Structural connectivity in a single case of progressive prosopagnosia: The role of the right inferior longitudinal fasciculus

Progressive prosopagnosia (PP) is a clinical syndrome characterized by a progressive and selective inability to recognize and identify faces of familiar people. Here we report a patient (G.S.) with PP, mainly related to a prominent deficit in recognition of familiar faces, without a semantic (cross-modal) impairment. An in-depth evaluation showed that his deficit extended to other classes of objects, both living and non-living. A follow-up neuropsychological assessment did not reveal substantial changes after about 1 year. Structural MRI showed predominant right temporal lobe atrophy. Diffusion tensor imaging was performed to elucidate structural connectivity of the inferior longitudinal fasciculus (ILF) and the inferior fronto-occipital fasciculus (IFOF), the two major tracts that project through the core fusiform region to the anterior temporal and frontal cortices, respectively. Right ILF was markedly reduced in G.S., while left ILF and IFOFs were apparently preserved. These data are in favour of a crucial role of the neural circuit subserved by right ILF in the pathogenesis of PP.

[1]  P. Garthwaite,et al.  Investigation of the single case in neuropsychology: confidence limits on the abnormality of test scores and test score differences , 2002, Neuropsychologia.

[2]  H. Moser,et al.  Imaging cortical association tracts in the human brain using diffusion‐tensor‐based axonal tracking , 2002, Magnetic resonance in medicine.

[3]  M. Albert,et al.  Visual agnosia-prosopagnosia. A clinicopathologic correlation. , 1974, Archives of neurology.

[4]  J. C. Meadows.  The anatomical basis of prosopagnosia , 1974, Journal of neurology, neurosurgery, and psychiatry.

[5]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[6]  K. Nakayama,et al.  Please Scroll down for Article Cognitive Neuropsychology Family Resemblance: Ten Family Members with Prosopagnosia and Within-class Object Agnosia , 2022 .

[7]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[8]  H. Spinnler,et al.  Slowly progressive semantic impairment with category specificity , 1995 .

[9]  Luigi Trojano,et al.  Do visuospatial and constructional disturbances differentiate frontal variant of frontotemporal dementia and Alzheimer's disease? An experimental study of a clinical belief , 2002, International journal of geriatric psychiatry.

[10]  H Spinnler,et al.  C ROSSMODAL AGNOSIA FOR FAMILIAR PEOPLE AS A CONSEQUENCE OF RIGHT INFERO POLAR TEMPORAL ATROPHY , 2001, Cognitive neuropsychology.

[11]  E. Barbeau,et al.  Progressive prosopagnosia , 2004, Neurology.

[12]  I. M. Harris,et al.  Please Scroll down for Article Cognitive Neuropsychology Face Inversion Superiority in a Case of Prosopagnosia following Congenital Brain Abnormalities: What Can It Tell Us about the Specificity and Origin of Face- Processing Mechanisms? , 2022 .

[13]  D. Grossi,et al.  Relationships between Constructional and Visuospatial Abilities in Normal Subjects and in Focal Brain-damaged Patients , 2004, Journal of clinical and experimental neuropsychology.

[14]  B L Miller,et al.  Progressive right frontotemporal degeneration: clinical, neuropsychological and SPECT characteristics. , 1993, Dementia.

[15]  M. Habib.  Visual hypoemotionality and prosopagnosia associated with right temporal lobe isolation , 1986, Neuropsychologia.

[16]  Giuseppe Zappalà,et al.  The mini‐mental state examination: Normative study of an Italian random sample , 1993 .

[17]  T Yamamoto,et al.  Selective impairment of facial recognition due to a haematoma restricted to the right fusiform and lateral occipital region , 2001, Journal of neurology, neurosurgery, and psychiatry.

[18]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[19]  Galit Yovel,et al.  Specialized Face Perception Mechanisms Extract Both Part and Spacing Information: Evidence from Developmental Prosopagnosia , 2006, Journal of Cognitive Neuroscience.

[20]  A. Kertesz,et al.  The Frontal Behavioural Inventory (Italian version) differentiates frontotemporal lobar degeneration variants from Alzheimer's disease , 2007, Neurological Sciences.

[21]  P. V. van Zijl,et al.  Analysis of noise effects on DTI‐based tractography using the brute‐force and multi‐ROI approach , 2004, Magnetic resonance in medicine.

[22]  R. Faber,et al.  Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. , 1999, Neurology.

[23]  L. Pelosi,et al.  On the different roles of the cerebral hemispheres in mental imagery: The “o'Clock Test” in two clinical cases , 1989, Brain and Cognition.

[24]  Paola Scifo,et al.  Evidence of white matter changes on diffusion tensor imaging in frontotemporal dementia. , 2007, Archives of neurology.

[25]  C. Jack,et al.  Two distinct subtypes of right temporal variant frontotemporal dementia , 2009, Neurology.

[26]  Nikolaus Weiskopf,et al.  Voxel-based morphometry reveals reduced grey matter volume in the temporal cortex of developmental prosopagnosics , 2009, Brain : a journal of neurology.

[27]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

[28]  Paul H Garthwaite,et al.  Comparison of a single case to a control or normative sample in neuropsychology: Development of a Bayesian approach , 2007, Cognitive neuropsychology.

[29]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[30]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[31]  P. Caffarra,et al.  Rey-Osterrieth complex figure: normative values in an Italian population sample , 2002, Neurological Sciences.

[32]  T. Allison,et al.  Face recognition in human extrastriate cortex. , 1994, Journal of neurophysiology.

[33]  Marcella Laiacona,et al.  Tre test clinici di ricerca e produzione lessicale , 1986 .

[34]  J. Keenan,et al.  Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia , 2002, Neurology.

[35]  Massimo Filippi,et al.  Brain networks in posterior cortical atrophy: A single case tractography study and literature review , 2012, Cortex.

[36]  Mitsuru Kawamura,et al.  Prosopagnosia: A Clinical and Anatomical Study of Four Patients , 1995, Cortex.

[37]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[38]  E. Renzi,et al.  Apperceptive and Associative Forms of Prosopagnosia , 1991, Cortex.

[39]  M N Rossor,et al.  Heterogeneity in progressive aphasia due to focal cortical atrophy. A clinical and PET study. , 1990, Brain : a journal of neurology.

[40]  Guido Gainotti,et al.  Slowly progressive defect in recognition of familiar people in a patient with right anterior temporal atrophy. , 2003, Brain : a journal of neurology.

[41]  Hans Spinnler,et al.  Progressive defective recognition of familiar people , 1999 .

[42]  J. Greene.  Contributions to Neuropsychological Assessment , 1995 .

[43]  Joachim Bodamer,et al.  Die Prosop-Agnosie , 2004, Archiv für Psychiatrie und Nervenkrankheiten.

[44]  Galia Avidan,et al.  Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia , 2009, Nature Neuroscience.

[45]  A. Paivio,et al.  Comparisons of mental clocks. , 1978, Journal of experimental psychology. Human perception and performance.

[46]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

[47]  J. Devlin,et al.  Triple Dissociation of Faces, Bodies, and Objects in Extrastriate Cortex , 2009, Current Biology.

[48]  R. Goebel,et al.  Tracking the Mind's Image in the Brain I Time-Resolved fMRI during Visuospatial Mental Imagery , 2002, Neuron.

[49]  C. Papagno,et al.  Verbal and spatial immediate memory span: Normative data from 1355 adults and 1112 children , 1987, The Italian Journal of Neurological Sciences.

[50]  E. De Renzi,et al.  Prosopagnosia in two patients with CT scan evidence of damage confined to the right hemisphere. , 1986, Neuropsychologia.

[51]  R. Tootell,et al.  An anterior temporal face patch in human cortex, predicted by macaque maps , 2009, Proceedings of the National Academy of Sciences.

[52]  S. Tobimatsu,et al.  Electrophysiological correlates of associative visual agnosia lesioned in the ventral pathway , 2004, Journal of the Neurological Sciences.

[53]  Marsel Mesulam,et al.  Defining Neurocognitive Networks in the BOLD New World of Computed Connectivity , 2009, Neuron.

[54]  J. Barton.  Structure and function in acquired prosopagnosia: lessons from a series of 10 patients with brain damage. , 2008, Journal of neuropsychology.

[55]  J. Barton,et al.  Impaired configurational processing in a case of progressive prosopagnosia associated with predominant right temporal lobe atrophy. , 2003, Brain : a journal of neurology.

[56]  P. Nichelli,et al.  The Frontal Assessment Battery (FAB): normative values in an Italian population sample , 2005, Neurological Sciences.

[57]  Galia Avidan,et al.  Structural imaging reveals anatomical alterations in inferotemporal cortex in congenital prosopagnosia. , 2007, Cerebral cortex.

[58]  K. Nakayama,et al.  The Cambridge Face Memory Test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants , 2006, Neuropsychologia.

[59]  Doris Y. Tsao,et al.  Comparing face patch systems in macaques and humans , 2008, Proceedings of the National Academy of Sciences.

[60]  S Mohammadi,et al.  Pattern and progression of white-matter changes in a case of posterior cortical atrophy using diffusion tensor imaging , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

[61]  K. Nagata,et al.  A case of associative visual agnosia: neuropsychological findings and theoretical considerations. , 1989, Journal of clinical and experimental neuropsychology.

[62]  M. Catani,et al.  The rises and falls of disconnection syndromes. , 2005, Brain : a journal of neurology.

[63]  M. Farah,et al.  The inverted face inversion effect in prosopagnosia: Evidence for mandatory, face-specific perceptual mechanisms , 1995, Vision Research.

[64]  Massimo Filippi,et al.  Ventral and dorsal visual streams in posterior cortical atrophy: A DT MRI study , 2012, Neurobiology of Aging.

[65]  N. Kanwisher,et al.  The fusiform face area subserves face perception, not generic within-category identification , 2004, Nature Neuroscience.

[66]  Philip Scheltens,et al.  The clinical profile of right temporal lobe atrophy. , 2004, Brain : a journal of neurology.

[67]  L. Fadda,et al.  Batteria per la valutazione del Deterioramento Mentale (parte I): descrizione di uno strumento di diagnosi neuropsicologica , 1995 .

[68]  John R. Hodges,et al.  Progressive prosopagnosia associated with selective right temporal lobe atrophy. A new syndrome? , 1995, Brain : a journal of neurology.

[69]  Giuseppe Iaria,et al.  Disconnection in prosopagnosia and face processing , 2008, Cortex.

[70]  Paolo Bartolomeo,et al.  The quest for the ‘critical lesion site’ in cognitive deficits: Problems and perspectives , 2011, Cortex.

[71]  T. Allison,et al.  Human extrastriate visual cortex and the perception of faces, words, numbers, and colors. , 1994, Cerebral cortex.

[72]  C. Marra,et al.  Human Neuroscience , 2022 .

[73]  Katsuji Kobayashi,et al.  [Progressive prosopagnosia associated with selective right temporal lobe atrophy]. , 2004, Nihon rinsho. Japanese journal of clinical medicine.

[74]  M. Lee,et al.  Statistical Evidence in Experimental Psychology , 2011, Perspectives on psychological science : a journal of the Association for Psychological Science.

[75]  Andrea Weidenfeld,et al.  An evaluation of two commonly used tests of unfamiliar face recognition , 2003, Neuropsychologia.

[76]  Margot J. Taylor,et al.  The Faces of Development: A Review of Early Face Processing over Childhood , 2004, Journal of Cognitive Neuroscience.

[77]  Martha J. Farah,et al.  Face perception and within-category discrimination in prosopagnosia , 1995, Neuropsychologia.

[78]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[79]  Raja Muthupillai,et al.  Implications of SENSE MR in routine clinical practice. , 2003, European journal of radiology.

[80]  R. Goebel,et al.  Matching two imagined clocks: the functional anatomy of spatial analysis in the absence of visual stimulation. , 2000, Cerebral cortex.

[81]  C. Papagno,et al.  Famous face recognition and naming test: a normative study , 2002, Neurological Sciences.