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Published in: Brain Structure and Function 1/2013

01-01-2013 | Original Article

Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle

Authors: Silvio Sarubbo, Alessandro De Benedictis, Igor L. Maldonado, Gianpaolo Basso, Hugues Duffau

Published in: Brain Structure and Function | Issue 1/2013

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Abstract

The anatomy and functional role of the inferior fronto-occipital fascicle (IFOF) remain poorly known. We accurately analyze its course and the anatomical distribution of its frontal terminations. We propose a classification of the IFOF in different subcomponents. Ten hemispheres (5 left, 5 right) were dissected with Klingler’s technique. In addition to the IFOF dissection, we performed a 4-T diffusion tensor imaging study on a single healthy subject. We identified two layers of IFOF. The first one is superficial and antero-superiorly directed, terminating in the inferior frontal gyrus. The second is deeper and consists of three portions: posterior, middle and anterior. The posterior component terminates in the middle frontal gyrus (MFG) and dorso-lateral prefrontal cortex. The middle component terminates in the MFG and lateral orbito-frontal cortex. The anterior one is directed to the orbito-frontal cortex and frontal pole. In vivo tractography study confirmed these anatomical findings. We suggest that the distribution of IFOF fibers within the frontal lobe corresponds to a fine functional segmentation. IFOF can be considered as a “multi-function” bundle, with each anatomical subcomponent subserving different brain processing. The superficial layer and the posterior component of the deep layer, which connects the occipital extrastriate, temporo-basal and inferior frontal cortices, might subserve semantic processing. The middle component of the deep layer could play a role in a multimodal sensory–motor integration. Finally, the anterior component of the deep layer might be involved in emotional and behavioral aspects.
Literature
go back to reference Aralamask A, Ulmer JL, Kocak M, Salvan CV, Hillis AE, Youssen DM (2006) Association, commissural, and projection pathways and their functional deficit reported in literature. J Comput Assist Tomogr 30:695–715CrossRef Aralamask A, Ulmer JL, Kocak M, Salvan CV, Hillis AE, Youssen DM (2006) Association, commissural, and projection pathways and their functional deficit reported in literature. J Comput Assist Tomogr 30:695–715CrossRef
go back to reference Bookheimer S (2002) Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Ann Rev Neurosci 25:151–188PubMedCrossRef Bookheimer S (2002) Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Ann Rev Neurosci 25:151–188PubMedCrossRef
go back to reference Burgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29:1092–1105 Burgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29:1092–1105
go back to reference Cabeza R, Nyberg L (2000) Imaging cognition II: an empirical review of 275 pet and fMRI studies. J Cogn Neurosci 12:1–47PubMedCrossRef Cabeza R, Nyberg L (2000) Imaging cognition II: an empirical review of 275 pet and fMRI studies. J Cogn Neurosci 12:1–47PubMedCrossRef
go back to reference Catani M, Mesulam M (2008) The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex 44:953–961PubMedCrossRef Catani M, Mesulam M (2008) The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex 44:953–961PubMedCrossRef
go back to reference Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132PubMedCrossRef Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132PubMedCrossRef
go back to reference Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94PubMedCrossRef Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94PubMedCrossRef
go back to reference Curran EJ (1909) A new association fiber tract in the cerebrum. J Comp Neurol 19:645–656 Curran EJ (1909) A new association fiber tract in the cerebrum. J Comp Neurol 19:645–656
go back to reference Dejerine JJ (1895) Anatomie des Centres Nerveux. Rueff et Cie, Paris Dejerine JJ (1895) Anatomie des Centres Nerveux. Rueff et Cie, Paris
go back to reference Dorrichi F, Thiebaut De Schotten M, Tomaiuolo F, Bartolomeo P (2008) White matter (dis)connections and gray matter (dys)functions in visual neglect: gaining insights into the brain networks of spatial awareness. Cortex 44:983–985CrossRef Dorrichi F, Thiebaut De Schotten M, Tomaiuolo F, Bartolomeo P (2008) White matter (dis)connections and gray matter (dys)functions in visual neglect: gaining insights into the brain networks of spatial awareness. Cortex 44:983–985CrossRef
go back to reference Duffau H (2008) The anatomo-functional connectivity of language revisited: new insights provided by electrostimulation and tractography. Neuropsychologia 46:927–934PubMedCrossRef Duffau H (2008) The anatomo-functional connectivity of language revisited: new insights provided by electrostimulation and tractography. Neuropsychologia 46:927–934PubMedCrossRef
go back to reference Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128:797–810PubMedCrossRef Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128:797–810PubMedCrossRef
go back to reference Epelbaum S, Pinel P, Gaillard R, Delmaire C, Perrin M, Dupont S, Dehaene S, Cohen L (2008) Pure alexia as a disconnection syndrome. New diffusion imaging evidence for an old concept. Cortex 44:962–974PubMedCrossRef Epelbaum S, Pinel P, Gaillard R, Delmaire C, Perrin M, Dupont S, Dehaene S, Cohen L (2008) Pure alexia as a disconnection syndrome. New diffusion imaging evidence for an old concept. Cortex 44:962–974PubMedCrossRef
go back to reference Ernst M, Bolla K, Mouratidis M, Contoreggi C, Matochik JA, Kurian V, Cadet JL, Kimes AS, London ED (2002) Decision-making in a risk-taking task: a pet study. Neuropsychopharmacology 26:682–691PubMedCrossRef Ernst M, Bolla K, Mouratidis M, Contoreggi C, Matochik JA, Kurian V, Cadet JL, Kimes AS, London ED (2002) Decision-making in a risk-taking task: a pet study. Neuropsychopharmacology 26:682–691PubMedCrossRef
go back to reference Fox CJ, Iara G, Barton JJS (2008) Disconnection in prosopagnosia and face processing. Cortex 44:996–1009PubMedCrossRef Fox CJ, Iara G, Barton JJS (2008) Disconnection in prosopagnosia and face processing. Cortex 44:996–1009PubMedCrossRef
go back to reference Garibotto V, Scifo P, Gorini A, Alonso CR, Brambati S, Bellodi L, Perani D (2009) Disorganization of anatomical connectivity in obsessive compulsive disorder: a multi-parameter diffusion tensor imaging study in a subpopulation of patients. Neurobiol Dis 37:468–476PubMedCrossRef Garibotto V, Scifo P, Gorini A, Alonso CR, Brambati S, Bellodi L, Perani D (2009) Disorganization of anatomical connectivity in obsessive compulsive disorder: a multi-parameter diffusion tensor imaging study in a subpopulation of patients. Neurobiol Dis 37:468–476PubMedCrossRef
go back to reference Heimer I (1995) The human brain and spinal cord: functional neuroanatomy and dissection guide, 2nd edn. Springer, New York Heimer I (1995) The human brain and spinal cord: functional neuroanatomy and dissection guide, 2nd edn. Springer, New York
go back to reference Henry RG, Berman JI, Nagarajan SS, Mukherjee P, Berger MS (2004) Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping. Neuroimage 21:616–622PubMedCrossRef Henry RG, Berman JI, Nagarajan SS, Mukherjee P, Berger MS (2004) Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping. Neuroimage 21:616–622PubMedCrossRef
go back to reference Jacobson S, Kelleher I, Harley M, Murtagh A, Clarke M, Blanchard M, Connolly C, O’hanlon E, Garavan H, Cannon M (2010) Structural and functional brain correlates of subclinical psychotic symptoms in 11–13 year old schoolchildren. Neuroimage 49:1875–1885PubMedCrossRef Jacobson S, Kelleher I, Harley M, Murtagh A, Clarke M, Blanchard M, Connolly C, O’hanlon E, Garavan H, Cannon M (2010) Structural and functional brain correlates of subclinical psychotic symptoms in 11–13 year old schoolchildren. Neuroimage 49:1875–1885PubMedCrossRef
go back to reference Klingler J (1935) Erleichterung der makroskopischen Präparation des Gehirns 78 durch den Gefrierprozess. Schweiz Arch Neurol Psychiatr 36:247–256 Klingler J (1935) Erleichterung der makroskopischen Präparation des Gehirns 78 durch den Gefrierprozess. Schweiz Arch Neurol Psychiatr 36:247–256
go back to reference Kvickström P, Eriksson B, Van Westen D, Lätt J, Elfgren C, Nilsson C (2011) Selective frontal neurodegeneration of the inferior fronto-occipital fasciculus in progressive supranuclear palsy (PSP) demonstrated by diffusion tensor tractography. BMC Neurol 11:13PubMedCrossRef Kvickström P, Eriksson B, Van Westen D, Lätt J, Elfgren C, Nilsson C (2011) Selective frontal neurodegeneration of the inferior fronto-occipital fasciculus in progressive supranuclear palsy (PSP) demonstrated by diffusion tensor tractography. BMC Neurol 11:13PubMedCrossRef
go back to reference Lawes IN, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, Clark CA (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39:62–79PubMedCrossRef Lawes IN, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, Clark CA (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39:62–79PubMedCrossRef
go back to reference Lawrence NS, Jollant F, O’daly O, Zelaya F, Phillips ML (2009) Distinct roles of prefrontal cortical subregions in the Iowa gambling task. Cereb Cortex 19:1134–1143PubMedCrossRef Lawrence NS, Jollant F, O’daly O, Zelaya F, Phillips ML (2009) Distinct roles of prefrontal cortical subregions in the Iowa gambling task. Cereb Cortex 19:1134–1143PubMedCrossRef
go back to reference Ludwig E, Klingler J (1956) Atlas cerebri humani. The inner structure of the brain demonstrated on the basis of macroscopical preparations. Little Brown, Boston Ludwig E, Klingler J (1956) Atlas cerebri humani. The inner structure of the brain demonstrated on the basis of macroscopical preparations. Little Brown, Boston
go back to reference Martino J, Brogna C, Robles SG, Vergani F, Duffau H (2009) Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46:691–699PubMedCrossRef Martino J, Brogna C, Robles SG, Vergani F, Duffau H (2009) Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46:691–699PubMedCrossRef
go back to reference Martino J, Vergani F, Robles SG, Duffau H (2010) New insights into the anatomic dissection of the temporal stem with special emphasis on the inferior fronto-occipital fasciculus: implications in surgical approach to left mesiotemporal and temporoinsular structures. Neurosurgery 66:4–12PubMedCrossRef Martino J, Vergani F, Robles SG, Duffau H (2010) New insights into the anatomic dissection of the temporal stem with special emphasis on the inferior fronto-occipital fasciculus: implications in surgical approach to left mesiotemporal and temporoinsular structures. Neurosurgery 66:4–12PubMedCrossRef
go back to reference Mori S, Wakana S, Nagae-Poetscher LM, Van Zijl PCM (2005) MRI atlas of human white matter. Elsevier, Amsterdam Mori S, Wakana S, Nagae-Poetscher LM, Van Zijl PCM (2005) MRI atlas of human white matter. Elsevier, Amsterdam
go back to reference Petrides M, Pandya DN (2006) Efferent association pathways originating in the caudal prefrontal cortex in the macaque monkey. J Comp Neurol 498:227–251PubMedCrossRef Petrides M, Pandya DN (2006) Efferent association pathways originating in the caudal prefrontal cortex in the macaque monkey. J Comp Neurol 498:227–251PubMedCrossRef
go back to reference Philippi CL, Mehta S, Grabowski T, Adolphs R, Rudrauf D (2009) Damage to association fiber tracts impairs recognition of the facial expression of emotion. J Neurosci 29:15089–15099PubMedCrossRef Philippi CL, Mehta S, Grabowski T, Adolphs R, Rudrauf D (2009) Damage to association fiber tracts impairs recognition of the facial expression of emotion. J Neurosci 29:15089–15099PubMedCrossRef
go back to reference Plaza M, Gatignol P, Cohen H, Berger B, Duffau H (2008) A discrete area within the left dorsolateral prefrontal cortex involved in visual–verbal incongruence judgment. Cereb Cortex 18:1253–1259PubMedCrossRef Plaza M, Gatignol P, Cohen H, Berger B, Duffau H (2008) A discrete area within the left dorsolateral prefrontal cortex involved in visual–verbal incongruence judgment. Cereb Cortex 18:1253–1259PubMedCrossRef
go back to reference Rizzolatti G, Matelli M (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153:146–157PubMedCrossRef Rizzolatti G, Matelli M (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153:146–157PubMedCrossRef
go back to reference Rollins NK, Vachha B, Srinivasan P, Chia J, Pickering J, Hughes CW, Gimi B (2009) Simple developmental dyslexia in children: alterations in diffusion-tensor metrics of white matter tracts at 3 T. Radiology 251:882–891PubMedCrossRef Rollins NK, Vachha B, Srinivasan P, Chia J, Pickering J, Hughes CW, Gimi B (2009) Simple developmental dyslexia in children: alterations in diffusion-tensor metrics of white matter tracts at 3 T. Radiology 251:882–891PubMedCrossRef
go back to reference Rudrauff D, Mehta S, Grabowski T (2008) Disconnection’s renaissance takes shape: format incorporation in group-level lesion studies. Cortex 44:1084–1096CrossRef Rudrauff D, Mehta S, Grabowski T (2008) Disconnection’s renaissance takes shape: format incorporation in group-level lesion studies. Cortex 44:1084–1096CrossRef
go back to reference Rykhlevskaia E, Uddin LQ, Kondos L, Menon V (2009) Neuroanatomical correlates of developmental dyscalculia: combined evidence from morphometry and tractography. Front Hum Neurosci 3:51PubMedCrossRef Rykhlevskaia E, Uddin LQ, Kondos L, Menon V (2009) Neuroanatomical correlates of developmental dyscalculia: combined evidence from morphometry and tractography. Front Hum Neurosci 3:51PubMedCrossRef
go back to reference Schmahmann JD, Pandya DN (2006) Fiber pathways of the brain. Oxford University Press, New York Schmahmann JD, Pandya DN (2006) Fiber pathways of the brain. Oxford University Press, New York
go back to reference Schmahmann JD, Pandya DN (2007) The complex history of the fronto-occipital fasciculus. J Hist Neurosci 16:362–377PubMedCrossRef Schmahmann JD, Pandya DN (2007) The complex history of the fronto-occipital fasciculus. J Hist Neurosci 16:362–377PubMedCrossRef
go back to reference Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Wedeen VJ (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130:630–653PubMedCrossRef Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Wedeen VJ (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130:630–653PubMedCrossRef
go back to reference Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy R, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:208–219CrossRef Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy R, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:208–219CrossRef
go back to reference Vigneau M, Beaucousin V, Hervé PY, Duffau H, Crivello F, Houdé O, Mazoyer B, Tzourio-Mazoyer N (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30:1414–1432PubMedCrossRef Vigneau M, Beaucousin V, Hervé PY, Duffau H, Crivello F, Houdé O, Mazoyer B, Tzourio-Mazoyer N (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30:1414–1432PubMedCrossRef
Metadata
Title
Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle
Authors
Silvio Sarubbo
Alessandro De Benedictis
Igor L. Maldonado
Gianpaolo Basso
Hugues Duffau
Publication date
01-01-2013
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 1/2013
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-011-0372-3

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