield updating are less effective in the absence of the forebrain commissures. Together these findings reveal a dynamic circuit that contributes to updating spatial representations.

scholarly journals Spatial Updating in Monkey Superior Colliculus in the Absence of the Forebrain Commissures: Dissociation Between Superficial and Intermediate Layers

2010 ◽  
Vol 104 (3) ◽  
pp. 1267-1285 ◽  
Author(s):  
Catherine A. Dunn ◽  
Nathan J. Hall ◽  
Carol L. Colby
Keyword(s):  
Superior Colliculus ◽  
The Other ◽  
Spatial Updating ◽  
Subcortical Structure ◽  
Double Step ◽  
Split Brain ◽  
Lateral Intraparietal Cortex ◽  
Behavioral Level ◽  
Intermediate Layers

In previous studies, we demonstrated that the forebrain commissures are the primary pathway for remapping from one hemifield to the other. Nonetheless, remapping in lateral intraparietal cortex (LIP) across hemifield is still present in split brain monkeys. This finding indicates that a subcortical structure must contribute to remapping. The primary goal of the current study was to characterize remapping activity in the superior colliculus in intact and split brain monkeys. We recorded neurons in both the superficial and intermediate layers of the SC. We found that across-hemifield remapping was reduced in magnitude and delayed compared with within-hemifield remapping in the intermediate layers of the SC in split brain monkeys. These results mirror our previous findings in area LIP. In contrast, we found no difference in the magnitude or latency for within- compared with across-hemifield remapping in the superficial layers. At the behavioral level, we compared the performance of the monkeys on two conditions of a double-step task. When the second target remained within a single hemifield, performance remained accurate. When the second target had to be updated across hemifields, the split brain monkeys' performance was impaired. Remapping activity in the intermediate layers was correlated with the accuracy and latency of the second saccade during the across-hemifield trials. Remapping in the superficial layers was correlated with latency of the second saccade during the within- and across-hemifield trials. The differences between the layers suggest that different circuits underlie remapping in the superficial and intermediate layers of the superior colliculus.

scholarly journals Remapping for visual stability

2011 ◽  
Vol 366 (1564) ◽  
pp. 528-539 ◽  
Author(s):  
Nathan J. Hall ◽  
Carol L. Colby
Keyword(s):  
Visual Representations ◽  
Visual Space ◽  
Neural Circuitry ◽  
Single Neurons ◽  
Visual Stability ◽  
Lateral Intraparietal Area ◽  
Cortical Connections ◽  
Stable Representation ◽  
Temporal And Spatial ◽  
New Evidence

Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.

scholarly journals Parallel updating and weighting of multiple spatial maps for visual stability during whole body motion

2015 ◽  
Vol 114 (6) ◽  
pp. 3211-3219 ◽  
Author(s):  
J. J. Tramper ◽  
W. P. Medendorp
Keyword(s):  
Reference Frame ◽  
Reference Frames ◽  
Spatial Information ◽  
Target Location ◽  
Visual Space ◽  
Body Motion ◽  
Whole Body ◽  
Spatial Representations ◽  
Integration Model ◽  
The Brain

It is known that the brain uses multiple reference frames to code spatial information, including eye-centered and body-centered frames. When we move our body in space, these internal representations are no longer in register with external space, unless they are actively updated. Whether the brain updates multiple spatial representations in parallel, or whether it restricts its updating mechanisms to a single reference frame from which other representations are constructed, remains an open question. We developed an optimal integration model to simulate the updating of visual space across body motion in multiple or single reference frames. To test this model, we designed an experiment in which participants had to remember the location of a briefly presented target while being translated sideways. The behavioral responses were in agreement with a model that uses a combination of eye- and body-centered representations, weighted according to the reliability in which the target location is stored and updated in each reference frame. Our findings suggest that the brain simultaneously updates multiple spatial representations across body motion. Because both representations are kept in sync, they can be optimally combined to provide a more precise estimate of visual locations in space than based on single-frame updating mechanisms.

scholarly journals Representation of the Ipsilateral Visual Field by Neurons in the Macaque Lateral Intraparietal Cortex Depends on the Forebrain Commissures

2010 ◽  
Vol 104 (5) ◽  
pp. 2624-2633 ◽  
Author(s):  
Catherine A. Dunn ◽  
Carol L. Colby
Keyword(s):  
Receptive Field ◽  
Eye Movement ◽  
Visual Information ◽  
Visual Fields ◽  
Receptive Fields ◽  
Neural Mechanism ◽  
Brain Regions ◽  
Spatial Updating ◽  
Split Brain ◽  
Lateral Intraparietal Cortex

Our eyes are constantly moving, allowing us to attend to different visual objects in the environment. With each eye movement, a given object activates an entirely new set of visual neurons, yet we perceive a stable scene. One neural mechanism that may contribute to visual stability is remapping. Neurons in several brain regions respond to visual stimuli presented outside the receptive field when an eye movement brings the stimulated location into the receptive field. The stored representation of a visual stimulus is remapped, or updated, in conjunction with the saccade. Remapping depends on neurons being able to receive visual information from outside the classic receptive field. In previous studies, we asked whether remapping across hemifields depends on the forebrain commissures. We found that, when the forebrain commissures are transected, behavior dependent on accurate spatial updating is initially impaired but recovers over time. Moreover, neurons in lateral intraparietal cortex (LIP) continue to remap information across hemifields in the absence of the forebrain commissures. One possible explanation for the preserved across-hemifield remapping in split-brain animals is that neurons in a single hemisphere could represent visual information from both visual fields. In the present study, we measured receptive fields of LIP neurons in split-brain monkeys and compared them with receptive fields in intact monkeys. We found a small number of neurons with bilateral receptive fields in the intact monkeys. In contrast, we found no such neurons in the split-brain animals. We conclude that bilateral representations in area LIP following forebrain commissures transection cannot account for remapping across hemifields.

scholarly journals Sounds are remapped across saccades

2019 ◽  
Author(s):  
Martin Szinte ◽  
David Aagten-Murphy ◽  
Donatas Jonikaitis ◽  
Luca Wollenberg ◽  
Heiner Deubel
Keyword(s):  
Visual Space ◽  
Double Step ◽  
Visual Objects ◽  
Object Locations ◽  
Space Constancy ◽  
Saccade Task ◽  
Saccade Trajectory

AbstractTo 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.

Directional Selectivity of BOLD Activity in Human Posterior Parietal Cortex for Memory-Guided Double-Step Saccades

2006 ◽  
Vol 95 (3) ◽  
pp. 1645-1655 ◽  
Author(s):  
W. Pieter Medendorp ◽  
Herbert C. Goltz ◽  
Tutis Vilis
Keyword(s):  
Visual Field ◽  
Parietal Cortex ◽  
Posterior Parietal Cortex ◽  
Target Location ◽  
Double Step ◽  
Fmri Signal ◽  
Posterior Parietal ◽  
Visual Hemifields ◽  
Target Locations

We used functional magnetic resonance imaging (fMRI) to investigate the role of the human posterior parietal cortex (PPC) in storing target locations for delayed double-step saccades. To do so, we exploited the laterality of a subregion of PPC that preferentially responds to the memory of a target location presented in the contralateral visual field. Using an event-related design, we tracked fMRI signal changes in this region while subjects remembered the locations of two sequentially flashed targets, presented in either the same or different visual hemifields, and then saccaded to them in sequence. After presentation of the first target, the fMRI signal was always related to the side of the visual field in which it had been presented. When the second target was added, the cortical activity depended on the respective locations of both targets but was still significantly selective for the target of the first saccade. We conclude that this region within the human posterior parietal cortex not only acts as spatial storage center by retaining target locations for subsequent saccades but is also involved in selecting the target for the first intended saccade.

Processing symmetry between visual and auditory spatial representations in updating working memory

2021 ◽  
Author(s):  
Tomoki Maezawa ◽  
Jun Kawahara
Keyword(s):  
Working Memory ◽  
Visual Cues ◽  
Spatial Information ◽  
Spatial Working Memory ◽  
Spatial Updating ◽  
Spatial Representations ◽  
Attentional Resources ◽  
Visual Spatial ◽  
Matrix Surface ◽  
Memory Representations

Updating spatial representations in visual and auditory working memory relies on common processes, and the modalities should compete for attentional resources. The present study examined the relative dominance of memory updating using incompatible spatial information conveyed from two different cue modalities. Participants maneuvered a designated target on a matrix surface according to visual or auditory stimuli that were simultaneously presented, to identify a terminal location. Prior to the navigation task, the relative perceptual salience of the visual cues was manipulated to be equal, superior, or inferior to the auditory cues. The results demonstrated that visual and auditory inputs competed for attentional resources such that visual/auditory guidance was impaired by incongruent cues delivered from the other modality. Although visual dominance was favored in working memory navigation on average, stimuli of relatively high salience interfered with or facilitated other stimuli regardless of modality, demonstrating the similarity of updating processes in visual and auditory spatial working memory. Furthermore, processing asymmetry can be identified during the encoding of sensory inputs into working memory representations. The present results suggest that auditory spatial updating is comparable to visual spatial updating in that salient stimuli receive a high priority when selecting inputs and are used when tracking spatial representations.

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