Neuroscience Letters 578 (2014) 66–70
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Neural connectivity of the lateral geniculate body in the human brain: Diffusion tensor imaging study Hyeok Gyu Kwon, Sung Ho Jang ∗ Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, 317-1, Daemyung dong, Namku, Daegu 705-717, Republic of Korea
h i g h l i g h t s • • • •
Neural connectivity of the lateral geniculate body (LGB). LGB provides a relay station for all axons of retinal ganglion cells. LGB was connected with the contralateral target areas via the corpus callosum. LGB showed high connectivity with the ipsilateral hemisphere: temporal lobe, V1.
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Article history: Received 11 December 2013 Received in revised form 3 June 2014 Accepted 13 June 2014 Available online 23 June 2014 Keywords: Diffusion tensor imaging Neural connectivity Lateral geniculate body Corpus callosum Visual system
a b s t r a c t A few studies have reported on the neural connectivity of some neural structures of the visual system in the human brain. However, little is known about the neural connectivity of the lateral geniculate body (LGB). In the current study, using diffusion tensor tractography (DTT), we attempted to investigate the neural connectivity of the LGB in normal subjects. A total of 52 healthy subjects were recruited for this study. A seed region of interest was placed on the LGB using the FMRIB Software Library which is a probabilistic tractography method based on a multi-ﬁber model. Connectivity was deﬁned as the incidence of connection between the LGB and target brain areas at the threshold of 5, 25, and 50 streamlines. In addition, connectivity represented the percentage of connection in all hemispheres of 52 subjects. We found the following characteristics of connectivity of the LGB at the threshold of 5 streamline: (1) high connectivity to the corpus callosum (91.3%) and the contralateral temporal cortex (56.7%) via the corpus callosum, (2) high connectivity to the ipsilateral cerebral cortex: the temporal lobe (100%), primary visual cortex (95.2%), and visual association cortex (77.9%). The LGB appeared to have high connectivity to the corpus callosum and both temporal cortexes as well as the ipsilateral occipital cortex. We believe that the results of this study would be helpful in investigation of the neural network associated with the visual system and brain plasticity of the visual system after brain injury. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction The visual system is a complex neural system comprising various neural structures, including the retino-geniculo-striate visual pathway, visual processing system, and ocular motor system [1,6,8,16,28]. The visual system is known to have the characteristic of high potential in brain plasticity [9,15,23,30,38]. Unmasking of a latent neural connection is an important mechanism of brain plasticity following brain injury and many studies have reported on this topic in patients with brain injury [2,3]. Therefore,
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(S.H. Jang). http://dx.doi.org/10.1016/j.neulet.2014.06.033 0304-3940/© 2014 Elsevier Ireland Ltd. All rights reserved.
elucidation of the neural connectivity of a neural structure is important in research on normal visual function and brain plasticity of the visual system following brain injury. Many studies have reported on the neural connectivity of the visual system in both animal and human brain using various techniques including the post-mortem, electromyography, transcranial magnetic stimulation, and functional MRI [7,20,25,31,32,34–36]. However, these techniques have a common limitation in that three-dimensional visualization and localization of neural tract. Recently developed diffusion tensor imaging (DTI) enables evaluation of the integrity of white matter tracts in three-dimensional by virtue of its ability to image water diffusion characteristics . In addition, diffusion tensor tractography (DTT), which is derived from DTI, has an advantage for research on the neural connectivity of a neural structure. Therefore, many studies have reported on the
H.G. Kwon, S.H. Jang / Neuroscience Letters 578 (2014) 66–70
neural connectivity of the neural system for motor and memory function in the human brain [14,17,42,43]. Regarding the visual system, a few studies have reported on neural connectivity of some portions of the visual system, such as the pulvinar and superior colliculus in the normal human brain [22–24]. The classic retino-geniculo-striate visual pathway, which terminates in the primary visual cortex (V1, the striate cortex), is associated with visual discrimination and perception [1,6]. The lateral geniculate body (LGB) provides a relay station for all axons of retinal ganglion cells and is connected to the V1 through the optic radiation . The LGB is also connected to the pretectal area, superior colliculus, and pulvinar, which are important in visual attention and eye movement [6,7,24,33]. In addition, the LGB is known to be connected to the parietal and temporal lobes for unconscious vision (blindsight) . Therefore, the LGB has been suggested to have an important role in brain plasticity of the visual system following brain injury [15,19,25]. However, little is known about the neural connectivity of the LGB in the human brain. In the current study, using DTT, we attempted to investigate the neural connectivity of the LGB in normal subjects.
and applied in the current study utilizing tractography routines implemented in FMRIB Diffusion (5000 streamline samples, 0.5 mm step lengths, curvature thresholds = 0.2) [4,5,37]. We used two regions of interest (ROIs) in order to elucidate the connectivity of the LGB. For the seed ROI, we reconstructed the optic radiation on each hemisphere and we then identiﬁed and drew the LGB, which could clearly be seen, in accordance with known anatomical location on the FA map with axial slice [27,31,40]. The second ROI was drawn on the midline of the posterior part of the occipital lobe in order to exclude the possibility of inexistent connectivity between hemispheres. Out of 5000 samples generated from a seed voxel, results were visualized at the threshold of 5, 25, and 50 streamlines through each voxel for analysis. Connectivity represented the percentage of connection in all hemispheres of 52 subjects. 2.4. Determination of connection between the LGB and target brain areas Connectivity was deﬁned as the incidence of connection between the LGB and target brain areas: the parietal cortex (Brodmann areas 5, 7, 39, 40), prefrontal cortex (Brodmann area 9, 10, 11, 12), V1 (Brodmann area 17), visual association cortex (Brodmann area 18, 19), temporal cortex (Brodmann area 20, 21, 22, 27, 28, 34, 35, 36, 37) corpus callosum, anterior commissure, and posterior commissure [10,11].
2. Methods 2.1. Subjects We recruited 52 healthy subjects (males: 29, females: 23, mean age: 32.1 years, range: 20–55 years) with no previous history of neurological, physical, or psychiatric illness. All subjects understood the purpose of the study and provided written, informed consent prior to participation. The study protocol was approved by the Institutional Review Board of a university hospital.
3. Results A summary of the connectivity of the LGB is shown in Table 1. Regarding the ipsilateral hemisphere at the threshold of 5, 25, and 50 streamlines, the LGB showed connectivity with the target ROI, in order, to the temporal cortex (100%, 100%, and 100%), V1 (95.2%, 86.5%, and 80.8%), corpus callosum (91.3%, 76%, and 67.3%), visual association cortex (77.9%, 64.4%, and 62.5%), prefrontal cortex (59.6%, 41.3%, and 35.6%), parietal cortex (46.2%, 25%, and 19.2%), posterior commissure (45.2%, 38.5%, and 29.8), and anterior commissure (43.3%, 22.1%, and 17.3), respectively (Fig. 1). A summary of the connectivity between the LGB and contralateral target brain areas is shown in Table 2. The LGB was found to be connected with the contralateral target areas via three kinds of passage structures (the corpus callosum, anterior connissure, and posterior commissure). First, the LGB was connected with the contralateral target brain areas via the corpus callosum at the threshold of 5, 25, and 50 streamlines—to the temporal cortex (56.7%, 26.9%, and 15.4%), visual association cortex (32.7%, 11.5%, and 6.7%), parietal cortex (28.9%, 4.8%, and 4.8%), V1 (26.9%, 11.5%, and 6.7%), prefrontal cortex (10.6%, 1.9%, and 1.9%), and posterior commissure (8.7%, 1.9, and 0.9%), respectively. Second, via the posterior commissure at the threshold of 5, 25, and 50 streamlines, it was found to be connected with the temporal cortex (16.4%, 4.8%, and 1.9%), corpus callosum (4.8%, 2.9%, and 0%), V1 (2.9%, 0.9%, and 0%), parietal cortex (0.9%, 0%, and 0%), and visual association cortex (0.9%, 0%, and 0%), respectively. However, regarding the anterior commissure, the LGB did not show any connectivity with the contralateral target
2.2. Data acquisition A 6-channel head coil on a 1.5 T Philips Gyroscan Intera (Philips, Ltd, Best, The Netherlands) with single-shot echoplanar imaging (EPI) was used for acquisition of DTI data. For each of the 32 non-collinear, diffusion-sensitizing gradients, we acquired 67 contiguous slices parallel to the anterior commissureposterior commissure line. Imaging parameters were as follows: acquisition matrix = 96 × 96; reconstructed matrix = 128 × 128; ﬁeld of view = 221 × 221 mm2 ; TR = 10,726 ms; TE = 76 ms; parallel imaging reduction factor (SENSE factor) = 2; EPI factor = 49; b = 1000 s/mm2 ; NEX = 1; and a slice thickness of 2.3 mm (acquired voxel size 1.73 × 1.73 × 2.3 mm3 ). 2.3. Probabilistic ﬁber tracking Analysis of diffusion-weighted imaging data was performed using the Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB) Software Library (FSL; www.fmrib.ox.ac.uk/fsl). Head motion effect and image distortion due to eddy current were corrected by afﬁne multi-scale twodimensional registration. Fiber tracking was performed using a probabilistic tractography method based on a multi-ﬁber model, Table 1 Incidence of connectivity between the lateral geniculate body and target areas. th
5 25 50
46.2 25 19.2
28.9 4.8 4.8
59.6 41.3 35.6
Primary visual cortex
Visual association cortex
10.6 1.9 1.9
95.2 86.5 80.8
28.9 12.5 6.7
77.9 64.4 62.5
32.7 11.5 6.7
100 100 100
61.5 26.9 16.3
91.3 76 67.3
43.3 22.1 17.3
45.2 38.5 29.8
Connectivity (%), Ant. Com: anterior commissure, Post. Com: posterior commissure, th: threshold, I: ipsilateral, C: contralateral.
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Fig. 1. (A) The regions of interest (ROIs) are drawn at the portion of lateral geniculate body (LGB) as the seed ROI on the b0 and FA map with the axial slice and the midline of the posterior part of the occipital lobe as the exclusion ROI on the coronal slice. (B) Results for neural connectivity between the LGB and the target brain areas. Frequency of connectivity (red [low] to yellow [high]) (C) LGB showed connectivity with the contralateral target brain areas via three kinds of passage areas at a threshold of 5, 25, and 50. Corpus callosum (green): LGB connected with the contralateral target areas via the corpus callosum at a threshold of 5, 25, and 50. Anterior commissure (red): LGB connected with the contralateral target areas via the anterior commissure at a threshold of 5, 25, and 50. Posterior commissure (sky–blue): LGB connected with the contralateral target areas via the posterior commissure at a threshold of 5, 25, and 50. ROI: region of interest for the LGB. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of this article.)
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Table 2 Incidence of connectivity between the lateral geniculate body and the contralateral target areas through passage areas. Passage areas
Primary visual cortex
Visual association cortex
5 25 50 5 25 50 5 25 50
28.9 4.8 4.8 0 0 0 0.9 0 0
10.6 1.9 1.9 0 0 0 0 0 0
26.9 11.5 6.7 0 0 0 2.9 0.9 0
32.7 11.5 6.7 0 0 0 0.9 0 0
56.7 26.9 15.4 2.8 0 0 16.4 4.8 1.9
– – – 0 0 0 4.8 2.9 0
0 0 0 – – – 0 0 0
8.7 1.9 0.9 0 0 0 – – –
Connectivity (%), th: threshold.
brain areas, except for the temporal cortex (2.8%) at the threshold 5 streamline. 4. Discussion In the current study, using probabilistic tracking, we investigated neural connectivity of the LGB in the normal human brain. We found the following characteristics of connectivity of the LGB (the threshold of 5 streamline): (1) high connectivity with the corpus callosum (91.3%) and the contralateral temporal cortex (56.7%) via the corpus callosum, (2) high connectivity with the ipsilateral cerebral cortex: the temporal lobe (100%), V1 (95.2%), and the visual association cortex (77.9%). The high connectivity with the corpus callosum and the contralateral temporal cortex via the corpus callosum appears to be related to the high potential of brain plasticity in the visual system [9,12,30,34,35]. Many studies have reported that the corpus callosum connects both occipital lobes and callosal connections represent a major pathway in induction of plastic rearrangements in the visual cortex [12,30]. Some studies have demonstrated that the abnormal neural pathway to the human motion area (MT+/V5: middle temporal visual area) through the corpus callosum after V1 injury could be attributed to recovery of visual function [9,34,35]. Bridge et al. demonstrated two abnormal neural connections that were not observed in normal control subjects in a blindsight patient who had a left V1 injury due to a trafﬁc accident: a contralateral pathway from the right (contra-lesional) LGB to the left MT+/V5, and a cortico-cortical connection between bilateral MT+/V5 through the corpus callosum . Subsequently, using transcranial magnetic stimulation, Silvanto et al. reported the same results as those reported by Bridge’s for the same patient with left V1 injury . During the same year, Larsen et al. found that connectivity of the contralateral V1 via corpus callosum in visual impaired mice as well as normal mice using trace-injections technique . The classic geniculo-striate visual pathway, which terminates in the V1, is associated with identiﬁcation of objects; in contrast, the visual processing system (the parietal and temporal lobe) involves analysis of motion, form, and color of a subject [1,6]. Neurons of the LGB are known to have a strong connection with the temporal lobe (MT+/V5) as well as the occipital cortex [15,36]. On the other hand, the parietal and temporal lobes have been reported to have a signiﬁcant role in unconscious vision after injury of the geniculostriatal pathway [15,23,39]. Leh et al. demonstrated change of subcortical structure in two patients with attention blindsight after hemispherectomy . They reconstructed the neural tracts from the superior colliculus and found that the patients showed ipsi- and contralateral connections from the superior colliculus to visual association areas, primary visual areas, parietal areas, and prefrontal areas, and to the posterior part of the internal capsule, whereas the control subjects showed mainly ipsilateral connections to visual association areas, parietal cortex, prefrontal
areas, and an area close to the frontal eye ﬁeld. Subsequently, Stoerig and Cowey (1997) reported two patients with temporoparietal lesion who showed strong activation of the contralesional striate cortex without activation of the ipsilesional striate cortex using fMRI . Based on animal studies, Guzzetta et al. suggested a possible mechanism of functional reorganization for unconscious vision in patients with congenital brain damage . The most likely explanation for the striking residual visual capacities after V1 injury is the expansion of pathways that can bypass V1 and connect directly with subcortical nuclei with extrastriate visual structures . During the same year, Schmid et al. investigated the LGB of two monkeys with chronic V1 lesion using fMRI. They demonstrated that the LGB has major role in V1-independent visual function after V1 lesion and directly projects to the extrastriate cortex which is bypass V1 which contributes to the blindsight . Direct connections exist from the LGB to the extrastriate visual structures for both ventral and dorsal streams. In addition, the network connecting the superior colliculus with the pulvinar and the extrastriate cortex is massively expansive, especially to dorsal stream areas such as V5 or middle temporal/middle superior temporal areas. Consequently, we believe that our results show that the high connectivity to the ipsi- and contralateral temporal lobes of the LGB might be related to unconscious vision. To the best of our knowledge, since introduction of DTI, three studies have reported on the neural connectivity of the visual system in the normal human brain [22–24]. Leh et al. reported that the superior colliculus was connected to the ipsilateral visual association areas, parieto-occipital cortex, frontal eye ﬁeld, and prefrontal areas as well as bilateral frontal eye ﬁeld in six normal subjects . Subsequently, Leh et al. demonstrated interconnection of the human pulvinar with subcortical structures (superior colliculus, thalamus, and caudate nucleus) as well as with cortical regions (the V1 and visual association cortex), visual inferotemporal areas (area 20), posterior parietal association areas (area 7), and frontal eye ﬁelds and prefrontal areas in six normal subjects . Maleki et al. demonstrated the neural connectivity of the pulvinar with some other cortical areas, including the primary and secondary auditory cortex, gustatory cortex, and insular cortex in nine normal subjects . As a result, this is the ﬁrst study to demonstrate neural connectivity of the LGB in normal subjects. In conclusion, we investigated the neural connectivity of the LGB in normal subjects and found that the LGB had high connectivity to the corpus callosum and both temporal cortexes as well as the ipsilateral occipital cortex. We believe that the results of this study would be helpful in investigation of the neural network associated with the visual system and brain plasticity of the visual system after brain injury. However, limitations of DTI must be considered [13,18,21,29,41]. DTI, powerful anatomic imaging tool, can demonstrate gross ﬁber architecture. However, DTI can lead to false negative results due to crossing ﬁber or partial volume effect in the white matter of brain, or false positive results; in particular, probabilistic ﬁber tracking based on the multi-tensor model can
H.G. Kwon, S.H. Jang / Neuroscience Letters 578 (2014) 66–70
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