Elsevier

Cortex

Volume 44, Issue 8, September 2008, Pages 914-927
Cortex

Special issue: Original article
Classical disconnection studies of the corpus callosum

https://doi.org/10.1016/j.cortex.2008.04.001Get rights and content

Abstract

The corpus callosum is one of the most prominent fiber systems of the mammalian brain. Early reports of animals in which the callosum was cut, often confused the effects attributable to callosum damage with those caused by lesions of other brain structures. Early clinical reports also failed to establish the role of the callosum in humans. Two sorts of evidence began to reveal the functions of the corpus callosum. People with callosal damage cannot read text presented in the left visual field, and animals in which the callosum is divided, and sensory input restricted to one hemisphere, fail to show interhemispheric transfer of learning. These functional findings are consistent with anatomical and physiological studies of the role of the corpus callosum in communication between the hemispheres.

Section snippets

The early history

The corpus callosum is an obvious subdivision of the mammalian brain. When scientific interest shifted from ventricular localization to the substance of brain, the distinction between grey and white matter, and the unique position of the corpus callosum between the two hemispheres were clearly described.

Vesalius wrote:

“It comes into view of those dissecting when they manually separate the right side of the brain slightly from the left, for with the brain so separated, that which unites its

Behavioral study of inter-hemispheric transfer

In the first half of the 20th century there was an increasing interest in the laboratory study of learning and its mechanisms. Two different experimental approaches were used. One was classical conditioning as used by Pavlov and his students (Pavlov, 1927). The other approach, common in American laboratories, was to train animals to perform a voluntary task such as running a maze or selecting one of two visual targets. Both methods were to lead towards a deeper understanding of the functions of

Influence of the animal studies on neurosurgical practice and neuropsychology

Some years before these animal experiments were done, Van Wagenen and Herren (1940) reported on a series of cases in which they had cut the corpus callosum in patients in an attempt to limit the spread of epilepsy. They found that section of the corpus callosum was most effective in limiting the spread of the epileptic discharge in those cases in which the source of the epilepsy was due to a large cortical or subcortical scar. The patients were studied extensively by Akelaitis (1941) but they

Other advances in understanding stimulated by the Sperry discoveries

Another of Lashley's students, Chow (1951), and later Pribram and Mishkin (1955) demonstrated that lesions of the inferotemporal cortex produce deficits in acquisition and retention of visual discrimination learning. Mishkin used the callosum studies as a basis for establishing the fact that the linkage between primary visual cortex and the inferotemporal areas is by way of cortico-cortical circuits. When he made a large inferotemporal lesion on one side of the brain, and a visual cortical

Other routes linking the two hemispheres

Although detailed knowledge of the sensory properties of the two stimuli failed to transfer between the two hands in callosum-sectioned monkeys, the habit of testing the two objects before deciding which to choose did transfer from the hand first trained to the second hand. Earlier, Hartmann and Trendelenburg (1927) had shown that there is high level coordination between the hands in a callosum-sectioned monkey, and KU Smith had found significant transfer between the hands in the patients that

Anatomical and physiological studies of callosal connections

Strychnine and the corpus callosum. Convulsant effects from the systemic administration of strychnine had been scientifically described since the early 19th century by Magendie (Simon, 1999). Baglioni and Magnini (1909), working in Luciani's laboratory in Rome, discovered that strychnine directly applied to neurons of the motor cortex of dogs caused spontaneous contractions of the corresponding muscles of the opposite side, as well as a reduction in the threshold for the motor response to local

The primary visual cortex and the corpus callosum

In primates the primary visual cortex (area V1 or calcarine cortex) receives the great majority of the projections from the main thalamic nucleus of the optic pathways, the lateral geniculate nucleus. V1 coincides with Brodmann's cytoarchitectonic area 17 and is also called area striata because the prominent stria of Gennari unmistakably distinguishes it from the adjacent area V2. The apparent absence of commissural connections in area V1 borne out by strychnine neuronography was in agreement

First attempts to correlate callosal electrophysiology and callosal behavioral transfers: Frédéric Bremer

The Belgian physiologist and pathologist Frédéric Bremer (Fig. 9) is mostly known for his studies on the neural bases of the sleep-wake cycle, based on his famous preparations cerveau and encéphale isolé. By contrast, his important contributions to the understanding the functional significance of the corpus callosum with an electrophysiological approach are almost forgotten, in spite of the fact that he wrote three authoritative reviews on the subject (Bremer et al., 1956, Bremer, 1958, Bremer,

Electrophysiological transmission of visual inputs by the corpus callosum

One of the main scientific interests of the British physiologist David Whitteridge was the pattern of representation of the visual field in the cortex. Like Bremer he approached the functions of the corpus callosum electrophysiologically but aiming at the single neuron level. In 1965 he published with Choudhury and Wilson a pioneering experiment on the function of the callosal connections of the visual cortex, in which they cut the left optic tract in cats and recorded from single visual

Conclusion

In this paper we have presented a selective history of studies on the corpus callosum as seen mainly from an anatomo-behavioral and physiological perspective. We have described how the first attempts to identify a pattern of deficits specific to section of the corpus callosum in experimental animals were inconclusive either due to the prevalence of symptoms caused by unintentional lesions of non-callosal brain structures, or because of the use of behavioral methods inappropriate to reveal the

Uncited references

Bremer and Stoupel, 1957, Engel et al., 1991, Kanne and Finger, 1999, Pavlov, 1927.

Acknowledgements

We thank Marco Veronese (Department of Neural and Visual Sciences, University of Verona) for preparing the illustrations.

References (99)

  • K.M. Heilman et al.

    The disconnection apraxias

    Cortex

    (2008)
  • D.K. Jones

    Studying connections in the living human brain with diffusion MRI

    Cortex

    (2008)
  • H. Kennedy et al.

    Functional implications of the anatomical organization of the callosal projections of visual areas V1 and V2 in the macaque monkey

    Behavioural Brain Research

    (1988)
  • M.G. Knyazeva et al.

    EEG coherence studies in the normal brain and after early-onset cortical pathologies

    Brain Research Brain Research Reviews

    (2001)
  • W. McCulloch

    Mechanisms for the spread of epileptic activation of the brain

    Electroencephalography and Clinical Neurophysiology

    (1949)
  • A. Rosina et al.

    Pontocerebellar system linking the two hemispheres by intracerebellar branching

    Brain Research

    (1984)
  • J. Schmahmann et al.

    Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems

    Cortex

    (2008)
  • K. Shoumura et al.

    Structural organization of the “callosal” OBg in human corpus callosum agenesis

    Brain Research

    (1975)
  • J. Simon

    Naming and toxicity: a history of strychnine

    Studies in History and Philosophy of Biological and Biomedical Sciences

    (1999)
  • N. Sloan et al.

    The identity of spreading depression and “suppression”

    Electroencephalography and Clinical Neurophysiology

    (1950)
  • W.B. Spatz et al.

    Area 17 of anthropoid primates does participate in visual callosal connections

    Neuroscience Letters

    (1984)
  • M. Thiebaut de Schotten et al.

    Visualization of disconnection syndromes in humans

    Cortex

    (2008)
  • S.M. Zeki

    Interhemispheric connections of prestriate cortex in monkey

    Brain Research

    (1970)
  • P.L. Abel et al.

    Organization of callosal linkages in visual area V2 of macaque monkey

    Journal of Comparative Neurology

    (2000)
  • A.J. Akelaitis

    Studies on the corpus callosum II. The higher visual functios in each homonymous field following complete section of the corpus callosum

    Archives of Neurology and Psychiatry

    (1941)
  • G.V. Anrep

    The irradiation of conditioned reflexes

    Proceedings of the Royal Society of London, Series B

    (1923)
  • S. Baglioni et al.

    Azione di alcune sostanze chimiche sulle zone eccitabili della corteccia cerebrale del cane

    Archivio di Fisiologia

    (1909)
  • P. Bailey et al.

    Cortical origin and distribution of corpus callosum and anterior commissure in chimpanzee (Pan satyrus)

    Journal of Neurophysiology

    (1941)
  • P. Bailey et al.

    Functional organization of temporal lobe of monkey (Macaca mulatta) and chimpanzee (Pan satyrus)

    Journal of Neurophysiology

    (1943)
  • C.E. Beevor

    On the course of the fibres of the cingulum and the posterior part of the corpus callosum and fornix in the marmoset monkey

    Philosophical Transactions of the Royal Society B: Biological Sciences

    (1891)
  • G. Berlucchi

    Commissurotomy studies in animals

  • G. Berlucchi

    The midline fusion hypothesis is all right but cannot explain all callosal functions

  • G. Berlucchi et al.

    Microelectrode analysis of transfer of visual information by the corpus callosum

    Archives italiennes de Biologie

    (1967)
  • G. Berlucchi et al.

    Binoculary driven neurons in visual cortex of split chiasm cats

    Science

    (1968)
  • J.E. Bogen et al.

    Cerebral commissurotomy in man. Preliminary case report

    Bulletin of the Los Angeles Neurological Society

    (1962)
  • J.E. Bogen et al.

    Treatment of generalized seizure by cerebral commissurotomy

    Surgical Forum

    (1963)
  • F. Bremer

    Un aspect de la physiologie du corps calleux

    Archives internationales de Physiologie

    (1953)
  • F. Bremer

    Physiology of the corpus callosum

    Research Publications of the Association for Research on Nervous and Mental Diseases

    (1958)
  • F. Bremer

    Le corps calleux dans la dynamique cérébrale

    Experientia

    (1966)
  • F. Bremer

    Étude electrophysiologique d'un transfert interhémisphérique callosal

    Archives Italiennes de Biologie

    (1966)
  • F. Bremer et al.

    Physiologie et pathologie du corps calleux

    Schweizer Archiv für Neurologie und Psychiatrie

    (1956)
  • F. Bremer et al.

    Transmission interhémisphérique des influx visuels par le corps calleux

    Journal de Physiologie (Paris)

    (1956)
  • F. Bremer et al.

    Étude de mécanismes de la synergie bioélectrique des hémisphères cerebraux

    Acta Physiologica et Pharmacologica Neerlandica

    (1957)
  • F. Bremer et al.

    Transfert interhémisphérique d'informations sensoriels par le corps calleux

    Journal de Physiologie (Paris)

    (1955)
  • Bykov KM and Speranskii AD. (Russian); “Dog with a cut corpus callosum” Trud. fiziol. labor. I.P.Pavlov. Proceedings of...
  • M. Catani et al.

    The rises and falls of disconnection syndromes

    Brain

    (2005)
  • B.P. Choudhury et al.

    The function of the callosal connections of the visual cortex

    Quarterly Journal of Experimental Physiology

    (1965)
  • K.L. Chow

    Effects of partial extirpations of the posterior association cortex on visually mediated behavior

    Comparative Psychology Monograph

    (1951)
  • E. Claes

    Contribution a l'étude physiologique de la fonction visuelle. I. Analyse oscillographique de l'activité spontanée et sensorielle de l'aire visuelle coticale chez le chat non anesthesia

    Archives internationales de Physiologie

    (1939)
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