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New insights in the limbic modulation of visual inputs: The role of the inferior longitudinal fasciculus and the Li-Am bundle

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Abstract

Recent anatomical and DTI data demonstrated new aspects in the subcortical occipito-temporal connections. Although a direct (inferior longitudinal fasciculus, ILF) pathway has been previously described, its fine description is still matter of debate. Moreover, a fast and direct subcortical connection between the limbic system and the occipital lobe has been previously recognized in many functional studies but it still remains poorly documented by anatomical images. We provided for the first time an extensive and detailed anatomical description of the ILF subcortical segmentation. We dissected four human hemispheres with modified Klingler’s technique, from the basal to the lateral occipito-temporal surface in the two steps, tracking the ILF fibers until their cortical termination. Pictures of this direct temporo-occipital pathway are discussed in the light of recent literature regarding anatomy and functions of occipito-temporal areas. The dissection confirmed the classical originating branches of ILF and allowed a fine description of two main subcomponent of this bundle, both characterized by separate hierarchical distribution: a dorsal ILF and a ventral ILF. Moreover, a direct pathway between lingual cortex and amygdala, not previously demonstrated, is here described with anatomical images. Even if preliminary in results, this is the first fine description of ILF’s subcomponents. The complex but clearly segregated organization of the fibers of this bundle (dILF and vILF) supports different level of functions mediated by visual recognition. Moreover, the newly described direct pathway from lingual to amygdala (Li-Am), seems involved in the limbic modulation of visual processing, so it may support physiological conditions the crucial role of this connection in human social cognition. In pathological conditions, on the other hand, this may be one of the hyperactivated pathways in temporo-occipital epileptic and nonepileptic syndromes.

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Acknowledgments

We acknowledge Dr Roberta Schivalocchi from Ferrara University-Hospital (Italy) for her constant support and we would like to express our sincere thanks for the enthusiastic help and courtesy in providing the fine artistic illustrations of this article.

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  1. Division of Neurosurgery, Department of Neuroscience and Rehabilitation, S. Anna University Hospital, Ferrara, Italy

    Francesco Latini

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Guilherme Carvalhal Ribas, São Paulo, Brazil

The fiber dissection technique was already employed by early anatomists as Thomas Willis (1621–1675), Nicholas Steno (1638–1686), Raymond Vieussens (1641–1715), Charles Bell (1774–1842), Johan Christian Reil (1759–1813), Achille Foville (1799–1878), Bartholomeo Panizza (1785–1867), Louis Pierre Gratiolet (1815–1865), and Theodor H Meynert (1833–1892) among others(2,5) in order to understand the complex white matter architectural organization and to better describe its tracts, fasciculi, and commissural fibers, but it was only with the contribution of Joseph Klinger (1888–1963) that this technique became more feasible and widely used(4,5). Klinger described in 1935 the freezing technique of previously formalin-fixed brains, which generates the development of formalin ice crystals between the fibers which facilitates their dissection that is done by their progressive peeling(3).

More recently, the advent of tractography, which is a 3D MRI modeling technique based on collected data obtained by diffusion tensor imaging (DTI) that evaluates brain water diffusion in a tensor, which is the major axis parallel to the direction of fibers—different bundles of fiber tracts make the water diffuse asymmetrically in a tensor, which is directly related with the number of fibers and is known as anisotropy—is generating a significant amount of imaging data which subsequently requires to be validated, and the Klinger technique or its variations still are the most practical way of doing it.

In this direction, Dr. Latini, taking into consideration also previous DTI findings, studied the inferior longitudinal fasciculus and its related subcomponents. Although based on the dissections of only four hemispheres of two brain specimens, this interesting article brings some more light into the understanding of the complex inferior longitudinal fascicle, and, above all, has the merit of describing a new bundle, the lingual-amygdaloidal bundle.

Nevertheless, for a proper appraisal of the author’s study, it is important to consider that both fiber dissection and DTI techniques have similar limitations regarding the identification of small bundles, particularly in regions where fibers intermingle. Even when the fiber dissection technique is done under magnification, it is very difficult to dissect and peel the multiple layers of fibers that are intermingled with fibers that run in other directions, and also to securely identify the fibers that belong to different fasciculi which are superimposed and running along the same direction. On the other hand, the DTI technique, although extremely helpful, uses a computer-based image analysis to do a nondirect measure of the fiber’s structure and integrity, which implies some degree of subjectiveness since this technique is in part dependent on a number of factors under the control of the experimenter, such as the angular and anisotropy thresholds and the choice of the tractography algorithm itself, as stated by Catani et al.(1).

Considering these methodological issues and the small number of dissected specimens, the results of this elegant study, and their discussed inferential functional roles, should now motivate further research of this important subject in order to corroborate its findings and considerations.

References

1. Catani M, Schotten MT (2012) Introduction to diffusion imaging tractography. In: Atlas of Human Brain Connections. New York: Oxford University Press.

2. Clarke E, O’Malley CD (eds) (1996) The human brain and spinal cord: a historical study illustrated by writings from antiquity to the twentieth century. San Francisco: Norman.

3. Klinger J (1935) Erleichterung der makroskopischen Präparation des Gehirn durch den Gefrierprozess. Schweiz Arch-Neurol Psychiat 36: 247–256 apud Türe U, Yasargil MG, Friedman AH, Al-Mefty O (2000) Fiber dissection technique: lateral aspect of the brain. Neurosurgery 47: 417–427.

4. Ludwig E, Klinger J (1956) Atlas Cerebri Humani. Basel: S. Karger.

5. Türe U, Yasargil MG, Friedman AH, Al-Mefty O (2000) Fiber dissection technique: lateral aspect of the brain. Neurosurgery 47: 417–427.

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Latini, F. New insights in the limbic modulation of visual inputs: The role of the inferior longitudinal fasciculus and the Li-Am bundle. Neurosurg Rev 38, 179–190 (2015). https://doi.org/10.1007/s10143-014-0583-1

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