Active Vision: Memory, Attention and Spatial Representation in Parietal Cortex Carol Colby Rebecca Berman Cathy Dunn Chris Genovese Laura Heiser Eli Merriam Kae Nakamura Richard Saunders Department of Neuroscience Center for the Neural Basis of Cognition University of Pittsburgh Department of Statistics Carnegie Mellon University Laboratory of Neuropsychology,NIMH

1) Remapping in monkey area LIP and extrastriate visual cortex 2) Remapping in split-brain monkeys Behavior Physiology 3) Remapping in human cortex

LIP memory guided saccade Stimulus OnSaccade

Stimulus appears outside of RF Saccade moves RF to stimulus location

Single step task

Spatial updating or remapping The brain combines visual and corollary discharge signals to create a representation of space that takes our eye movements into account

LIP Summary Area LIP neurons encode attended spatial locations. The spatial representation of an attended location is remapped when the eyes move. Remapping is initiated by a corollary discharge of the eye movement command. Remapping produces a representation that is oculocentric: a location is represented in the coordinates of the movement needed to acquire the location. Remapping allows humans and monkeys to perform a spatial memory task accurately.

Extrastriate Summary Remapping occurs at early stages of the visual hierarchy. Corollary discharge has an impact far back into the system. Remapping implies widespread connectivity in which many neurons have rapid access to information well beyond the classical receptive field. Vision is an active process of building representations.

1) Remapping in monkey area LIP and extrastriate visual cortex 2) Remapping in split-brain monkeys Behavior Physiology 3) Remapping in human cortex

Stimulus appears outside of RF Saccade moves RF to stimulus location

What is the brain circuit that produces remapping?

The obvious pathway: forebrain commissures (FC)

Are the forebrain commissures necessary for updating visual signals across the vertical meridian? Behavior in double step task Physiology in single step and double step task

Attain fixation FP T1 appears FP T1 T2 flashes briefly T1 T2 FP Saccade to T1 T1 Saccade to T2 T2

Attain fixation FP T1 appears FP T1 T2 flashes T1 T2 FP

WITHIN T1 T2 Transfer of visual signals

T2 WITHIN T1 T2 T2’

VISUAL-ACROSS T2 T1 T2 WITHIN T1 T2 T2’

VISUAL-ACROSS T2 T1 T2 T2’ WITHIN T1 T2 T2’

WITHIN T1 T2 Is performance impaired on visual-across sequences in split-brain monkeys? VISUAL-ACROSS T2 T1 T2 T2’T2T2’

Central AcrossWithin Central WithinAcross

Day 1: Initial impairment for visual-across WithinAcrossCentralWithinAcrossCentral Monkey C Monkey E correct incorrect

TRIALS 1-10 WithinCentralAcrossWithinCentralAcross

Horizontal eye position (degrees) Vertical eye position (degrees) Monkey C First day saccade endpoints Monkey E

Horizontal eye position (degrees) Vertical eye position (degrees) Monkey E Monkey C Last day saccade endpoints Monkey E

WithinAcross Central WithinAcross Central Learning? Or a monkey trick?

no monkey tricks..

Monkey EMMonkey CH Both monkeys really update the visual representation

Are the forebrain commissures necessary for updating spatial information across the vertical meridian? No. The FC are the primary route but not the only route. What are LIP neurons doing?

Stimulus appears outside of RF Saccade moves RF to stimulus location

SINGLE STEP STIMULUS ALONE SACCADE ALONE

Population activity in area LIP

SINGLE STEP DOUBLE STEP

Split Brain Monkey Summary The forebrain commissures normally transmit remapped visual signals across the vertical meridian but they are not required. Single neurons in area LIP continue to encode remapped stimulus traces in split-brain animals.

1) Remapping in monkey area LIP and extrastriate visual cortex 2) Remapping in split-brain monkeys Behavior Physiology 3) Remapping in human cortex

Remapping in human cortex Task and predictions Parietal cortex Striate and extrastriate visual cortex Remapping in a split brain human

Functional Imaging Predictions 1) Robust activation in cortex ipsilateral to the stimulus. 2) Ipsilateral activation should be smaller than the contralateral visual response. 3) It should not be attributable to the stimulus alone or to the saccade alone. 4) Ipsilateral activation should occur around the time of the saccade.

Contralateral Visual Response (Fixation Task)

Ipsilateral Remapped Response

Visual and Remapped Responses

Human Parietal Imaging Summary Remapping in humans produces activity in parietal cortex ipsilateral to the visual stimulus. Remapped activity is lower amplitude than visual activity. The activity cannot be accounted for by the stimulus or the saccade alone. Remapped activity occurs in conjunction with the eye movement.

Remapping in human cortex Task and predictions Parietal cortex Striate and extrastriate visual cortex Remapping in a split brain human

Contralateral Visual Response

Ipsilateral Remapped Response

Remapping in Multiple Visual Areas

Magnitude of Remapped Response

Remapping in human cortex Task and predictions Parietal cortex Striate and extrastriate visual cortex Remapping in a split brain human

Intact Subjects Split Brain Subject

Parietal Responses in Split Brain and Intact Subjects

Human Imaging Summary Remapping in humans produces activity in the hemisphere ipsilateral to the stimulus.

Human Imaging Summary Remapping in humans produces activity in the hemisphere ipsilateral to the stimulus. Remapped activity is present in human parietal, extrastriate and striate cortex.

Human Imaging Summary Remapping in humans produces activity in the hemisphere ipsilateral to the stimulus. Remapped activity is present in human parietal, extrastriate and striate cortex. Remapped visual signals are more prevalent at higher levels of the visual system hierarchy.

Human Imaging Summary Remapping in humans produces activity in the hemisphere ipsilateral to the stimulus. Remapped activity is present in human parietal, extrastriate and striate cortex. Remapped visual signals are more prevalent at higher levels of the visual system hierarchy. Remapping occurs in parietal and visual cortex in a split brain human subject.

Conclusions Remapping of visual signals is widespread in monkey cortex.

Conclusions Remapping of visual signals is widespread in monkey cortex. Split-brain monkeys are able to remap visual signals across the vertical meridian.

Conclusions Remapping of visual signals is widespread in monkey cortex. Split-brain monkeys are able to remap visual signals across the vertical meridian. Remapped visual signals are present in area LIP in split-brain monkeys.

Conclusions Remapping of visual signals is widespread in monkey cortex. Split-brain monkeys are able to remap visual signals across the vertical meridian. Remapped visual signals are present in area LIP in split-brain monkeys. Remapped visual signals are robust in human parietal and visual cortex.

Conclusions Remapping of visual signals is widespread in monkey cortex. Split-brain monkeys are able to remap visual signals across the vertical meridian. Remapped visual signals are present in area LIP in split-brain monkeys. Remapped visual signals are robust in human parietal and visual cortex. In a split-brain human, remapped visual signals are present in parietal and visual cortex.

Conclusions Remapping of visual signals is widespread in monkey cortex. Split-brain monkeys are able to remap visual signals across the vertical meridian. Remapped visual signals are present in area LIP in split-brain monkeys. Remapped visual signals are robust in human parietal and visual cortex. In a split-brain human, remapped visual signals are present in parietal and visual cortex. Vision is an active process of building representations from sensory, cognitive and motor signals.