From Phineas Gage and Monsieur Leborgne to H.M.: Revisiting Disconnection Syndromes.

M Thiebaut De Schotten,P Ratiu,F Dell'Acqua,A Simmons,H Howells,M T Iba-Zizen,E Cabanis,O Plaisant,S Corkin,N F Dronkers,A Leslie,M Catani

doi:10.1093/cercor/bhv173

Abstract

On the 50th anniversary of Norman Geschwind's seminal paper entitled ‘Disconnexion syndrome in animal and man’, we pay tribute to his ideas by applying contemporary tractography methods to understand white matter disconnection in 3 classic cases that made history in behavioral neurology. We first documented the locus and extent of the brain lesion from the computerized tomography of Phineas Gage's skull and the magnetic resonance images of Louis Victor Leborgne's brain, Broca's first patient, and Henry Gustave Molaison. We then applied the reconstructed lesions to an atlas of white matter connections obtained from diffusion tractography of 129 healthy adults. Our results showed that in all 3 patients, disruption extended to connections projecting to areas distant from the lesion. We confirmed that the damaged tracts link areas that in contemporary neuroscience are considered functionally engaged for tasks related to emotion and decision-making (Gage), language production (Leborgne), and declarative memory (Molaison). Our findings suggest that even historic cases should be reappraised within a disconnection framework whose principles were plainly established by the associationist schools in the last 2 centuries.

Highlights

Much of our knowledge about higher cognitive functions and complex behaviors derives from the description of historic seminal cases that helped shape neuroscience (Finger 1994; Compston 2009, 2011a,b, 2014)
These cases reinforced localizationist ideas of cognitive functions related to the activity of discrete and fairly localized brain regions (Catani, Dell’acqua, Bizzi et al 2012), including the association of social behavior with orbitofrontal cortex (Harlow 1868; Damasio et al 1994), speech production with Broca’s area (Broca 1861a,b), and declarative memory with medial temporal lobe structures (Scoville and Milner 1957)
Modern neuroimaging has shown that many complex functions rely on the coordinated activity of distant regions connected by long-range fibers coursing through the cerebral white matter

Summary

Introduction

Much of our knowledge about higher cognitive functions and complex behaviors derives from the description of historic seminal cases that helped shape neuroscience (Finger 1994; Compston 2009, 2011a,b, 2014). These cases reinforced localizationist ideas of cognitive functions related to the activity of discrete and fairly localized brain regions (Catani, Dell’acqua, Bizzi et al 2012), including the association of social behavior with orbitofrontal cortex (Harlow 1868; Damasio et al 1994), speech production with Broca’s area (Broca 1861a,b), and declarative memory with medial temporal lobe structures (Scoville and Milner 1957). Detailed cortical parcellation and localization became the only way to understanding cognitive functions (Von Economo and Koskinas 1925; Vogt and Vogt 1926)

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Conclusion