Corollary discharge and spatial updating: When the brain is split, is space still unified?

Carol L. Colby, Rebecca A. Berman, Laura Heiser, Richard C. Saunders

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

How does the brain keep track of salient locations in the visual world when the eyes move? In parietal, frontal and extrastriate cortex, and in the superior colliculus, neurons update or 'remap' stimulus representations in conjunction with eye movements. This updating reflects a transfer of visual information, from neurons that encode a salient location before the saccade, to neurons that encode the location after the saccade. Copies of the oculomotor command - corollary discharge signals - must initiate this transfer. We investigated the circuitry that supports spacial updating in the primate brain. Our central hypothesis was that the forebrain commissures provide the primary route for remapping spatial locations across visual hemifields, from one cortical hemisphere to the other. Further, we hypothesized that these commissures provide the primary route for communicating corollary discharge signals from one hemisphere to the other. We tested these hypotheses using the double-step task and subsequent physiological recording in two split-brain monkeys. In the double-step task, monkeys made sequential saccades to two briefly presented targets, T1 and T2. In the visual version of the task, the representation of T2 was updated either within the same hemifield ("visual-within"), or across hemifields ("visual-across"). In the motor version, updating of the visual stimulus was always within-hemifield. The corollary discharge signal that initiated the updating, however, was generated either within the same hemisphere ("motor- within") or in the opposite hemisphere ("motor-across"). We expected that, in the absence of the forebrain commissures, both visual-across and motor-across conditions would be impaired relative to their "within" controls. In behavioral experiments, we observed striking initial impairments in the monkeys' ability to update stimuli across visual hemifields. Surprisingly, however, both animals were ultimately capable of performing the visual-across sequences of the double-step task. In subsequent physiological experiments, we found that neurons in lateral intraparietal cortex (LIP) can remap stimuli across visual hemifields, albeit with a reduction in the strength of remapping activity. These behavioral and neural findings indicate that the transfer of visual information is compromised, but by no means abolished, in the absence of the forebrain commissures. We found minimal evidence of impairment of the motor-across condition. Both monkeys readily performed the motor-across sequences of the double-step task, and LIP neurons were robustly active when within-hemifield updating was initiated by a saccade into the opposite hemifield. These results indicate that corollary discharge signals are available bilaterally. Altogether, our findings show that both visual and corollary discharge signals from opposite hemispheres can converge to update spatial representations in the absence of the forebrain commissures. These investigations provide new evidence that a unified and stable representation of visual space is supported by a redundant circuit, comprised of cortical as well as subcortical pathways, with a remarkable capacity for reorganization.

Original languageEnglish (US)
Pages (from-to)187-205
Number of pages19
JournalProgress in Brain Research
Volume149
DOIs
StatePublished - 2005
Externally publishedYes

Fingerprint

Saccades
Haplorhini
Neurons
Brain
Split-Brain Procedure
Parietal Lobe
Superior Colliculi
Frontal Lobe
Visual Cortex
Eye Movements
Primates
Telencephalic Commissures

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Corollary discharge and spatial updating : When the brain is split, is space still unified? / Colby, Carol L.; Berman, Rebecca A.; Heiser, Laura; Saunders, Richard C.

In: Progress in Brain Research, Vol. 149, 2005, p. 187-205.

Research output: Contribution to journalArticle

Colby, Carol L. ; Berman, Rebecca A. ; Heiser, Laura ; Saunders, Richard C. / Corollary discharge and spatial updating : When the brain is split, is space still unified?. In: Progress in Brain Research. 2005 ; Vol. 149. pp. 187-205.
@article{f57eb2db0d5747bd96447d6d718aa7be,
title = "Corollary discharge and spatial updating: When the brain is split, is space still unified?",
abstract = "How does the brain keep track of salient locations in the visual world when the eyes move? In parietal, frontal and extrastriate cortex, and in the superior colliculus, neurons update or 'remap' stimulus representations in conjunction with eye movements. This updating reflects a transfer of visual information, from neurons that encode a salient location before the saccade, to neurons that encode the location after the saccade. Copies of the oculomotor command - corollary discharge signals - must initiate this transfer. We investigated the circuitry that supports spacial updating in the primate brain. Our central hypothesis was that the forebrain commissures provide the primary route for remapping spatial locations across visual hemifields, from one cortical hemisphere to the other. Further, we hypothesized that these commissures provide the primary route for communicating corollary discharge signals from one hemisphere to the other. We tested these hypotheses using the double-step task and subsequent physiological recording in two split-brain monkeys. In the double-step task, monkeys made sequential saccades to two briefly presented targets, T1 and T2. In the visual version of the task, the representation of T2 was updated either within the same hemifield ({"}visual-within{"}), or across hemifields ({"}visual-across{"}). In the motor version, updating of the visual stimulus was always within-hemifield. The corollary discharge signal that initiated the updating, however, was generated either within the same hemisphere ({"}motor- within{"}) or in the opposite hemisphere ({"}motor-across{"}). We expected that, in the absence of the forebrain commissures, both visual-across and motor-across conditions would be impaired relative to their {"}within{"} controls. In behavioral experiments, we observed striking initial impairments in the monkeys' ability to update stimuli across visual hemifields. Surprisingly, however, both animals were ultimately capable of performing the visual-across sequences of the double-step task. In subsequent physiological experiments, we found that neurons in lateral intraparietal cortex (LIP) can remap stimuli across visual hemifields, albeit with a reduction in the strength of remapping activity. These behavioral and neural findings indicate that the transfer of visual information is compromised, but by no means abolished, in the absence of the forebrain commissures. We found minimal evidence of impairment of the motor-across condition. Both monkeys readily performed the motor-across sequences of the double-step task, and LIP neurons were robustly active when within-hemifield updating was initiated by a saccade into the opposite hemifield. These results indicate that corollary discharge signals are available bilaterally. Altogether, our findings show that both visual and corollary discharge signals from opposite hemispheres can converge to update spatial representations in the absence of the forebrain commissures. These investigations provide new evidence that a unified and stable representation of visual space is supported by a redundant circuit, comprised of cortical as well as subcortical pathways, with a remarkable capacity for reorganization.",
author = "Colby, {Carol L.} and Berman, {Rebecca A.} and Laura Heiser and Saunders, {Richard C.}",
year = "2005",
doi = "10.1016/S0079-6123(05)49014-7",
language = "English (US)",
volume = "149",
pages = "187--205",
journal = "Progress in Brain Research",
issn = "0079-6123",
publisher = "Elsevier",

}

TY - JOUR

T1 - Corollary discharge and spatial updating

T2 - When the brain is split, is space still unified?

AU - Colby, Carol L.

AU - Berman, Rebecca A.

AU - Heiser, Laura

AU - Saunders, Richard C.

PY - 2005

Y1 - 2005

N2 - How does the brain keep track of salient locations in the visual world when the eyes move? In parietal, frontal and extrastriate cortex, and in the superior colliculus, neurons update or 'remap' stimulus representations in conjunction with eye movements. This updating reflects a transfer of visual information, from neurons that encode a salient location before the saccade, to neurons that encode the location after the saccade. Copies of the oculomotor command - corollary discharge signals - must initiate this transfer. We investigated the circuitry that supports spacial updating in the primate brain. Our central hypothesis was that the forebrain commissures provide the primary route for remapping spatial locations across visual hemifields, from one cortical hemisphere to the other. Further, we hypothesized that these commissures provide the primary route for communicating corollary discharge signals from one hemisphere to the other. We tested these hypotheses using the double-step task and subsequent physiological recording in two split-brain monkeys. In the double-step task, monkeys made sequential saccades to two briefly presented targets, T1 and T2. In the visual version of the task, the representation of T2 was updated either within the same hemifield ("visual-within"), or across hemifields ("visual-across"). In the motor version, updating of the visual stimulus was always within-hemifield. The corollary discharge signal that initiated the updating, however, was generated either within the same hemisphere ("motor- within") or in the opposite hemisphere ("motor-across"). We expected that, in the absence of the forebrain commissures, both visual-across and motor-across conditions would be impaired relative to their "within" controls. In behavioral experiments, we observed striking initial impairments in the monkeys' ability to update stimuli across visual hemifields. Surprisingly, however, both animals were ultimately capable of performing the visual-across sequences of the double-step task. In subsequent physiological experiments, we found that neurons in lateral intraparietal cortex (LIP) can remap stimuli across visual hemifields, albeit with a reduction in the strength of remapping activity. These behavioral and neural findings indicate that the transfer of visual information is compromised, but by no means abolished, in the absence of the forebrain commissures. We found minimal evidence of impairment of the motor-across condition. Both monkeys readily performed the motor-across sequences of the double-step task, and LIP neurons were robustly active when within-hemifield updating was initiated by a saccade into the opposite hemifield. These results indicate that corollary discharge signals are available bilaterally. Altogether, our findings show that both visual and corollary discharge signals from opposite hemispheres can converge to update spatial representations in the absence of the forebrain commissures. These investigations provide new evidence that a unified and stable representation of visual space is supported by a redundant circuit, comprised of cortical as well as subcortical pathways, with a remarkable capacity for reorganization.

AB - How does the brain keep track of salient locations in the visual world when the eyes move? In parietal, frontal and extrastriate cortex, and in the superior colliculus, neurons update or 'remap' stimulus representations in conjunction with eye movements. This updating reflects a transfer of visual information, from neurons that encode a salient location before the saccade, to neurons that encode the location after the saccade. Copies of the oculomotor command - corollary discharge signals - must initiate this transfer. We investigated the circuitry that supports spacial updating in the primate brain. Our central hypothesis was that the forebrain commissures provide the primary route for remapping spatial locations across visual hemifields, from one cortical hemisphere to the other. Further, we hypothesized that these commissures provide the primary route for communicating corollary discharge signals from one hemisphere to the other. We tested these hypotheses using the double-step task and subsequent physiological recording in two split-brain monkeys. In the double-step task, monkeys made sequential saccades to two briefly presented targets, T1 and T2. In the visual version of the task, the representation of T2 was updated either within the same hemifield ("visual-within"), or across hemifields ("visual-across"). In the motor version, updating of the visual stimulus was always within-hemifield. The corollary discharge signal that initiated the updating, however, was generated either within the same hemisphere ("motor- within") or in the opposite hemisphere ("motor-across"). We expected that, in the absence of the forebrain commissures, both visual-across and motor-across conditions would be impaired relative to their "within" controls. In behavioral experiments, we observed striking initial impairments in the monkeys' ability to update stimuli across visual hemifields. Surprisingly, however, both animals were ultimately capable of performing the visual-across sequences of the double-step task. In subsequent physiological experiments, we found that neurons in lateral intraparietal cortex (LIP) can remap stimuli across visual hemifields, albeit with a reduction in the strength of remapping activity. These behavioral and neural findings indicate that the transfer of visual information is compromised, but by no means abolished, in the absence of the forebrain commissures. We found minimal evidence of impairment of the motor-across condition. Both monkeys readily performed the motor-across sequences of the double-step task, and LIP neurons were robustly active when within-hemifield updating was initiated by a saccade into the opposite hemifield. These results indicate that corollary discharge signals are available bilaterally. Altogether, our findings show that both visual and corollary discharge signals from opposite hemispheres can converge to update spatial representations in the absence of the forebrain commissures. These investigations provide new evidence that a unified and stable representation of visual space is supported by a redundant circuit, comprised of cortical as well as subcortical pathways, with a remarkable capacity for reorganization.

UR - http://www.scopus.com/inward/record.url?scp=26844580946&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=26844580946&partnerID=8YFLogxK

U2 - 10.1016/S0079-6123(05)49014-7

DO - 10.1016/S0079-6123(05)49014-7

M3 - Article

C2 - 16226585

AN - SCOPUS:26844580946

VL - 149

SP - 187

EP - 205

JO - Progress in Brain Research

JF - Progress in Brain Research

SN - 0079-6123

ER -