Decoding the visuospatial map in primate cerebral cortex

During normal vision, the brain accomplishes the formidable task of converting a continuous stream of retinal images into a stable map of the environment.  This process is not trivial, since every time the eyes move, the image of the visual world on our retinae jumps in the opposite direction.  However, we appropriately take into account movements of our eyes and head and perceive that the world is stationary.  Moreover, we retain this ability even when we operate in the dark.

The neural circuitry underlying this ability to gauge motion in the external world as relative to our own is believed to reside within the cerebral hemispheres, where visual signals from occipital cortex converge with oculomotor and vestibular signals arising from brainstem pathways.  Electrophysiological recordings in the posterior parietal cortex (PPC) of the macaque monkey have revealed that neurons with spatially-tuned responses to visual stimuli can maintain their activity for many seconds after the visual stimulus has been extinguished.  Critically, this neuronal memory trace is not fixed, but rather appears to compensate for changes in gaze that alter the position of the memorized location relative to the eyes.  By studying the effects of various gaze perturbations on short-term visuospatial memory, we aim i) to characterize and quantify the interactions between visual, oculomotor, and vestibular systems in PPC, ii) to determine whether activity in PPC is sufficient to support accurate behavior in the absence of visual stimuli, and iii) to dissociate the specific roles of collaborating cortical regions, such as the frontal eye fields (FEF) and dorsolateral prefrontal cortex (DLPFC), in maintaining the brain’s map of space.

To examine the interactions between visual, oculomotor, and vestibular systems, we designed a paradigm in which subjects memorize spatial targets that either remain fixed in the world (world-fixed) or move with gaze (subject-fixed) after being extinguished.  Both are common scenarios in natural settings, but since only world-fixed targets change position relative to the eyes, PPC neurons should incorporate gaze signals only for world-fixed targets.  Therefore, subject-fixed targets serve as an internal control in which visual and gaze signals are matched, but the animal must effectively ignore the gaze information to solve the task.  To compare PPC activity in these situations, we recorded from 82 neurons in two monkeys trained to maintain spatial memories during three types of gaze perturbations: saccadic eye movements, smooth pursuit eye movements, and whole-body rotations.  Across the neuronal population, the spatial map was appropriately unchanged for subject-fixed targets regardless of the gaze perturbation.  However, for world-fixed targets, a more complex picture emerged.  Although the spatial map showed some compensation for gaze perturbations, only after saccadic perturbations was the accuracy of the map intact.  Following slow gaze shifts (whole-body rotation and smooth pursuit eye movements), there was a systemic error in the PPC map for world-fixed relative to subject-fixed targets.

These results support previous evidence that PPC can incorporate oculomotor and vestibular signals to update visual memories.  However, these data significantly advance our understanding of parietal spatial processing by suggesting that this incorporation is both flexible (occurs only when a target is believed to be part of the stable background) and imperfect (only after saccades was the map adequately updated).  And yet surprisingly, subjects performed equally accurately for both world-fixed and subject-fixed targets after all gaze perturbations (as evidenced by a final eye movement to the remembered location), suggesting that the spatial map in PPC is not sufficient to support spatially accurate behaviors under all conditions.  Rather, other brain areas, such as FEF and DLPFC, must contribute in these situations to maintain the integrity of the spatial map.  It is currently unknown whether and when neural circuits in these areas actively take part in visuospatial memory processing and when their activity merely reflects the input from areas where the spatial map is truly stored.

To establish the respective roles of cortical areas involved in short-term spatial memory, we will use a novel application of an established technique: applying subthreshold electrical microstimulation at specific times during the memory period of the gaze perturbation task, and then testing for enduring changes in remembered information.  By separately stimulating sites within PPC, FEF, and DLPFC while subjects maintain and update spatial memories, we will establish whether a causal link exists between short-term spatial memory and local neuronal activity in these areas.  To compare the impact of nonvisual signals in these areas, we will quantify the effects of stimulation on spatial memory during vestibular and oculomotor gaze changes.  We hypothesize that gaze signals are incorporated into short-term spatial memories in PPC and that updating in FEF and DLPFC merely reflect processing that occurs in the parietal lobe.  We predict that microstimulation will have greater effects in PPC when animals remember world-fixed targets compared to subject-fixed targets.  Based on the previous data, we predict that microstimulation in PPC during slow gaze perturbations will have less effect on spatial memory than saccadic perturbations.  In contrast, we predict that the effects of microstimulation in FEF and DLPFC will not depend on whether a target is world-fixed or subject-fixed.  However, if either frontal region actively contributes in situations where the PPC map is inadequate, we predict that under those circumstances microstimulation in the frontal areas would have greater effect for world-fixed than subject-fixed targets. 

Click here to download the powerpoint poster of this project.