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Existing evidence fails to support the contention that the uncinate fasciculus has a primary role in anxiety disorders or schizophrenia. Schmahmann JD, Smith EE, Eichler FS, Filley CM. DTI and MTR abnormalities in schizophrenia: analysis of white matter integrity. diffusion tensor imaging, episodic memory, orbitofrontal cortex, schizophrenia, anterior temporal lobe. Understanding the function and dysfunction of the uncinate fasciculus is of particular interest because of its clinical relevance. Separate value compairson and learning mechanisms in macaque medial and lateral orbitofrontal cortex. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health or the National Institutes of Health. Next, we critically evaluate the literature associating abnormalities in the uncinate fasciculus with a range of neurological and psychiatric disorders. The uncinate fasciculus is a bidirectional, long-range white matter tract that connects lateral orbitofrontal cortex and Brodmann area 10 with the anterior temporal lobes. Several studies in monkeys and a related study in humans (Thomas et al., 2012) suggest that the uncinate fasciculus supports some types of associative learning, but perhaps not in the obvious way of forming the actual linkage between two stimuli, such as a face and a place. Our hypothesis is vague regarding the effects of laterality on uncinate fasciculus function, reflecting the state of the literature. Some caution in extending function from monkeys to humans is in order given the putative role of the human anterior temporal lobe and the uncinate fasciculus in one aspect of language processing, semantic retrieval. Traumatic brain injury and the frontal lobes: What can we gain with diffusion tensor imaging? Uncinate fasciculus abnormalities in recent onset schizophrenia and affective psychosis: a diffusion tensor imaging study. For instance, if our hypothesis is true, the question arises as to why there are no reports of patients with epilepsy who undergo incidental disconnection of the uncinate fasciculus who become psychopathic or exhibited abnormalities in forming emotional associations? Episodic memory formation relies on the function of medial temporal lobe structures, especially the hippocampus and portions of the frontal lobe, such as dorsolateral prefrontal cortex. Frontotemporal dementias: a review. It is widely accepted that radiological tracer studies offer better precision compared with dissection and DTI; however, tracer studies cannot be conducted in humans. The association between proper naming and the left uncinate fasciculus was indirectly studied by Damasio et al. Language networks in semantic dementia. Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study. Diffusion tensor imaging of incentive effects in prospective memory after pediatric traumatic brain injury. Raine A, Lencz T, Bihrle S, LaCasse L, Colletti P. Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. Zappal G, Thiebaut de Schotten M, Eslinger PJ. Findings of uncinate abnormalities are quite common in this population (Matsuo et al., 2008; Agosta et al., 2010; Whitwell et al., 2010; Acosta-Cabronero et al., 2011; Galantucci et al., 2011). A cerebral stimulation study. An early case study (Jackson and Colman, 1898) identified an epileptic patient who experienced dreamy states and unusual tastes immediately before seizing; post-mortem examination found damage only in the left uncinate fasciculus and the left uncus. Travers BG, Adluru M, Ennis C, Tromp DPM, Destiche D, Doran S, et al. A new association fiber tract in the cerebrum with remarks on the fiber tract dissection method of studying the brain. Bouckoms A, Martuza R, Henderson M. Capgras syndrome with subarachnoid hemorrhage. Diffusion tensor imaging in autism spectrum disorder: a review. National Library of Medicine The selectivity and functional connectivity of the anterior temporal lobes. de Zubicaray GI, Rose SE, McMahon KL. For example, Craig et al. Papagno C. Naming and the role of the uncinate fasciculus in language function. Parker A, Gaffan D. Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions. Based on this evidence, it was hypothesized that the uncinate fasciculus, particularly on the left, was part of the ventral language pathway and that it supported semantic naming by relaying sensory information about objects (presumably in ventral temporal cortex) to language supporting regions (in the lateral frontal lobe; Parker et al., 2005). Grey matter regions connected by the uncinate are also implicated in the abovementioned disorders, as well as in social and emotional processing in general. Focal unilateral lesions of the human uncinate fasciculus occur from time to time, usually in the context of surgical removal of low-grade gliomas. Thiebaut de Schotten et al.s (2012) reconstructions of the uncinate fasciculus using post-mortem axonal tracing in monkeys (modified from Schmahmann and Pandya, 2006) and in vivo tractography in humans demonstrates that anatomical connections of the uncinate fasciculus are largely conserved between the human and monkey brain (used with permission from Thiebaut de Schotten et al., 2012). Although the left uncinate fasciculus does not appear to play a general or exclusive role in language, there is some evidence that it plays a minor supporting role, particularly in lexical retrieval of semantic knowledge. 3). Thomas C, Walker L, Pierpaoli C, Baker C. The role of the uncinate fasciculus in human visual-associative learning. In actuality, however, the function(s) and information transmission properties of this white matter tract are largely unknown. As noted above, there is surprisingly little research on the uncinate fasciculus in epilepsy resection patients. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, et al. In contrast, other deficits that were present immediately after surgery, such as difficulties in remembering lists of words, and deficits in verbal fluency, improved to normal levels 3 months post-surgery. Murray EA, Graham KS, Gaffan D. Perirhinal cortex and its neighbours in the medial temporal lobe: contributions to memory and perception. Whitwell JL, Avula R, Senjem ML, Kantarci K, Weigand SD, Samikoglu A, et al. Capgras delusion is characterized by a patients insistence, despite all evidence to the contrary, that his or her loved one has been replaced by an impostor (Hirstein and Ramachandran, 1997; Edelstyn et al., 2001). Mabbott DJ, Rovet J, Noseworthy MD, Smith ML, Rockel C. The relations between white matter and declarative memory in older children and adolescents. Kier EL, Staib LH, Davis LM, Bronen RA. Second, there is also evidence from some clinical populations suggesting a socialemotional role for the uncinate. (2012) followed-up the monkey studies described above; in their study, participants were required to learn facescene associations through computerized feedback across 1000+ learning trials. After reviewing the literature on uncinate fasciculus function, two credible accounts of uncinate fasciculus function become apparent. Lipson SE, Sacks O, Devinsky O. The enigmatic temporal pole: a review of findings on social and emotional processing. Findings from another subtype of frontotemporal dementia, behavioural variant FTD, complicate this picture. Skipper LM, Ross LA, Olson IR. Markowitsch (1982) proposed that retrograde amnesia was caused by the disconnection of temporal limbic structures from the frontal lobe The task of the uncinate fascicle will be to guide and channel this information flow to the prefrontal cortex and to transmit preprocessed information back to the temporal cortex for the final act of representation (Markowitsch, 1982). Cerebral white matter damage in frontotemporal dementia assessed by diffusion tensor tractography. Visual learning for an auditory secondary reinforcer by macaques is intact after uncinate fascicle section: indirect evidence for the involvement of the corpus striatum. Cells in the ventral anterior temporal lobe have rapid association formation capacities. White matter integrity and prediction of social and role functioning in subjects at ultra-high risk for psychosis. Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, et al. Yang Y, Raine A, Narr KL, Colletti P, Toga AW. Along these lines, Levine et al. Frontotemporal connections in episodic memory and aging: A diffusion MRI tractography study. The temporal pole and nearby tissue constitute part of the anterior temporal lobe. Piguet O, Hornberger M, Mioshi E, Hodges JR. Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management. Mummery CJ, Patterson K, Price CJ, Ashburner J, Frackowiak RSJ, Hodges JR. A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. For instance, patients with behavioural variant FTD have deficits that are primarily related to social and emotional processing (Piguet et al., 2011), as opposed to other variants of FTD, whose symptoms are more linguistic and mnemonic (Hodges, 2001; Whitwell et al., 2010). Olson IR, Plotzker A, Ezzyat Y. The site is secure. McIntosh AM, Maniega SM, Lymer KS, McKirdy J, Hall J, Sussman JED, et al. Why do many psychiatric disorders emerge during adolescence? All DTI studies reported reduced fractional anisotropy values in the right uncinate fasciculus. Kubicki M, McCarley R, Westin CF, Park HJ, Maier S, Kikinis R, et al. The importance of the type of memory tested is highlighted by research on non-human primates. Grabowski TJ, Damasio H, Tranel D, Boles Ponto LL, Hichwa RD, Damasio AR. Croxson PL, Johansen-Berg H, Behrens TEJ, Robson MD, Pinsk MA, Gross CG, et al. The particulars of this function are only beginning to be understood. Lee et al. Adolphs R, Tranel D, Damasio H, Damasio A. Naming deficits are a diagnostic symptom of this disease (Snowden et al., 1989; Hodges et al., 1992; Neary et al., 1998), although patients also usually present with personality changes and are reported by family members to be emotionally distant and lacking in empathy. There is long-standing interest in understanding how fibre pathways that connect these regions function in episodic memory. Preliminary evidence of white matter abnormality in the uncinate fasciculus in generalized social anxiety disorder. a persons name + face + voice + your feelings about a person) to modify behaviour by interacting with systems in the lateral orbital frontal cortex that are instrumental for making associations between stimuli and rewards, and ultimately, decision making. Rudebeck PH, Murray EA. Bishop SJ. This work was supported by a National Institute of Health grant to I. Olson [RO1 MH091113]. Howe JG, Gibson JD. Findings are mixed. A functional MRI study of amygdala responses to angry schematic faces in social anxiety disorder. (2002). More global semantic retrieval deficits are observed in semantic dementia and there is some evidence, reviewed above, linking semantic dementia to uncinate fasciculus deterioration. White matter hemisphere asymmetries in healthy subjects and in schizophrenia: a diffusion tensor MRI study. FOIA There is disagreement as to whether the temporal segment of the uncinate fasciculus extends into the amygdala proper (Croxson et al., 2005; Petrides and Pandya, 2007; Thiebaut de Schotten et al., 2012) and at least one tracer study provided clear evidence that it did not (Ungerleider et al., 1989). One would expect then, that white matter tracts connecting limbic regions to orbitofrontal cortices, like the uncinate fasciculus, might be structurally impaired in anxiety disorders. However, to interpret the findings from DTI, we must gain a better understanding of functional tractography. The left uncinate fasciculus has frequently been associated with language function because it connects regions of the brain that have putative functions in language: the anterior temporal lobes and portions of the frontal lobes, both of which have been proposed to encode, store and retrieve semantic knowledge (Grossman et al., 2004; Catani and Mesulam, 2008). Reduced left uncinate fasciculus fractional anisotropy in deficit schizophrenia but not in non-deficit schizophrenia. Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates. the uncinate fasciculuss connections to social and emotional grey matter regions), correlational (e.g. One interpretation of this finding is that the uncinate fasciculus is involved in associating stimuli with various types of rewards, non-rewards, and punishments that when broadly defined, would include error monitoring (Metzler-Braddeley et al., 2011) that may serve to modulate retrieval of correct pairings (Table 2). Historically, research in these patients has focused on episodic memory and there are few studies of social or emotional processes. In the following section we lay out the argument that the uncinate fasciculus does not have general mnenomic, linguistic, or socialemotional functions. However, further consideration is required. Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys. Han DH, Renshaw PF, Dager SR, Chung A, Hwang J, Daniels MA, et al. However, because the anterior temporal lobe and orbital portions of the frontal lobe are among the earliest regions to experience cell loss in this disorder, the integrity of the uncinate fasciculus is necessarily affected. Parrino JJ. Ghashghaei HT, Hilgetag CC, Barbas H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. government site. The volume of the tract, which was measured by the tractography algorithm as the number of trajectories, correlated negatively with antisocial behaviour in both the left and right uncinate. Indeed, there are no instances of retrograde or anterograde amnesia in which the uncinate alone was destroyed. The uncinate fasciculus does not appear to play a general role in episodic memory, however, nor is it critical for forming or retrieving many common types of mnemonic associations. It is likely that changes in white matter properties of the uncinate fasciculus are the result of aberrant neuronal morphology or firing and thus epiphenomenal to the disorder because most seizures are localized in the medial and anterior temporal lobe regions. A review of diffusion tensor imaging studies in schizophrenia. Another study compared patients diagnosed with behavioural variant FTD and Alzheimers disease, and found no significant differences between the two groups in fractional anisotropy measures of the uncinate fasciculus, although patients with behavioural variant FTD did, on average, have smaller fractional anisotropy values in both the left and right uncinate fasciculus (Tartaglia et al., 2012). Curran EJ. One interpretation of these findings is that the uncinate fasciculus was necessary for retrieving information and keeping count as to which facescene associations were rewarded or punished in the past. We urge future investigators to use larger and more homogenous clinical populations and to correlate specific symptoms, rather than presence or absence of disease state, with changes in white matter. Recommendations for future researchers interested in investigating the role of the uncinate fasciculus in various psychiatric and neurological disorders include: testing larger and more homogeneous clinical samples; correlating specific symptoms and/or theory-driven test performance, rather than disease presence or absence, with various DTI values; and using more rigorous statistical thresholding procedures. Papagno C, Miracapillo C, Casarotti A, Romero Lauro LJ, Castellano A, Falini A, et al. Adolphs R. What does the amygdala contribute to social cogntiion? Converging evidence from DTI and neuropsychology support this contention. a hospital room moved to the patients home) (Politis and Loane, 2012). Orbitofrontal and anterior temporal regions are involved in behavioural variant FTD and psychopathy (Hodges, 2001; Yang et al., 2009; Hornberger et al., 2011; Gregory et al., 2012), whereas amygdala dysfunction has been implicated in autism spectrum disorder (Dalton et al., 2005; Nacewicz et al., 2006; Kleinhans et al., 2009). Tranel D, Damasio H, Damasio AR. Catani M, Mesulam M. The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Hierarchical organization and functional streams in the visual cortex. Hettema JM, Kettenmann B, Ahluwalia V, McCarthy C, Kates WR, Schmitt JE, et al. However, these patients performed normally when naming animals and objects. Klingler J, Gloor P. The connections of the amygdala and of the anterior temporal cortex in the human brain. Parker GJM, Luzzi S, Alexander DC, Wheeler-Kingshott CAM, Ciccarelli O, Lambon Ralph MA. An image of Marilyn Monroe, for example, evokes not only a name but also semantic and emotional associations, such as her performance in the film Gentlemen Prefer Blondes, her extreme version of female sexuality, her relationships with several famous men such as John F. Kennedy and Joe DiMaggio, and her tragic death by drug overdose.


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