VSS, May 13-18

Development

Talk Session: Sunday, May 15, 2022, 10:45 am – 12:30 pm EDT, Talk Room 1
Moderator: Michael Arcaro, Penn

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Talk 1, 10:45 am, 32.11

Mapping anatomical connectivity between visual cortex and the pulvinar in human neonates

Chenjie Song1 (), Michael Arcaro1; 1University of Pennsylvania

The primate pulvinar contains extensive, reciprocal connections with visual cortex. Through this connectivity the pulvinar is thought to regulate communication within and between cortical visual areas and facilitate the processing of low- and high-level visual information (Saalmann & Kastner 2011). Here, we explored the development of these connections in humans. We analyzed diffusion imaging data collected in neonates (37-42w gestation) as part of the developing human connectome project (Bastiani et al. 2019). To identify cortical regions for tracking, we aligned an adult retinotopic atlas (Wang et al. 2015) to each neonate’s native brain. Probabilistic tractography (FSL) was performed between individual retinotopic maps and the pulvinar in accordance with prior analyses in adults (Arcaro et al. 2015). Briefly, an initial tractography analysis was performed to identify the most probable thalamic radiations interconnecting cortical areas and the pulvinar. A second analysis restricted to tracking through these radiations identified voxels in the pulvinar with the largest connectivity values with each cortical map. Data were normalized and aligned to a 40-week neonate template for group-level analyses. For occipital cortical maps, the largest connectivity values were within the ventral lateral pulvinar. Medial to this tracking was a region of the ventral pulvinar that was most strongly connected with motion-sensitive maps TO1&2. For posterior parietal maps the largest connectivity values were within the dorsal pulvinar. Tracking from parietal maps extended to the superior colliculus. Overall, pulvino-cortical tracking in neonates followed the known white matter pathways in adults and the spatial organization of connections within the pulvinar was in good correspondence with the organization previously found in adults (Arcaro et al. 2015). These results indicate that the pulvino-cortical pathways that support visual processing in adults are established in utero. We propose that these connections play an important role in shaping postnatal development across visual cortex.

Talk 2, 11:00 am, 32.12

Neural selectivity for faces in human infants after pandemic lockdown

Tristan Yates1 (), Cameron Ellis2, Nicholas Turk-Browne1,3; 1Yale University, 2Haskins Laboratories, 3Wu Tsai Institute

The role of visual experience in the development of face processing has long been debated. Deprivation studies in non-human primates and studies of adults with congenital blindness have yielded mixed results. Here we pursue a different angle on this question through a serendipitous study that can never be repeated. We rely on a classic fMRI repetition suppression design from adult cognitive neuroscience to study the representation of facial identity in infants. Namely, the adult fusiform face area (FFA) tends to show reduced neural activity when the identity of a face is repeated compared to when a novel identity is presented, suggesting that beyond responding to faces, FFA can tell identities apart. In our study, we showed awake infants short blocks of faces or scenes during fMRI. In half of face blocks, the same identity was repeated multiple times in a row (Repeat); in the other half of face blocks, a matching number of faces were presented but each a unique identity (Novel). As a natural experiment, we happened to collect part of our sample before the COVID-19 pandemic and the rest after the first lockdown in Connecticut was lifted. The resulting sample of 12 infants aged 9–23 months divided equally into pre- and post-lockdown groups that were age-matched and had similar data quantity and quality. The two groups had strikingly different neural responses: pre-lockdown infants showed repetition suppression (Novel > Repeat), whereas post-lockdown infants showed repetition enhancement (Repeat > Novel). This interaction was most pronounced in FFA and for human (vs. sheep) faces. Repetition enhancement in adult fMRI has been observed when repetitions provide an opportunity for additional learning. Thus, we tentatively interpret these findings as consistent with delayed development of neural selectivity to faces, and speculate that it may result from altered experience with faces during the pandemic.

Acknowledgements: NSF GRFP, James S. McDonnell Foundation (https://doi.org/10.37717/2020-1208)

Talk 3, 11:15 am, 32.13

Face perception after prolonged early-onset visual deprivation

Asael Sklar1 (), Yuval Porat1, Ehud Zohary1; 1The Hebrew University of Jerusalem

Humans can accurately tell the age, gender, current emotional state, and direction of gaze of person by a mere glimpse at his face. In normal development, this amazing capacity develops early, within the first year or two. Yet, what happens when early visual experience is lacking? We examined a unique population of Ethiopian children (N=24) who had congenital bilateral cataracts that were surgically removed only in late childhood (Mean age at surgery 10.8 years). These children had extremely poor vision prior to cataract removal (M=0.99 cpd). After the operation, their visual acuity substantially improved (M=5.59 cpd), but the improvement varied considerably. As early as five months after cataract removal, many patients (but not all) were able to distinguish the age (M=85.8% correct, p<0.001 compared to chance level performance) and gender (M=64.0% correct, p=0.005), differentiate between emotional expressions (M=68.9% correct, p<0.001) and select a face with straight-ahead gaze based on head (M=64.6% correct, p<0.001) or eye orientation (M=61.9% correct, P=0.003). Postoperative visual acuity was a major factor explaining the variance in the patients’ performance across these face understanding tasks (r=0.59-0.69 across tasks, all p<0.003), while preoperative was significantly related only to selection of faces with straight-ahead gaze based on head orientation (r=0.59, p=0.005). Crucially, control participants who did the same tasks under severe image blur, matching the conditions experienced by the patients with the poorest visual acuity (i.e., visual acuity = 1 cpd), could perform all the above tasks extremely well (M=87.4%-95.8% correct across tasks, all p<0.001). Thus, sufficient visual acuity is probably required for learning these tasks, but once acquired, useful facial information can be extracted even in conditions when the face is dramatically blurred. We conclude that there is evidence for a critical level of acuity, but not a critical period for the acquisition of social information from faces.

Talk 4, 11:30 am, 32.14

Neurochemical markers of degeneration in the visual cortex after vision loss from Stargardt macular dystrophy

Aislin Sheldon1 (), Jasleen Jolly1,2,3,4, Betina Ip1, William Clarke1, Saad Jbabdi1, Susan Downes2,3, Holly Bridge1; 1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), Wellcome Centre for Integrative Neuroimaging (WIN), Nuffield Department of Clinical Neuroscience, University of Oxford, 2Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neuroscience, University of Oxford, 3Oxford Eye Hospital, Oxford University Hospitals NHS Foundation Trust, 4Vision and Eye Research Institute, Anglia Ruskin University, Cambridge

Stargardt macular dystrophy (STGD1) causes progressive degeneration of the photoreceptors in the retina, predominantly affecting the central macula. A focal region of vision loss in STGD1 is projected into a localised region of the primary visual cortex (V1). There are therapies in development that allow functional restoration of the retina, but it is unclear how the visual cortex will process restored visual input in adulthood. Loss of visual input will influence cortical processing, leading to degeneration that would be reflected in the local chemical environment. This study explores if vision loss from STGD1 affects in vivo neurochemistry by using high resolution Magnetic Resonance Spectroscopy Imaging (MRSI). STGD1 (n=16, mean age 34.0 ± 15.1 SD) were compared to normally sighted controls (n=14, mean age 38.7 ± 14.6 SD). A MRSI slab (resolution = 5x5x15mm, FOV=240x240x15mm) was placed in the occipital lobe. For each participant, neurochemical concentrations relative to total creatine were quantified in voxels constrained within V1 (defined by the Juelich atlas), averaged across voxels, and then compared between groups. The concentrations were then correlated with the extent of disease severity through visual field loss in STGD1 patients. Myo-inositol (a marker for glial cell proliferation) was higher within V1 in STGD1 compared to controls (t(28)=2.69; p=.012) and correlated with the extent of vision loss (higher concentrations related to greater loss; r(17)=-.68; p<.001). Glutamate (marker for neuronal function) (r(22)=.47; p=.022) and NAA (marker for neuronal integrity) (r(12)=.61 ;p=.020) correlated with the extent of vision loss (lower concentrations related to greater loss). These findings show a significant change in neurochemical concentrations related to glial and neuronal integrity in adults with vision loss compared to those without. The capacity for the visual cortex to process restored input should be considered alongside potential visual restoration therapies, as their effectiveness could be hindered by cortical degeneration.

Acknowledgements: With thanks to the Medical Research Council, the Nuffield Department of Clinical Neuroscience and Eurofins Scientific for the funding support.

Talk 5, 11:45 am, 32.15

Stimulus-evoked and endogenous alpha oscillations show a linked dependence on patterned visual experience for development.

Rashi Pant1 (), José Ossandón1, Liesa Stange1, Idris Shareef2,3, Ramesh Kekunnaya2, Brigitte Röder1; 1University of Hamburg, 2LV Prasad Eye Institute, 3University of Nevada, Reno

When stimulated with visual “white noise” stimuli, individuals typically show a characteristic evoked response in the alpha frequency range (8-14 Hz) of the electroencephalogram (EEG). This phenomenon has been hypothesized to indicate the underlying frequency of the visual system. However, the relationship between endogenous and stimulus-evoked alpha oscillations is debated. Endogenous alpha activity is known to crucially depend on patterned visual experience after birth. In order to test whether the same is true of evoked alpha activity, we compared individuals who had received delayed surgery for dense bilateral congenital cataracts (n = 13, Mean duration of visual deprivation = 11.0 (SD = 8.9) years) to typically sighted individuals matched for age (n = 13) on an EEG paradigm adapted from VanRullen and MacDonald (2012). Participants performed a target detection task while observing a central visual stimulus that changed in luminance at frequencies between 0-30 Hz, with equal power at all frequencies. We observed a reduced likelihood of exhibiting an evoked alpha response and an overall decreased amplitude of the evoked alpha response in cataract-reversal individuals compared to sighted individuals. This reduction corresponded with a reduction of the resting state alpha activity in the same cataract-reversal individuals. Together, these findings demonstrate that the development of characteristic alpha activity, both in the evoked response and at rest, requires typical visual input at birth. Further, our results provide empirical evidence from humans in favor of evoked and endogenous visual alpha activity being supported by closely related neural mechanisms and similar developmental trajectories.

Acknowledgements: This project was funded by the German Research Foundation (DFG Ro 2625/10-1) and SFB 936-B1 awarded to Prof. Brigitte Röder. Rashi Pant is supported by a student research fellowship awarded by the Hector Fellow Academy gGmbH

Talk 6, 12:00 pm, 32.16

Differentiating the impact of amblyopia on spatial frequency encoding within human V2/V3 thin and thick stripes

Shahin Nasr1,2,3 (), Bryan Kennedy1,2, Jan Skerswetat4, Nicolas Aycardi4, Amanda Nabasaliza5, Roger B.H. Tootell1,2,3, David G. Hunter5,6, Peter Bex4; 1Massachusetts General Hospital, 2Athinoula A. Martinos Center for Biomedical Imaging, 3Department of Radiology, Harvard Medical School, 4Department of Psychology, Northeastern University, 5Department of Ophthalmology, Boston Children's Hospital, 6Department of Ophthalmology, Harvard Medical School

Spatial frequency (SF) encoding in the human visual system is influenced by amblyopia. Amblyopic individuals struggle with low-contrast, high-SF stimuli, especially when presented monocularly to their amblyopic (suppressed) eye. To assess the neuronal underpinning of this phenomenon, we compared the amblyopia impact on SF preference in V2/V3 thick and thin stripes. These mesoscale sites are known to be involved in SF encoding (Tootell and Nasr, 2017). However, the amblyopia impact on their function remains largely unknown. Six strabismic and five anisometropic (best-corrected visual acuity in the amblyopic eye between 20/60 to 20/300) individuals, aged 19-55 years old, participated in this study. Using high-resolution fMRI (7T; voxel size = 1 mm isotropic), we localized their iso-eccentric (3˚<r<10˚) thin and thick stripes across V2 and V3 (Tootell and Nasr, 2021). Then, we measured the activity within these stripes as subjects were presented with low- vs. high-contrast gratings of 0.1 – 5.8 cycle/deg., monocularly. When high-contrast stimuli were presented, iso-eccentric thin and thick stripes showed a stronger preference for high- and low-SF stimuli, respectively. This difference in SF preference between thin vs. thick stripes is consistent with our previous study in individuals with normal vision (Tootell and Nasr, 2017). For high-contrast stimuli, the activity evoked by stimulation of amblyopic- vs. fellow-eye remained equivalent. When low-contrast stimuli were presented, we found a significantly weaker response to higher (but not lower) SF in both stripes, in the amblyopic- vs. fellow-eye stimulation (p<0.01). In thin (but not thick) stripes, this effect led to a shift in response preference to lower SF values. These effects were detected in both strabismic and anisometropic individuals, ruling out the possibility that they are due to an interocular difference in uncorrected visual acuity. Thus, amblyopia has a stronger impact on low-contrast SF preference of thin (compared to thick) stripes.

Acknowledgements: This work was supported by NIH NEI (grant R01EY030434), and by the MGH/HST Athinoula A. Martinos Center for Biomedical Imaging. Crucial resources were made available by a NIH Shared Instrumentation Grant S10-RR019371.

Talk 7, 12:15 pm, 32.17

Assessing the contribution of eye movements to slow binocular reading in children with amblyopia

Dorsa Mir Norouzi1, Lori Dao2, Cynthia Beauchamp2, David Stager, Jr3, Jeffrey Hunter4, Krista Kelly1,5; 1Retina Foundation of the Southwest, Dallas, TX, 2ABC Eyes Pediatric Ophthalmology, PA, Dallas, TX, 3Pediatric Ophthalmology & Adult Strabismus, PA, Plano, TX, 4Heaton Eye Associates, Tyler, TX, 5UT Southwestern Medical Center, Dallas, TX

Introduction: Previous research has shown a relationship between slow silent reading in amblyopic children and ocular motor dysfunction (i.e., fixation instability, increased forward saccades) during binocular viewing (1,2). Here, we investigated the hypothesis that children with amblyopia will read at a similar speed as controls if the need for inter-word saccades is removed during binocular reading. Methods: Silent reading was assessed during binocular viewing in amblyopic children aged 7-12 years and compared to an age-similar control group. Children silently read grade-appropriate sentences presented in rapid serial visual presentation (RSVP; single word presentation at screen center). Participants were asked a ‘yes/no’ question after each sentence. Words in each sentence had the same exposure time. Exposure time per sentence changed based on a descending adaptive 2 down-1 up staircase method to determine the child’s reading speed threshold in log words per minute (WPM). Results: A total of 16 amblyopic children (mean age±SD=9.6±1.3 years, mean amblyopic eye visual acuity±SD=0.4±0.2 logMAR) and 14 control children (10.1±1.2 years, 0.0±.00 logMAR) were enrolled. During binocular viewing, amblyopic children read slower than age-matched controls (2.6±0.5 log WPM vs 3.0±0.4 log WPM, U=64, p=0.044). Conclusions: Amblyopic children read slower than control children, regardless of whether the text is presented in a fixed location (i.e., RSVP reading) or if the reader has to scan the text in a conventional manner (i.e., paragraph reading). Removing the need for inter-word saccades during silent, binocular reading does not help amblyopic children to read at a similar speed as controls. However, this finding does not rule out a role for other types of ocular motor dysfunction such as fixation instability in slow reading. Other possible factors to slow reading in amblyopia may be crowding and reduced visual span. Slow reading in children with amblyopia may hinder academic success.