A clinico-anatomical dissection of the magnocellular and parvocellular pathways in a patient with the Riddoch syndrome.

KEY MESSAGE: The Riddoch syndrome is thought to be caused by damage to the primary visual cortex (V1), usually following a vascular event. This study shows that damage to the anatomical input to V1, i.e., the optic radiations, can result in selective visual deficits that mimic the Riddoch syndrome. The results also highlight the differential susceptibility of the magnocellular and parvocellular visual systems to injury. Overall, this study offers new insights that will improve our understanding of the impact of brain injury and neurosurgery on the visual pathways. The Riddoch syndrome, characterised by the ability to perceive, consciously, moving visual stimuli but not static ones, has been associated with lesions of primary visual cortex (V1). We present here the case of patient YL who, after a tumour resection surgery that spared his V1, nevertheless showed symptoms of the Riddoch syndrome. Based on our testing, we postulated that the magnocellular (M) and parvocellular (P) inputs to his V1 may be differentially affected. In a first experiment, YL was presented with static and moving checkerboards in his blind field while undergoing multimodal magnetic resonance imaging (MRI), including structural, functional, and diffusion, acquired at 3 T. In a second experiment, we assessed YL's neural responses to M and P visual stimuli using psychophysics and high-resolution fMRI acquired at 7 T. YL's optic radiations were partially damaged but not severed. We found extensive activity in his visual cortex for moving, but not static, visual stimuli, while our psychophysical tests revealed that only low-spatial frequency moving checkerboards were perceived. High-resolution fMRI revealed strong responses in YL's V1 to M stimuli and very weak ones to P stimuli, indicating a functional P lesion affecting V1. In addition, YL frequently reported seeing moving stimuli and discriminating their direction of motion in the absence of visual stimulation, suggesting that he was experiencing visual hallucinations. Overall, this study highlights the possibility of a selective loss of P inputs to V1 resulting in the Riddoch syndrome and in hallucinations of visual motion.

Rapid white matter changes in children with conduct problems during a parenting intervention.

Studies report that the microstructural integrity of the uncinate fasciculus (UF; connecting the anterior temporal lobe to the orbitofrontal cortex) is abnormal in adults with psychopathy and children with conduct problems (CP), especially those with high callous-unemotional (CU) traits. However, it is unknown if these abnormalities are 'fixed' or 'reversible'. Therefore, we tested the hypothesis that a reduction in CP symptoms, following a parenting intervention, would be associated with altered microstructural integrity in the UF. Using diffusion tensor imaging tractography we studied microstructural differences (mean diffusivity (MD) and radial diffusivity (RD)) in the UF of 43 typically developing (TD) and 67 boys with CP before and after a 14-week parenting intervention. We also assessed whether clinical response in CP symptoms or CU traits explained changes in microstructure following the intervention. Prior to intervention, measures of MD and RD in the UF were increased in CP compared to TD boys. Following intervention, we found that the CP group had a significant reduction in RD and MD. Further, these microstructural changes were driven by the group of children whose CU traits improved (but not CP symptoms as hypothesized). No significant microstructural changes were observed in the TD group. Our findings suggest, for the first time, that microstructural abnormalities in the brains of children with CP may be reversible following parenting intervention.

Neural patterns of conscious visual awareness in the Riddoch syndrome.

The Riddoch syndrome is one in which patients blinded by lesions to their primary visual cortex can consciously perceive visual motion in their blind field, an ability that correlates with activity in motion area V5. Our assessment of the characteristics of this syndrome in patient ST, using multimodal MRI, showed that: 1. ST's V5 is intact, receives direct subcortical input, and decodable neural patterns emerge in it only during the conscious perception of visual motion; 2. moving stimuli activate medial visual areas but, unless associated with decodable V5 activity, they remain unperceived; 3. ST's high confidence ratings when discriminating motion at chance levels, is associated with inferior frontal gyrus activity. Finally, we report that ST's Riddoch Syndrome results in hallucinatory motion with hippocampal activity as a correlate. Our results shed new light on perceptual experiences associated with this syndrome and on the neural determinants of conscious visual experience.

The neural determinants of abstract beauty.

We have enquired into the neural activity which correlates with the experience of beauty aroused by abstract paintings consisting of arbitrary assemblies of lines and colours. During the brain imaging experiments, subjects rated abstract paintings according to aesthetic appeal. There was low agreement on the aesthetic classification of these paintings among participants. Univariate analyses revealed higher activity with higher declared aesthetic appeal in both the visual areas and the medial frontal cortex. Additionally, representational similarity analysis (RSA) revealed that the experience of beauty correlated with decodable patterns of activity in visual areas. These results are broadly similar to those obtained in previous studies on facial beauty. With abstract art, it was the involvement of visual areas implicated in the processing of lines and colours while with faces it was of visual areas implicated in the processing of faces. Both categories of aesthetic experience correlated with increased activity in medial frontal cortex. We conclude that the sensory areas participate in the selection of stimuli according to aesthetic appeal and that it is the co-operative activity between the sensory areas and the medial frontal cortex that is the basis for the experience of abstract visual beauty. Further, this co-operation is enabled by "experience dependent" functional connections, in the sense that currently the existence and high specificity of these connections can only be demonstrated during certain experiences.

A Prospective Study of the Impact of Severe Childhood Deprivation on Brain White Matter in Adult Adoptees: Widespread Localized Reductions in Volume But Unaffected Microstructural Organization.

Early childhood neglect can impact brain development across the lifespan. Using voxel-based approaches we recently reported that severe and time-limited institutional deprivation in early childhood was linked to substantial reductions in total brain volume in adulthood, >20 years later. Here, we extend this analysis to explore deprivation-related regional white matter volume and microstructural organization using diffusion-based techniques. A combination of tensor-based morphometry (TBM) analysis and tractography was conducted on diffusion-weighted imaging (DWI) data from 59 young adults who spent between 3 and 41 months in the severely depriving Romanian institutions of the 1980s before being adopted into United Kingdom families, and 20 nondeprived age-matched United Kingdom controls. Independent of total volume, institutional deprivation was associated with smaller volumes in localized regions across a range of white matter tracts including (1) long-ranging association fibers such as bilateral inferior longitudinal fasciculus (ILF), bilateral inferior fronto-occipital fasciculus (IFOF), left superior longitudinal fasciculi (SLFs), and left arcuate fasciculus; (2) tracts of the limbic circuitry including fornix and cingulum; and (3) projection fibers with the corticospinal tract particularly affected. Tractographic analysis found no evidence of altered microstructural organization of any tract in terms of hindrance modulated orientational anisotropy (HMOA), fractional anisotropy (FA), or mean diffusivity (MD). We provide further evidence for the effects of early neglect on brain development and their persistence in adulthood despite many years of environmental enrichment associated with successful adoption. Localized white matter effects appear limited to volumetric changes with microstructural organization unaffected.

Simultaneous Motor and Visual Intraoperative Neuromonitoring in Asleep Parietal Lobe Surgery: Dual Strip Technique.

Background: The role played by the non-dominant parietal lobe in motor cognition, attention and spatial awareness networks has potentiated the use of awake surgery. When this is not feasible, asleep monitoring and mapping techniques should be used to achieve an onco-functional balance. Objective: This study aims to assess the feasibility of a dual-strip method to obtain direct cortical stimulation for continuous real-time cortical monitoring and subcortical mapping of motor and visual pathways simultaneously in parietal lobe tumour surgery. Methods: Single-centre prospective study between 19 May−20 November of patients with intrinsic non-dominant parietal-lobe tumours. Two subdural strips were used to simultaneously map and monitor motor and visual pathways. Results: Fifteen patients were included. With regards to motor function, a large proportion of patients had abnormal interhemispheric resting motor threshold ratio (iRMTr) (71.4%), abnormal Cortical Excitability Score (CES) (85.7%), close distance to the corticospinal tract­Lesion-To-Tract Distance (LTD)­4.2 mm, Cavity-To-Tract Distance (CTD)­7 mm and intraoperative subcortical distance­6.4 mm. Concerning visual function, the LTD and CTD for optic radiations (OR) were 0.5 mm and 3.4 mm, respectively; the mean intensity for positive subcortical stimulation of OR was 12 mA ± 2.3 mA and 5/6 patients with deterioration of VEPs > 50% had persistent hemianopia and transgression of ORs. Twelve patients remained stable, one patient had a de-novo transitory hemiparesis, and two showed improvements in motor symptoms. A higher iRMTr for lower limbs was related with a worse motor outcome (p = 0.013) and a longer CTD to OR was directly related with a better visual outcome (p = 0.041). At 2 weeks after hospital discharge, all patients were ambulatory at home, and all proceeded to have oncological treatment. Conclusion: We propose motor and visual function boundaries for asleep surgery of intrinsic non-dominant parietal tumours. Pre-operative abnormal cortical excitability of the motor cortex, deterioration of the VEP recordings and CTD < 2 mm from the OR were related to poorer outcomes.

The medial occipital longitudinal tract supports early stage encoding of visuospatial information.

Visuospatial learning depends on the parahippocampal place area (PPA), a functionally heterogenous area which current visuospatial processing models place downstream from parietal cortex and only from area V4 of early visual cortex (EVC). However, evidence for anatomical connections between the PPA and other EVC areas is inconsistent, and these connections are not discussed in current models. Through a data-driven analysis based on diffusion MRI tractography, we present evidence that the PPA sits at the confluence of two white matter systems. The first conveys information from the retrosplenial complex to the anterior PPA and runs within the cingulum bundle. The second system connects all peripheral EVC areas to the posterior PPA and corresponds to the medial occipital longitudinal tract (MOLT), a white matter pathway that is distinct from the cingulum and that we describe here in detail. Based on further functional connectivity analysis and meta-analytic data, we propose that the MOLT supports early stage encoding of visuospatial information by allowing direct reciprocal exchange between the PPA and EVC. Our findings may improve symptom interpretation in stroke and tumour patients with damage to the medial occipito-temporal region and call for revisiting current visuospatial processing models.

Medial-tonsillar telovelar approach for resection of a superior medullary velum cerebral cavernous malformation: anatomical and tractography study of the surgical approach and functional implications.

BACKGROUND: Superior medullary velum cerebral cavernous malformations pose a challenge in terms of appropriate microsurgical approach. Safe access to this deep location as well as preservation of surrounding anatomical structures, in particular the superior cerebellar peduncle just lateral to the superior medullary velum and the dentate nuclei, is paramount to achieve a good functional outcome. METHODS: Cadaveric dissections provide useful knowledge of the normal anatomy while tractography allows a better understanding of the individual anatomy in the presence of a lesion. The medial-tonsillar telovelar approach provides a feasible corridor for accessing superior velum cerebral cavernous malformations without compromising the fibres contained in the superior cerebellar peduncle. The major cerebellar efferents-cerebello-rubral, cerebello-thalamic and cerebello-vestibular tracts-and afferents, anterior spinocerebellar, tectocerebellar and trigeminocerebellar tracts, within the superior cerebellar peduncle are preserved, and the dentate nuclei are not affected. RESULTS AND CONCLUSION: A retraction-free exposure through this natural posterior fossa corridor allows the patient with the anatomical and functional subtract to make a good functional recovery by minimizing the risk of a superior cerebellar syndrome, ataxia, tremor and dysmetria; decomposition of movement in the ipsilateral extremities, nystagmus and hypotonia; or akinetic mutism, reduced or absent speech with onset within the first post-operative week.

Altered corticospinal microstructure and motor cortex excitability in gliomas: an advanced tractography and transcranial magnetic stimulation study.

OBJECTIVE: This prospective case-control study was conducted to examine whether spherical deconvolution (SD) can unveil microstructural abnormalities in the corticospinal tract (CST) caused by IDH-mutant gliomas. To determine the significance of abnormal microstructure, the authors investigated the correlation between diffusion parameters and neurophysiological data collected with navigated transcranial magnetic stimulation (nTMS). METHODS: Twenty participants (10 patients and 10 healthy controls) were recruited. Diffusion-weighted images were acquired on a 3-T MRI scanner using a cardiac-gated single-shot spin echo echo-planar imaging multiband sequence (TE 80 msec, TR 4000 msec) along 90 diffusion directions with a b-value of 2500 sec/mm2 (FOV 256 × 256 mm). Diffusion tensor imaging tractography and SD tractography were performed with deterministic tracking. The anterior portion of the ipsilateral superior peduncle and the precentral gyrus were used as regions of interest to delineate the CST. Diffusion indices were extracted and analyzed for significant differences between hemispheres in patients and between patient and control groups. A navigated brain stimulation system was used to deliver TMS pulses at hotspots at which motor evoked potentials (MEPs) for the abductor pollicis brevis, first digital interosseous, and abductor digiti minimi muscles are best elicited in patients and healthy controls. Functional measurements such as resting motor threshold (rMT), amplitude of MEPs, and latency of MEPs were noted. Significant differences between hemispheres in patients and between patients and controls were statistically analyzed. The Spearman rank correlation was used to investigate correlations between diffusion indices and functional measurements. RESULTS: The hindrance modulated orientational anisotropy (HMOA), measured with SD tractography, is lower in the hemisphere ipsilateral to glioma (p = 0.028). The rMT in the hemisphere ipsilateral to a glioma is significantly greater than that in the contralateral hemisphere (p = 0.038). All measurements contralateral to the glioma, except for the mean amplitude of MEPs (p = 0.001), are similar to those of healthy controls. Mean diffusivity and axial diffusivity from SD tractography are positively correlated with rMT in the hemisphere ipsilateral to glioma (p = 0.02 and 0.006, respectively). The interhemispheric difference in HMOA and rMT is correlated in glioma patients (p = 0.007). CONCLUSIONS: SD tractography can demonstrate microstructural abnormality within the CST of patients with IDH1-mutant gliomas that correlates to the functional abnormality measured with nTMS.

Frontoparietal Tracts Linked to Lateralized Hand Preference and Manual Specialization.

Humans show a preference for using the right hand over the left for tasks and activities of everyday life. While experimental work in non-human primates has identified the neural systems responsible for reaching and grasping, the neural basis of lateralized motor behavior in humans remains elusive. The advent of diffusion imaging tractography for studying connectional anatomy in the living human brain provides the possibility of understanding the relationship between hemispheric asymmetry, hand preference, and manual specialization. In this study, diffusion tractography was used to demonstrate an interaction between hand preference and the asymmetry of frontoparietal tracts, specifically the dorsal branch of the superior longitudinal fasciculus, responsible for visuospatial integration and motor planning. This is in contrast to the corticospinal tract and the superior cerebellar peduncle, for which asymmetry was not related to hand preference. Asymmetry of the dorsal frontoparietal tract was also highly correlated with the degree of lateralization in tasks requiring visuospatial integration and fine motor control. These results suggest a common anatomical substrate for hand preference and lateralized manual specialization in frontoparietal tracts important for visuomotor processing.

Short parietal lobe connections of the human and monkey brain.

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.