Perceptual unity in the split brain: the role of subcortical connections

Perceptual unity in the split brain: the role of subcortical connections Sir, In two recent articles, Pinto and colleagues (2017a, c) challenge the classic view that section of the forebrain commissures creates a division of consciousness, with each hemisphere operating as a distinct conscious entity. In an investigation focusing on visual perception in split-brained patients, they conclude that while perception is divided, consciousness is not. Volz and Gazzaniga (2017) reaffirm findings of divided consciousness in the split brain, and suggest a number of mechanisms whereby limited information might be transferred between hemispheres, noting evidence for attentional transfer (Holtzman et al., 1981) but emphasizing particularly the role of external cross-cueing. This is disputed in turn by Pinto et al. (2017b), but reiterated by Volz et al. (2018). Throughout this barrage there is only passing reference to the potential role of subcortical connections. Split-brained patients do not report any sense that the visual world is divided, and generally act with what Bogen (1993) described as ‘social ordinariness’ (p. 5). Where their visuospatial processing seems integrated, it may well be sustained by a subcortical system, sometimes called the ‘second visual system’ or the ‘ambient system’ (Trevarthen and Sperry, 1973), which courses through the superior colliculi, the pulvinar nuclei, and thence to the parietal lobes, bypassing the ‘focal’ geniculo-striate system, and is connected interhemispherically via the collicular commissure or other possible subcortical routes. The superior colliculi themselves play a role in implementing both saccadic and pursuit eye movements, and are also involved in the normal control of spatial attention during perceptual judgements (Krauzlis et al., 2013). In animals (including birds) with little or no cortical vision, vision is dependent on this system, and the corpus callosum itself is present only in placental mammals. Within the geniculo-striate system the two sides of space are integrated only at the cortical level, by the cerebral commissures. This system is specialized for perception of detail and the identification of objects, and is centred on foveal vision. Several lines of evidence suggest that the intact ambient system may be key to the sense of visuospatial unity in the split brain. For instance, Trevarthen and Sperry (1973) presented stimuli to split-brained patients in peripheral vision while they held fixation on a point. Two patients could easily tell whether two circles in opposite hemifields moved in the same direction (up or down) or in opposite directions. They could also describe the rhythm of movements, using terms such as ‘slow’, ‘fast’, ‘jerky’, and ‘bouncing about’ when the movements were in the left visual field, and therefore projected to the non-verbal right hemisphere. These results imply subcortical unification for motion perception. Interhemispheric integration is also necessary for the perception of apparent motion (‘phi motion’) across the vertical midline, which can be readily perceived by split-brained patients (Ramachandran et al., 1986). Gazzaniga (1987) suggested that the motion is inferred rather than perceived, but further study undermines this conclusion (Naikar and Corballis, 1996), although the perceived motion is less precise than in healthy controls (Forster et al., 2000). Split-brained patients can judge whether or not sloping lines in opposite hemifields are aligned (Sergent, 1987; Corballis and Trudel, 1993). Sergent (1987) also reported that a split-brained patient could readily judge whether or not an arrow in one hemifield pointed to a dot in the other, or whether the angle formed by lines in opposite hemifields is greater or less than 90°. Thus, line orientation and location are transferred subcortically, although again probably with less precision than in healthy controls. The patients can also respond to stimuli in either visual hemifield with the contralateral hand, implying interhemispheric transfer, although the estimated transfer time is longer than in controls (e.g. Berlucchi et al., 1995). It is delayed even further with short-wave visual stimuli (purple), undetectable by collicular neurons (Savazzi et al., 2007), implying a collicular role. Collicular input also contributes to ‘redundancy gain’—a lowering of reaction time when two stimuli are presented simultaneously in both hemifields rather than a single stimulus in just one. Redundancy gain is more pronounced in split-brained patients than in controls, but this added gain disappears when the stimuli are equiluminant with the background (Corballis, 1998) or shown in monochromatic purple (Savazzi and Marzi, 2004), again bypassing the collicular system. It also occurs when the cortical component is removed by hemi-spherectomy (Tomaiuolo et al., 1997), and in hemi-spherectomized patients it is enhanced when bilateral stimuli form a pattern, suggesting collicular sensitivity to gestalt-like properties (Georgy et al., 2016). These examples of interhemispheric integration, along with those reported by Pinto et al., are in stark contrast to the lack of ability of split-brained patients to judge whether pairs of letters, digits, colours, or faces presented in opposite hemifields are the same or different (Johnson, 1984; Corballis and Corballis, 2001). These judgements, though, require cortical analysis through the focal, geniculo-striate system. Although the collicular system appears to allow a unified sense of space and the perceptual integration of location, orientation, motion, and perhaps even pattern, it probably does so with less precision than in the focal system. Krauzlis et al. (2013) suggest that the expansion of the neocortex allowed for a proliferation of features for classifying objects and assigning meaning, but the ancient collicular system remains intact and functional for selecting the content of action or perception. The challenge by Pinto and colleagues reiterates the earlier one published in this journal by Sergent (1987), who drew the following conclusion from her data: ‘This subcortical coordination of hemisphere activity may thus underlie the behavioural integration displayed by commissurotomized patients in their daily activities, allowing them to relate different parts of the visual field and to maintain a unity of purpose in their action’ (p. 1389). A few of Sergent’s split-brain experiments were incorrectly interpreted but those cited here appear to have been valid, and indeed informative (for more detail, see Corballis, 2016). Funding C.A.M. is funded by ERC Grant 339939 ‘Perceptual Awareness,’ and M.C.C. was earlier funded by grant UOA2019 from the Marsden Fund of the Royal Society of New Zealand. References Berlucchi G, Aglioti S, Marzi CA, Tassinari G. Corpus callosum and simple visuomotor integration. Neuropsychologia  1995; 33: 923– 36. Google Scholar CrossRef Search ADS PubMed  Bogen JE. The callosal syndromes. In: Heilman KM, Valentein E, editors. Clinical neuropsychology , 3rd edn. Oxford: Oxford University Press; 1993. p. 337– 407. Corballis MC. Interhemispheric neural summation in the absence of the corpus callosum. Brain  1998; 121: 1795– 807. Google Scholar CrossRef Search ADS PubMed  Corballis MC. Revisiting sperry: what the split brain tells us. In: Kolb B, Whishaw I, editors. Brain and behaviour: revisiting the classic studies . London: Sage; 2016. p. 55– 66. Corballis MC, Corballis PM. Interhemispheric visual matching in the split brain. Neuropsychologia  2001; 39: 1395– 400. Google Scholar CrossRef Search ADS PubMed  Corballis MC, Trudel CI. The role of the forebrain commissures in interhemispheric integration. Neuropsychology  1993; 7: 306– 24. Google Scholar CrossRef Search ADS   Forster BA, Corballis PM, Corballis MC. Effect of luminance on successiveness discrimination in the absence of the corpus callosum. Neuropsychologia  2000; 38: 441– 50. Google Scholar CrossRef Search ADS PubMed  Gazzaniga MS. Perceptual and attentional processes following callosal section in humans. Neuropsychologia  1987; 25: 119– 33. Google Scholar CrossRef Search ADS PubMed  Georgy L, Celeghin A, Marzi CA, Tamietto M, Ptito A. The superior colliculus is sensitive to gestalt-like stimulus configuration in hemispherectomy patients. Cortex  2016; 81: 151– 61. Google Scholar CrossRef Search ADS PubMed  Holtzman JD, Sidtis JJ, Volpe BT, Wilson DH, Gazzaniga MS. Dissociation of spatial information for stimulus localization and the control of attention. Brain  1981; 104: 861– 72. Google Scholar CrossRef Search ADS PubMed  Johnson LE. Bilateral visual cross-integration by human forebrain commissurotomy subjects. Neuropsychologia  1984; 22: 167– 75. Google Scholar CrossRef Search ADS PubMed  Krauzlis RJ, Lovejoy LP, Zenon A. Superior colliculus and visual spatial attention. Ann Rev Neurosci  2013; 36: 165– 82. Google Scholar CrossRef Search ADS PubMed  Naikar N, Corballis MC. Perception of apparent motion across the retinal midline following commissurotomy. Neuropsychologia  1996; 34: 297– 309. Google Scholar CrossRef Search ADS PubMed  Pinto Y, de Haan EHF, Lamme VAF. The split-brain phenomenon revisited: a single conscious agent with split perception. Trends Cogn Sci  2017a; 21: 835– 51. Google Scholar CrossRef Search ADS   Pinto Y, Lamme VAF, de Haan EHF. Cross-cueing cannot explain unified control in split-brain patients. Brain  2017b; 140: e68. Google Scholar CrossRef Search ADS   Pinto Y, Neville DA, Otten M, Corballis PM, Lamme VAF, de Haan EHF, et al.   Split brain: divided perception but undivided consciousness. Brain  2017c; 140: 1231– 7. Google Scholar CrossRef Search ADS   Ramachandran V, Cronin-Golomb A, Myers JJ. Perception of apparent motion by commissurotomy patients. Nature  1986; 320: 358– 9. Google Scholar CrossRef Search ADS PubMed  Savazzi S, Fabri M, Rubboli G, Paggi A, Tassinari CA, Marzi CA. Interhemispheric transfer following callosotomy in humans: role of the superior colliculus. Neuropsychologia  2007; 45: 2417– 27. Google Scholar CrossRef Search ADS PubMed  Savazzi S, Marzi CA. The superior colliculus subserves interhemispheric neural summation in both normals and patients with a total section or agenesis of the corpus callosum. Neuropsychologia  2004; 42: 1608– 18. Google Scholar CrossRef Search ADS PubMed  Sergent J. A new look at the human split brain. Brain  1987; 110: 1375– 92. Google Scholar CrossRef Search ADS PubMed  Tomaiuolo F, Ptito M, Marzi CA, Paus T, Ptit A. Blindsight in hemispherectomized patients as revealed by spatial summation across the vertical meridian. Brain  1997; 120: 795– 803. Google Scholar CrossRef Search ADS PubMed  Trevarthen CT, Sperry RW. Perceptual unity of the ambient visual field in human commissurotomy patients. Brain  1973; 96: 547– 70. Google Scholar CrossRef Search ADS PubMed  Volz LJ, Gazzaniga MS. Interaction in isolation: 50 years of insights from split-brain research. Brain  2017; 140: 2051– 60. Google Scholar CrossRef Search ADS PubMed  Volz LJ, Hillyard SA, Miller MB, Gazzaniga MS. Unifying control over the body: consciousness and cross-cueing in split-brain patients. Brain  2018; 141: e15. Google Scholar CrossRef Search ADS   © The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Brain Oxford University Press

Perceptual unity in the split brain: the role of subcortical connections

Loading next page...
 
/lp/ou_press/perceptual-unity-in-the-split-brain-the-role-of-subcortical-GjmJHDBm99
Publisher
Oxford University Press
Copyright
© The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For permissions, please email: journals.permissions@oup.com
ISSN
0006-8950
eISSN
1460-2156
D.O.I.
10.1093/brain/awy085
Publisher site
See Article on Publisher Site

Abstract

Sir, In two recent articles, Pinto and colleagues (2017a, c) challenge the classic view that section of the forebrain commissures creates a division of consciousness, with each hemisphere operating as a distinct conscious entity. In an investigation focusing on visual perception in split-brained patients, they conclude that while perception is divided, consciousness is not. Volz and Gazzaniga (2017) reaffirm findings of divided consciousness in the split brain, and suggest a number of mechanisms whereby limited information might be transferred between hemispheres, noting evidence for attentional transfer (Holtzman et al., 1981) but emphasizing particularly the role of external cross-cueing. This is disputed in turn by Pinto et al. (2017b), but reiterated by Volz et al. (2018). Throughout this barrage there is only passing reference to the potential role of subcortical connections. Split-brained patients do not report any sense that the visual world is divided, and generally act with what Bogen (1993) described as ‘social ordinariness’ (p. 5). Where their visuospatial processing seems integrated, it may well be sustained by a subcortical system, sometimes called the ‘second visual system’ or the ‘ambient system’ (Trevarthen and Sperry, 1973), which courses through the superior colliculi, the pulvinar nuclei, and thence to the parietal lobes, bypassing the ‘focal’ geniculo-striate system, and is connected interhemispherically via the collicular commissure or other possible subcortical routes. The superior colliculi themselves play a role in implementing both saccadic and pursuit eye movements, and are also involved in the normal control of spatial attention during perceptual judgements (Krauzlis et al., 2013). In animals (including birds) with little or no cortical vision, vision is dependent on this system, and the corpus callosum itself is present only in placental mammals. Within the geniculo-striate system the two sides of space are integrated only at the cortical level, by the cerebral commissures. This system is specialized for perception of detail and the identification of objects, and is centred on foveal vision. Several lines of evidence suggest that the intact ambient system may be key to the sense of visuospatial unity in the split brain. For instance, Trevarthen and Sperry (1973) presented stimuli to split-brained patients in peripheral vision while they held fixation on a point. Two patients could easily tell whether two circles in opposite hemifields moved in the same direction (up or down) or in opposite directions. They could also describe the rhythm of movements, using terms such as ‘slow’, ‘fast’, ‘jerky’, and ‘bouncing about’ when the movements were in the left visual field, and therefore projected to the non-verbal right hemisphere. These results imply subcortical unification for motion perception. Interhemispheric integration is also necessary for the perception of apparent motion (‘phi motion’) across the vertical midline, which can be readily perceived by split-brained patients (Ramachandran et al., 1986). Gazzaniga (1987) suggested that the motion is inferred rather than perceived, but further study undermines this conclusion (Naikar and Corballis, 1996), although the perceived motion is less precise than in healthy controls (Forster et al., 2000). Split-brained patients can judge whether or not sloping lines in opposite hemifields are aligned (Sergent, 1987; Corballis and Trudel, 1993). Sergent (1987) also reported that a split-brained patient could readily judge whether or not an arrow in one hemifield pointed to a dot in the other, or whether the angle formed by lines in opposite hemifields is greater or less than 90°. Thus, line orientation and location are transferred subcortically, although again probably with less precision than in healthy controls. The patients can also respond to stimuli in either visual hemifield with the contralateral hand, implying interhemispheric transfer, although the estimated transfer time is longer than in controls (e.g. Berlucchi et al., 1995). It is delayed even further with short-wave visual stimuli (purple), undetectable by collicular neurons (Savazzi et al., 2007), implying a collicular role. Collicular input also contributes to ‘redundancy gain’—a lowering of reaction time when two stimuli are presented simultaneously in both hemifields rather than a single stimulus in just one. Redundancy gain is more pronounced in split-brained patients than in controls, but this added gain disappears when the stimuli are equiluminant with the background (Corballis, 1998) or shown in monochromatic purple (Savazzi and Marzi, 2004), again bypassing the collicular system. It also occurs when the cortical component is removed by hemi-spherectomy (Tomaiuolo et al., 1997), and in hemi-spherectomized patients it is enhanced when bilateral stimuli form a pattern, suggesting collicular sensitivity to gestalt-like properties (Georgy et al., 2016). These examples of interhemispheric integration, along with those reported by Pinto et al., are in stark contrast to the lack of ability of split-brained patients to judge whether pairs of letters, digits, colours, or faces presented in opposite hemifields are the same or different (Johnson, 1984; Corballis and Corballis, 2001). These judgements, though, require cortical analysis through the focal, geniculo-striate system. Although the collicular system appears to allow a unified sense of space and the perceptual integration of location, orientation, motion, and perhaps even pattern, it probably does so with less precision than in the focal system. Krauzlis et al. (2013) suggest that the expansion of the neocortex allowed for a proliferation of features for classifying objects and assigning meaning, but the ancient collicular system remains intact and functional for selecting the content of action or perception. The challenge by Pinto and colleagues reiterates the earlier one published in this journal by Sergent (1987), who drew the following conclusion from her data: ‘This subcortical coordination of hemisphere activity may thus underlie the behavioural integration displayed by commissurotomized patients in their daily activities, allowing them to relate different parts of the visual field and to maintain a unity of purpose in their action’ (p. 1389). A few of Sergent’s split-brain experiments were incorrectly interpreted but those cited here appear to have been valid, and indeed informative (for more detail, see Corballis, 2016). Funding C.A.M. is funded by ERC Grant 339939 ‘Perceptual Awareness,’ and M.C.C. was earlier funded by grant UOA2019 from the Marsden Fund of the Royal Society of New Zealand. References Berlucchi G, Aglioti S, Marzi CA, Tassinari G. Corpus callosum and simple visuomotor integration. Neuropsychologia  1995; 33: 923– 36. Google Scholar CrossRef Search ADS PubMed  Bogen JE. The callosal syndromes. In: Heilman KM, Valentein E, editors. Clinical neuropsychology , 3rd edn. Oxford: Oxford University Press; 1993. p. 337– 407. Corballis MC. Interhemispheric neural summation in the absence of the corpus callosum. Brain  1998; 121: 1795– 807. Google Scholar CrossRef Search ADS PubMed  Corballis MC. Revisiting sperry: what the split brain tells us. In: Kolb B, Whishaw I, editors. Brain and behaviour: revisiting the classic studies . London: Sage; 2016. p. 55– 66. Corballis MC, Corballis PM. Interhemispheric visual matching in the split brain. Neuropsychologia  2001; 39: 1395– 400. Google Scholar CrossRef Search ADS PubMed  Corballis MC, Trudel CI. The role of the forebrain commissures in interhemispheric integration. Neuropsychology  1993; 7: 306– 24. Google Scholar CrossRef Search ADS   Forster BA, Corballis PM, Corballis MC. Effect of luminance on successiveness discrimination in the absence of the corpus callosum. Neuropsychologia  2000; 38: 441– 50. Google Scholar CrossRef Search ADS PubMed  Gazzaniga MS. Perceptual and attentional processes following callosal section in humans. Neuropsychologia  1987; 25: 119– 33. Google Scholar CrossRef Search ADS PubMed  Georgy L, Celeghin A, Marzi CA, Tamietto M, Ptito A. The superior colliculus is sensitive to gestalt-like stimulus configuration in hemispherectomy patients. Cortex  2016; 81: 151– 61. Google Scholar CrossRef Search ADS PubMed  Holtzman JD, Sidtis JJ, Volpe BT, Wilson DH, Gazzaniga MS. Dissociation of spatial information for stimulus localization and the control of attention. Brain  1981; 104: 861– 72. Google Scholar CrossRef Search ADS PubMed  Johnson LE. Bilateral visual cross-integration by human forebrain commissurotomy subjects. Neuropsychologia  1984; 22: 167– 75. Google Scholar CrossRef Search ADS PubMed  Krauzlis RJ, Lovejoy LP, Zenon A. Superior colliculus and visual spatial attention. Ann Rev Neurosci  2013; 36: 165– 82. Google Scholar CrossRef Search ADS PubMed  Naikar N, Corballis MC. Perception of apparent motion across the retinal midline following commissurotomy. Neuropsychologia  1996; 34: 297– 309. Google Scholar CrossRef Search ADS PubMed  Pinto Y, de Haan EHF, Lamme VAF. The split-brain phenomenon revisited: a single conscious agent with split perception. Trends Cogn Sci  2017a; 21: 835– 51. Google Scholar CrossRef Search ADS   Pinto Y, Lamme VAF, de Haan EHF. Cross-cueing cannot explain unified control in split-brain patients. Brain  2017b; 140: e68. Google Scholar CrossRef Search ADS   Pinto Y, Neville DA, Otten M, Corballis PM, Lamme VAF, de Haan EHF, et al.   Split brain: divided perception but undivided consciousness. Brain  2017c; 140: 1231– 7. Google Scholar CrossRef Search ADS   Ramachandran V, Cronin-Golomb A, Myers JJ. Perception of apparent motion by commissurotomy patients. Nature  1986; 320: 358– 9. Google Scholar CrossRef Search ADS PubMed  Savazzi S, Fabri M, Rubboli G, Paggi A, Tassinari CA, Marzi CA. Interhemispheric transfer following callosotomy in humans: role of the superior colliculus. Neuropsychologia  2007; 45: 2417– 27. Google Scholar CrossRef Search ADS PubMed  Savazzi S, Marzi CA. The superior colliculus subserves interhemispheric neural summation in both normals and patients with a total section or agenesis of the corpus callosum. Neuropsychologia  2004; 42: 1608– 18. Google Scholar CrossRef Search ADS PubMed  Sergent J. A new look at the human split brain. Brain  1987; 110: 1375– 92. Google Scholar CrossRef Search ADS PubMed  Tomaiuolo F, Ptito M, Marzi CA, Paus T, Ptit A. Blindsight in hemispherectomized patients as revealed by spatial summation across the vertical meridian. Brain  1997; 120: 795– 803. Google Scholar CrossRef Search ADS PubMed  Trevarthen CT, Sperry RW. Perceptual unity of the ambient visual field in human commissurotomy patients. Brain  1973; 96: 547– 70. Google Scholar CrossRef Search ADS PubMed  Volz LJ, Gazzaniga MS. Interaction in isolation: 50 years of insights from split-brain research. Brain  2017; 140: 2051– 60. Google Scholar CrossRef Search ADS PubMed  Volz LJ, Hillyard SA, Miller MB, Gazzaniga MS. Unifying control over the body: consciousness and cross-cueing in split-brain patients. Brain  2018; 141: e15. Google Scholar CrossRef Search ADS   © The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

BrainOxford University Press

Published: Apr 2, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off