Beyond cortical localization in clinico-anatomical correlation

doi:10.1016/j.cortex.2012.07.001

Cortex

Volume 48, Issue 10, November–December 2012, Pages 1262-1287

https://doi.org/10.1016/j.cortex.2012.07.001 Get rights and content

Abstract

Last year was the 150th anniversary of Paul Broca's landmark case report on speech disorder that paved the way for subsequent studies of cortical localization of higher cognitive functions. However, many complex functions rely on the activity of distributed networks rather than single cortical areas. Hence, it is important to understand how brain regions are linked within large-scale networks and to map lesions onto connecting white matter tracts. To facilitate this network approach we provide a synopsis of classical neurological syndromes associated with frontal, parietal, occipital, temporal and limbic lesions. A review of tractography studies in a variety of neuropsychiatric disorders is also included. The synopsis is accompanied by a new atlas of the human white matter connections based on diffusion tensor tractography freely downloadable on http://www.natbrainlab.com. Clinicians can use the maps to accurately identify the tract affected by lesions visible on conventional CT or MRI. The atlas will also assist researchers to interpret their group analysis results. We hope that the synopsis and the atlas by allowing a precise localization of white matter lesions and associated symptoms will facilitate future work on the functional correlates of human neural networks as derived from the study of clinical populations. Our goal is to stimulate clinicians to develop a critical approach to clinico-anatomical correlative studies and broaden their view of clinical anatomy beyond the cortical surface in order to encompass the dysfunction related to connecting pathways.

Introduction

The clinico-anatomical correlation method celebrates 150 years since Paul Broca brought it to existence in his seminal publication (Broca, 1861; Cubelli and De Bastiani, 2011; Lorch, 2011). To this day the method is still based on the circular reasoning that allows brain function to be inferred by studying the correspondence between clinical manifestations and lesion location. The validity of the method depends on: (i) the theoretical constructs and hypotheses being tested (e.g., psychological models); (ii) the level of sophistication of the methodology used for the patient's clinical characterization, and (iii) the resolution of the brain mapping methods (Damasio and Damasio, 1989; Catani and ffytche, 2010). In what follows we consider the evolution of the clinical-anatomical correlation method from the work of the pioneers to more recent neuroimaging approaches based on magnetic resonance imaging. The first part of our contribution is an historical introduction to the origin of the method, the ebb and flow of its fortune and the theoretical constructs derived from its application to neurological patients. In the second part we highlight the advantages of recent MRI methods to improve lesion localization and propose an atlas approach to extend the clinico-anatomical correlation to disorders affecting white matter tracts. In the final section we present a synopsis of the main clinical manifestations associated with lobe and tract lesions as a useful reference to guide the clinical and neuropsychological assessment of patients presenting with lesions to specific tracts.

Section snippets

Cortical localizationism and the origin of the clinico-anatomical correlation method

In April 1861, Ernest Auburtin (Fig. 1) presented at the meeting of the Société d’Anthropologie de Paris the case of Monsieur Cullerier, a patient who had shot himself in the head and was admitted to Saint-Louis hospital with an open wound in his forehead. The man remained conscious and possessed normal speech, but his anterior brain was exposed and Auburtin had the audacity to apply a light pressure with a blade to the wounded man's frontal lobe:

[…] the frontal bone was completely removed. The

Holism and the abandonment of the clinico-anatomical correlation method

The clinico-anatomical approach based on a narrow cortical localizationism attracted criticism since its beginning. In England John Hughlings Jackson was one of the first to point out that localization of symptoms does not necessarily imply localization of function. He argued that it is entirely possible that some symptoms can be explained by a secondary effect of the damage on other regions, such as, for example, some positive symptoms resulting from a ‘release’ mechanism (Jackson, 1881, 1894;

Associationist theories and the disconnection syndromes

The discovery of long-range connections in the brain and their importance for a complete understanding of the mechanisms underlying brain function and its disorders predates of two centuries Broca's description of cortical localization of speech. In 1664 Thomas Willis was among the first to use sections of the brainstem to differentiate between ascending and descending tracts in the ‘corpus striatum’ and to speculate on possible associated motor and sensory functions:

The medulla oblongata seems

A tractography atlas for clinico-anatomical correlation

Brain atlases have always played an important part in understanding the anatomical basis of neurological and psychiatric disorders. Previous atlases were the offspring of methodological advancements available at that time (Dejerine, 1895; Campbell, 1905; Brodmann, 1909; Von Economo and Koskinas, 1925; Talairach and Tournoux, 1988). Most of these atlases contain detailed cortical maps with little information on the anatomy of underlying white matter. In this section we introduce a

A network approach to classical cerebral lobe syndromes

In this section we present a synopsis of the classical neurological syndromes based on classical textbooks or monographs (Mesulam, 2000; Salloway et al., 2001; Stuss and Knight, 2002; Cummings and Mega, 2003; Darby and Walsh, 2005), supplemented by more recent clinical diffusion tensor tractography studies in common neuropsychiatric disorders. Although the order of presentation follows a lobar division, our aim is to stimulate a broader view of these syndromes and ultimately promote a network

Frontal lobe

The principal subdivisions of the frontal lobe (Fig. 8) are: (i) precentral cortex (BA 4 and inferior 6); (ii) premotor cortex (BA 6, 8, 44, 45) (iii) prefrontal cortex (BA 9, 10, 46, 47); and (iv) orbitofrontal cortex (BA 11, 47). The clinical manifestations commonly associated with frontal lobe lesions can be grouped into four syndromes (Table 1).

Parietal lobe

The parietal lobe includes: (i) post-central gyrus (BA 3, 1, 2); (ii) superior parietal lobule (BA 5, 7); (iii) inferior parietal lobule (BA 39, 40); (iv) precuneus (medial BA 5, 7); and (v) posterior parietal gyrus (BA 19) (Fig. 9). The parietal syndromes can be divided into five groups (Table 2).

Occipital lobe

The occipital lobe is divided into a primary visual cortex (BA17), also designated as striate cortex, and a much more extended extrastriate cortex, which corresponds to the occipital visual association areas (BA 18, 19) (Fig. 10). Disorders associated with occipital lobe lesions can be grouped into three categories (Table 3).

Temporal lobe

The main divisions of the temporal lobe include the: (i) primary auditory cortex (BA41); (ii) auditory association cortex (BA42, 22); (iii) visual association cortex (BA20, 21, 37); (iv) temporopolar cortex (BA38) (Fig. 11). Lesions to each of the above regions cause four distinct temporal lobe syndromes (Table 4).

Limbic lobe

The limbic system includes a core subcortical network (centred around the hippocampus and thalamus) formed by the fornix and mammillo-thalamic tract, and a group of paralimbic cortical areas connected through the cingulum and uncinate fasciculus (Fig. 12). Other tracts, such as the inferior longitudinal fasciculus and inferior fronto-occipital fasciculus connect the limbic regions to visual and auditory areas. The limbic lobe syndromes are divided into three distinct groups (Table 5).

Discussion and conclusions

In this study we provide a new digital atlas of white matter tracts based on diffusion tensor imaging tractography to facilitate the anatomical localization of deep white matter lesions. The atlas is accompanied by a synopsis of the major lobe syndromes to help correlating white matter lesions with clinical manifestations. The atlas has three main features: (i) it provides normalized maps in a reference space (i.e., MNI); (ii) it is derived from a statistical analysis at a group level and,

Acknowledgements

This project was generously supported by Guy's and St Thomas' Charity (GSST), The Wellcome Trust, the Medical Research Council, UK Autism Multi-Centre Imaging Study network (AIMS), the French Agence Nationale de la Recherche (project CAFORPFC, no. ANR-09-RPDOC-004-01 and project HM-TC, no. ANR-09-EMER-006) and the National Division of the South London and Maudsley NHS Foundation Trust. AS, SW, DM and Fd'A were supported by the NIHR Biomedical Research Centre for Mental Health at South London

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Research reportBeyond cortical localization in clinico-anatomical correlation

Abstract

Introduction

Section snippets

Cortical localizationism and the origin of the clinico-anatomical correlation method

Holism and the abandonment of the clinico-anatomical correlation method

Associationist theories and the disconnection syndromes

A tractography atlas for clinico-anatomical correlation

A network approach to classical cerebral lobe syndromes

Frontal lobe

Parietal lobe

Occipital lobe

Temporal lobe

Limbic lobe

Discussion and conclusions

Acknowledgements

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NeuroImage

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NeuroImage

NeuroImage

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Neuropsychologia

Cortex

Cortex

Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease

Brain

Impaired recognition of emotion in facial expressions following bilateral damage to the human amydgala

Nature

Language networks in semantic dementia

Brain

Topographical disorientation: A synthesis and taxonomy

Brain

Neuropsychological and neuroanatomical dimensions of ideomotor apraxia

Brain

Ueber die Selbstwahrnehmung der Herderkrankungen des Gehirns durch den Kranken bei Rindenblindheit und Rindentaubheit

Archiv für Psychiatrie

Disruption of white matter integrity in the inferior longitudinal fasciculus in adolescents with schizophrenia as revealed by fiber tractography

Archives of General Psychiatry

Considérations sur les localisations cérébrales et en particulier sur le siège de la faculté du language articulé

Reprise de la discussion sur la forme et le volume du cerveau

Bulletins de la Société d'Anthropologie de Paris

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In vivo fiber tractography using DT-MRI data

Magnetic Resonance in Medicine

Sensory syndromes in parietal stroke

Neurology

Visual hypoemotionality as a symptom of visual-limbic disconnection in man

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Frontal callosal disconnection syndromes

Cortex

Developmental Gerstmann syndrome

Neurology

Stimulating illusory own-body perceptions

Nature

Research report
Beyond cortical localization in clinico-anatomical correlation