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Catani, M., Robertsson, N., Beyh, A., Huynh, V., de Santiago Requejo, F., Howells, H., Barrett, R. L., Aiello, M., Cavaliere, C., Dyrby, T. B., Krug, K., Ptito, M., D'Arceuil, H., Forkel, S. J., & Dell'Acqua, F. (2017). Short parietal lobe connections of the human and monkey brain. Cortex, 97, 339-357. doi:10.1016/j.cortex.2017.10.022.
Abstract
The parietal lobe has a unique place in the human brain. Anatomically, it is at the crossroad between the frontal, occipital, and temporal lobes, thus providing a middle ground for multimodal sensory integration. Functionally, it supports higher cognitive functions that are characteristic of the human species, such as mathematical cognition, semantic and pragmatic aspects of language, and abstract thinking. Despite its importance, a comprehensive comparison of human and simian intraparietal networks is missing.
In this study, we used diffusion imaging tractography to reconstruct the major intralobar parietal tracts in twenty-one datasets acquired in vivo from healthy human subjects and eleven ex vivo datasets from five vervet and six macaque monkeys. Three regions of interest (postcentral gyrus, superior parietal lobule and inferior parietal lobule) were used to identify the tracts. Surface projections were reconstructed for both species and results compared to identify similarities or differences in tract anatomy (i.e., trajectories and cortical projections). In addition, post-mortem dissections were performed in a human brain.
The largest tract identified in both human and monkey brains is a vertical pathway between the superior and inferior parietal lobules. This tract can be divided into an anterior (supramarginal gyrus) and a posterior (angular gyrus) component in both humans and monkey brains. The second prominent intraparietal tract connects the postcentral gyrus to both supramarginal and angular gyri of the inferior parietal lobule in humans but only to the supramarginal gyrus in the monkey brain. The third tract connects the postcentral gyrus to the anterior region of the superior parietal lobule and is more prominent in monkeys compared to humans. Finally, short U-shaped fibres in the medial and lateral aspects of the parietal lobe were identified in both species. A tract connecting the medial parietal cortex to the lateral inferior parietal cortex was observed in the monkey brain only.
Our findings suggest a consistent pattern of intralobar parietal connections between humans and monkeys with some differences for those areas that have cytoarchitectonically distinct features in humans. The overall pattern of intraparietal connectivity supports the special role of the inferior parietal lobule in cognitive functions characteristic of humans. -
Besharati, S., Forkel, S. J., Kopelman, M., Solms, M., Jenkinson, P., & Fotopoulou, A. (2016). Mentalizing the body: Spatial and social cognition in anosognosia for hemiplegia. Brain, 139(3), 971-985. doi:10.1093/brain/awv390.
Abstract
Following right-hemisphere damage, a specific disorder of motor awareness can occur called anosognosia for hemiplegia, i.e. the denial of motor deficits contralateral to a brain lesion. The study of anosognosia can offer unique insights into the neurocognitive basis of awareness. Typically, however, awareness is assessed as a first person judgement and the ability of patients to think about their bodies in more ‘objective’ (third person) terms is not directly assessed. This may be important as right-hemisphere spatial abilities may underlie our ability to take third person perspectives. This possibility was assessed for the first time in the present study. We investigated third person perspective taking using both visuospatial and verbal tasks in right-hemisphere stroke patients with anosognosia ( n = 15) and without anosognosia ( n = 15), as well as neurologically healthy control subjects ( n = 15). The anosognosic group performed worse than both control groups when having to perform the tasks from a third versus a first person perspective. Individual analysis further revealed a classical dissociation between most anosognosic patients and control subjects in mental (but not visuospatial) third person perspective taking abilities. Finally, the severity of unawareness in anosognosia patients was correlated to greater impairments in such third person, mental perspective taking abilities (but not visuospatial perspective taking). In voxel-based lesion mapping we also identified the lesion sites linked with such deficits, including some brain areas previously associated with inhibition, perspective taking and mentalizing, such as the inferior and middle frontal gyri, as well as the supramarginal and superior temporal gyri. These results suggest that neurocognitive deficits in mental perspective taking may contribute to anosognosia and provide novel insights regarding the relation between self-awareness and social cognition. -
Besharati, S., Forkel, S. J., Kopelman, M., Solms, M., Jenkinson, P. M., & Fotopoulou, A. (2014). The affective modulation of motor awareness in anosognosia for hemiplegia: Behavioural and lesion evidence. Cortex, 61, 127-140. doi:10.1016/j.cortex.2014.08.016.
Abstract
The possible role of emotion in anosognosia for hemiplegia (i.e., denial of motor deficits contralateral to a brain lesion), has long been debated between psychodynamic and neurocognitive theories. However, there are only a handful of case studies focussing on this topic, and the precise role of emotion in anosognosia for hemiplegia requires empirical investigation. In the present study, we aimed to investigate how negative and positive emotions influence motor awareness in anosognosia. Positive and negative emotions were induced under carefully-controlled experimental conditions in right-hemisphere stroke patients with anosognosia for hemiplegia (n = 11) and controls with clinically normal awareness (n = 10). Only the negative, emotion induction condition resulted in a significant improvement of motor awareness in anosognosic patients compared to controls; the positive emotion induction did not. Using lesion overlay and voxel-based lesion-symptom mapping approaches, we also investigated the brain lesions associated with the diagnosis of anosognosia, as well as with performance on the experimental task. Anatomical areas that are commonly damaged in AHP included the right-hemisphere motor and sensory cortices, the inferior frontal cortex, and the insula. Additionally, the insula, putamen and anterior periventricular white matter were associated with less awareness change following the negative emotion induction. This study suggests that motor unawareness and the observed lack of negative emotions about one's disabilities cannot be adequately explained by either purely motivational or neurocognitive accounts. Instead, we propose an integrative account in which insular and striatal lesions result in weak interoceptive and motivational signals. These deficits lead to faulty inferences about the self, involving a difficulty to personalise new sensorimotor information, and an abnormal adherence to premorbid beliefs about the body.Additional information
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Forkel, S. J., Thiebaut de Schotten, M., Dell’Acqua, F., Kalra, L., Murphy, D. G. M., Williams, S. C. R., & Catani, M. (2014). Anatomical predictors of aphasia recovery: a tractography study of bilateral perisylvian language networks. Brain, 137, 2027-2039. doi:10.1093/brain/awu113.
Abstract
Stroke-induced aphasia is associated with adverse effects on quality of life and the ability to return to work. For patients and clinicians the possibility of relying on valid predictors of recovery is an important asset in the clinical management of stroke-related impairment. Age, level of education, type and severity of initial symptoms are established predictors of recovery. However, anatomical predictors are still poorly understood. In this prospective longitudinal study, we intended to assess anatomical predictors of recovery derived from diffusion tractography of the perisylvian language networks. Our study focused on the arcuate fasciculus, a language pathway composed of three segments connecting Wernicke’s to Broca’s region (i.e. long segment), Wernicke’s to Geschwind’s region (i.e. posterior segment) and Broca’s to Geschwind’s region (i.e. anterior segment). In our study we were particularly interested in understanding how lateralization of the arcuate fasciculus impacts on severity of symptoms and their recovery. Sixteen patients (10 males; mean age 60 ± 17 years, range 28–87 years) underwent post stroke language assessment with the Revised Western Aphasia Battery and neuroimaging scanning within a fortnight from symptoms onset. Language assessment was repeated at 6 months. Backward elimination analysis identified a subset of predictor variables (age, sex, lesion size) to be introduced to further regression analyses. A hierarchical regression was conducted with the longitudinal aphasia severity as the dependent variable. The first model included the subset of variables as previously defined. The second model additionally introduced the left and right arcuate fasciculus (separate analysis for each segment). Lesion size was identified as the only independent predictor of longitudinal aphasia severity in the left hemisphere [beta = −0.630, t(−3.129), P = 0.011]. For the right hemisphere, age [beta = −0.678, t(–3.087), P = 0.010] and volume of the long segment of the arcuate fasciculus [beta = 0.730, t(2.732), P = 0.020] were predictors of longitudinal aphasia severity. Adding the volume of the right long segment to the first-level model increased the overall predictive power of the model from 28% to 57% [F(1,11) = 7.46, P = 0.02]. These findings suggest that different predictors of recovery are at play in the left and right hemisphere. The right hemisphere language network seems to be important in aphasia recovery after left hemispheric stroke.Additional information
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Forkel, S. J. (2014). Identification of anatomical predictors of language recovery after stroke with diffusion tensor imaging. PhD Thesis, King's College London, London.
Abstract
Background Stroke-induced aphasia is associated with adverse effects on quality of life and the ability to return to work. However, the predictors of recovery are still poorly understood. Anatomical variability of the arcuate fasciculus, connecting Broca’s and Wernicke’s areas, has been reported in the healthy population using diffusion tensor imaging tractography. In about 40% of the population the arcuate fasciculus is bilateral and this pattern is advantageous for certain language related functions, such as auditory verbal learning (Catani et al. 2007). Methods In this prospective longitudinal study, anatomical predictors of post-stroke aphasia recovery were investigated using diffusion tractography and arterial spin labelling. Patients An 18-subject strong aphasia cohort with first-ever unilateral left hemispheric middle cerebral artery infarcts underwent post stroke language (mean 5±5 days) and neuroimaging (mean 10±6 days) assessments and neuropsychological follow-up at six months. Ten of these patients were available for reassessment one year after symptom onset. Aphasia was assessed with the Western Aphasia Battery, which provides a global measure of severity (Aphasia Quotient, AQ). Results Better recover from aphasia was observed in patients with a right arcuate fasciculus [beta=.730, t(2.732), p=.020] (tractography) and increased fractional anisotropy in the right hemisphere (p<0.05) (Tract-based spatial statistics). Further, an increase in left hemisphere perfusion was observed after one year (p<0.01) (perfusion). Lesion analysis identified maximal overlay in the periinsular white matter (WM). Lesion-symptom mapping identified damage to periinsular structure as predictive for overall aphasia severity and damage to frontal lobe white matter as predictive of repetition deficits. Conclusion These findings suggest an important role for the right hemisphere language network in recovery from aphasia after left hemispheric stroke.Additional information
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Forkel, S. J., Thiebaut de Schotten, M., Kawadler, J. M., Dell'Acqua, F., Danek, A., & Catani, M. (2014). The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography. Cortex, 56, 73-84. doi:10.1016/j.cortex.2012.09.005.
Abstract
The occipital and frontal lobes are anatomically distant yet functionally highly integrated to generate some of the most complex behaviour. A series of long associative fibres, such as the fronto-occipital networks, mediate this integration via rapid feed-forward propagation of visual input to anterior frontal regions and direct top–down modulation of early visual processing.
Despite the vast number of anatomical investigations a general consensus on the anatomy of fronto-occipital connections is not forthcoming. For example, in the monkey the existence of a human equivalent of the ‘inferior fronto-occipital fasciculus’ (iFOF) has not been demonstrated. Conversely, a ‘superior fronto-occipital fasciculus’ (sFOF), also referred to as ‘subcallosal bundle’ by some authors, is reported in monkey axonal tracing studies but not in human dissections.
In this study our aim is twofold. First, we use diffusion tractography to delineate the in vivo anatomy of the sFOF and the iFOF in 30 healthy subjects and three acallosal brains. Second, we provide a comprehensive review of the post-mortem and neuroimaging studies of the fronto-occipital connections published over the last two centuries, together with the first integral translation of Onufrowicz's original description of a human fronto-occipital fasciculus (1887) and Muratoff's report of the ‘subcallosal bundle’ in animals (1893).
Our tractography dissections suggest that in the human brain (i) the iFOF is a bilateral association pathway connecting ventro-medial occipital cortex to orbital and polar frontal cortex, (ii) the sFOF overlaps with branches of the superior longitudinal fasciculus (SLF) and probably represents an ‘occipital extension’ of the SLF, (iii) the subcallosal bundle of Muratoff is probably a complex tract encompassing ascending thalamo-frontal and descending fronto-caudate connections and is therefore a projection rather than an associative tract.
In conclusion, our experimental findings and review of the literature suggest that a ventral pathway in humans, namely the iFOF, mediates a direct communication between occipital and frontal lobes. Whether the iFOF represents a unique human pathway awaits further ad hoc investigations in animals. -
Vergani, F., Mahmood, S., Morris, C., Mitchell, P., & Forkel, S. J. (2014). Intralobar fibres of the occipital lobe: A post mortem dissection study. Cortex, 56, 145-156. doi:10.1016/j.cortex.2014.03.002.
Abstract
Introduction
The atlas by Heinrich Sachs (1892) provided an accurate description of the intralobar fibres of the occipital lobe, with a detailed representation of the short associative tracts connecting different parts of the lobe. Little attention has been paid to the work of Sachs since its publication. In this study, we present the results of the dissection of three hemispheres, performed according to the Klingler technique (1935). Our anatomical findings are then compared to the original description of the occipital fibres anatomy as detailed by Sachs.
Methods
Three hemispheres were dissected according to Klingler's technique (1935). Specimens were fixed in 10% formalin and frozen at −15 °C for two weeks. After defreezing, dissection of the white matter fibres was performed with blunt dissectors. Coronal sections were obtained according to the cuts originally described by Sachs. In addition, medial to lateral and lateral to medial dissection of the white matter of the occipital lobe was also performed.
Results
A network of short association fibres was demonstrated in the occipital lobe, comprising intralobar association fibres and U-shaped fibres, which are connecting neighbouring gyri. Lateral to the ventricles, longitudinal fibres of the stratum sagittale were also identified that are arranged as external and internal layers. Fibres of the forceps major were also found to be in direct contact with the ventricular walls. We were able to replicate all tracts originally described by Sachs. In addition, a previously unrecognised tract, connecting the cuneus to the lingual gyrus, was identified. This tract corresponds to the “sledge runner”, described in tractography studies.
Conclusions
The occipital lobe shows a rich network of intralobar fibres, arranged around the ventricular wall. Good concordance was observed between the Klingler dissection technique and the histological preparations of Sachs.
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