VSS, May 13-18

Plasticity

Talk Session: Tuesday, May 17, 2022, 10:45 am – 12:30 pm EDT, Talk Room 2
Moderator: Krystel Huxlin, Rochester

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Talk 1, 10:45 am, 52.21

Attributes of preserved motion discrimination inside perimetrically-blind fields early after V1 damage

Matthew Cavanaugh1 (), Jingyi Yang1, Berkeley Fahrenthold1, Elizabeth Saionz1, Michael Melnick1, Marisa Carrasco2, Duje Tadin1, Krystel Huxlin1; 1University of Rochester, 2New York University

BACKGROUND. Stroke-induced damage to the primary visual cortex (V1) causes immediate loss of luminance sensitivity in the contralateral hemifield when measured by automated perimetry, the clinical gold-standard. Unlike chronic stroke patients (>6 months post-stroke), we recently found (in a small sample) that some subacute patients <3 months post-stroke have preserved conscious motion discrimination within their perimetrically-defined blind-fields. Here, we standardized a method of defining visual preservation and used it to assess its incidence, location inside the blind-field, and quality in 32 subacute patients (23M/9F; mean±SEM: 57±2.3 yrs old) 65±5.3 days post-stroke. METHODS. Monocular Humphrey perimetry was used to identify binocular regions of clinical blindness (luminance sensitivity ≤12dB). Motion discrimination was mapped inside these regions using random dot stimuli (5° diameter, 500ms duration, black dots on mid-grey background). With eye-tracker enforced fixation, we mapped performance, starting at the vertical meridian, then moving laterally into the blind field in 1˚ steps. RESULTS. Preservation, defined as >75% correct performance and measurable direction difference (DD) or integration (DI) thresholds inside the blind-field, was found in 19/32 (~60%) participants. There were no significant differences in age or time since stroke for those with/without preservation. Preserved thresholds averaged 10.7±3.8° (DD) and 35.4±4.6% (DI) – similar to intact-field thresholds. Yet, mean perimetric luminance sensitivity at preserved locations was 2.9±0.3dB—well under the clinical definition of blindness. Preservation extended at least 1.6±0.5° from the nearest blind-field border, and as far as 10.4˚. Because we could not test the entire blind-field, these data may under-estimate preservation. CONCLUSIONS. A majority of subacute participants tested had preserved, near-normal direction discrimination and integration at one or more clinically-defined, blind-field locations. These results suggest a gradual, rather than sudden, loss of conscious motion perception after V1 damage, raising the question of what other visual modalities might show relative initial preservation, and over what time-course.

Acknowledgements: NIH/BEI R01 EY027314 NIH/NEI P30 EY001319 Research to Prevent Blindness (RPB) Foundation

Talk 2, 11:00 am, 52.22

Neurochemistry in hMT+ underlies residual vision in visual loss after stroke

Hanna E. Willis1 (), I. Betina Ip1, Archie Watt1, Saad Jbabdi1, William Clarke1, Matthew R. Cavanaugh2, Krystel R. Huxlin2, Kate E. Watkins4, Marco Tamietto3, Holly Bridge1; 1Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford, United Kingdom, OX3 9DU, 2Flaum Eye Institute and Center for Visual Science, University of Rochester, Rochester, NY 14642, USA, 3Department of Psychology, University of Torino, 10123 Torino, Italy, 4Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom, OX2 6GG

Damage to the primary visual cortex due to a stroke leads to visual loss in the contralateral visual fields. Many patients show spared visual processing abilities in the blind field, which has been linked to preserved activity in ipsilesional hMT+. Although hMT+ is known to be important for residual visual processing, it remains unclear how the functioning of hMT+ facilitates this residual vision. In this study, we explored the relationship between residual vision, fMRI activity and in vivo concentrations of neurotransmitters GABA and glutamate through GABA-edited MR Spectroscopy (MRS) in ipsilesional hMT+. Nineteen participants with visual loss after stroke (6 female; aged 24-74 years; >6 months post-stroke) were recruited. A 2AFC high-contrast Gabor detection task (diameter=5°, stimulus-duration=500ms, stimulus-contrast=50% and 100%; spatial-frequency=1cyl/°, temporal-frequency=10Hz), presented in the perimetrically-defined blind-fields, was used to measure residual vision. Resting MRS was used to quantify GABA+ (GABA+macromolecules) and Glx (glutamate, glutamine and glutathione) relative to creatine (Cr) in voxels (25x25x20mm) in ipsilesional hMT+ and primary motor cortex (M1; control region). Functional MRI was used to calculate percentage BOLD signal change in hMT+ during passive viewing of the high-contrast Gabor stimuli detailed earlier in the perimetrically-defined blind field. Reduced concentrations of GABA+ and Glx in the hMT+ voxel were related to improved performance on the contrast detection task, even when controlling for grey matter volume, age and time since lesion (GABA+: R2=0.41; p=0.012; Glx: R2=0.53; p=0.003). In contrast, there was no relationship between residual vision and BOLD signal in ipsilesional hMT+ (R2=-0.06, p=0.884), or GABA (R2=0.25, p=0.976) and Glx (R2=0.12, p=0.981) in M1. Resting neurochemistry in hMT+ reflects residual vision in patients with stroke-induced visual loss better than visually driven BOLD signals. Decreased inhibitory GABA+ and excitatory Glx levels may reflect a greater capacity for plasticity in these patients, facilitating improved performance, whilst preserving an excitatory-inhibitory balance.

Acknowledgements: The work was funded by the European Research Council, British Medical Associaton Foundation, Medical Research Council UK and a Waverley Scholarship from The Queen’s College, Oxford, UK.

Talk 3, 11:15 am, 52.23

Plasticity of visual cortex following large cortical resections

Tina T. Liu1 (), Michael C. Granovetter2,3,4, Anne Margarette S. Maallo2,3, Jason Z Fu1, Christina Patterson5, Marlene Behrmann2,3; 1Laboratory of Brain and Cognition, National Institutes of Mental Health, NIH, 2Department of Psychology, Carnegie Mellon University, 3Carnegie Mellon Neuroscience Institute, 4School of Medicine, University of Pittsburgh, 5Department of Pediatrics, University of Pittsburgh

The visual word form area (VWFA), typically located in the left ventral occipitotemporal cortex (VOTC), emerges during reading acquisition and interfaces between high-level vision and language. Small lesions in the VWFA in adults result in pure alexia, indicating that this area is necessary for word reading. Paradoxically, large cortical resections in children which include the left VOTC, undertaken for the treatment for pharmaco-resistant epilepsy, do not necessarily lead to reading impairments. To understand the neural and behavioral consequences and the ensuing plasticity of resections encompassing the left or right, anterior or posterior, VOTC, we mapped category-selective activations (face, scene, object, and word) in four right-handed pediatric patients and 26 age-matched controls, and tested their intermediate and high-level vision. We report evidence of VWFA-related plasticity in two patients (SN: M, 12y; TC: F, 13-15y) with cortical resections encompassing the left VOTC: word activations were identified in the right VWFA, right inferior frontal and superior temporal gyrus in both patients . These findings contrast with the topography of left-lateralized word-processing network in two other longitudinal patients with resections in the left anterior VOTC (OT: M, 14y-18y) or in the right posterior VOTC (UD: M, 7-10y) and age-matched controls. Parallel to their functional reorganization of the word-processing network, we uncovered atypical representational structure of the category-selective organization in patients SN and TC. Furthermore, in longitudinal comparisons, competition between face and word representations was observed in the left VOTC in patient UD and in the right VOTC in patient TC. Finally, normal intermediate and higher-order perception was evident in all four patients, attesting to functional plasticity in visual cortex. Together, these findings reveal the sufficiency and reorganization of preserved cortex for normal word processing and provide insights into dynamic functional changes in extrastriate cortical architecture.

Acknowledgements: This research was funded by a grant (R01EY027018) from the National Eye Institute to MB and CP, by a B^2 T32 grant (T32GM081760, NIGMS) to MCG, and by a presidential fellowship from Carnegie Mellon University to TTL.

Talk 4, 11:30 am, 52.24

Short-Term Monocular Deprivation in Adult Humans Alters Functional Brain Connectivity Measured With Ultra-High Field Magnetic Resonance Imaging

Miriam Acquafredda1,2 (), Francesco Scarlatti2, Laura Biagi3, Michela Tosetti3,4, Maria Concetta Morrone2, Paola Binda2; 1University of Florence, Italy, 2University of Pisa,Italy, 3IRCCS Stella Maris, Calambrone, Pisa, Italy, 4IMAGO Center, Pisa, Italy

INTRODUCTION: In adult humans, a brief period of monocular deprivation (patching one eye for two hours) induces a form of homeostatic plasticity. Stimuli in the deprived eye are transiently boosted, shifting ocular dominance (e.g., measured with binocular rivalry) and enhancing responses in visual cortex (measured with EEG or fMRI). We asked whether, above and beyond these changes in response amplitude, monocular deprivation also produces a reorganization of visual processing circuits, which we indexed with fMRI functional connectivity. METHODS: Ultra-high field 7T fMRI EPI sequences were acquired in 18 adult normally sighted participants, before and after application of a translucent patch on the dominant eye for two hours. During the acquisitions, a contrast modulated pattern was shown monocularly to the deprived or non-deprived eye and stimulus related activity was regressed out from the fMRI timeseries; in separate sessions, fMRI signals were also recorded in resting state conditions. We analyzed the correlations of the fMRI signal between a priori defined cortical and subcortical regions of interest. Primary visual cortex V1 was used as “seed” area, from which we extracted a reference timeseries and correlated it with timeseries from the other areas to give an index of functional connectivity. RESULTS: After monocular deprivation, V1 increased its functional connectivity with a set of regions primarily located in the ventral visual stream, but also including motor and somatosensory areas. V1 functional connectivity with the lateral geniculate nucleus, its main thalamic input, was unaffected by deprivation. In contrast, a selective post-deprivation increase in functional connectivity was observed for the adjacent ventral pulvinar. CONCLUSIONS: These results suggest that the effects of short-term monocular deprivation involve a transient reorganization of cortical circuits, including both local circuits and long-range projections. They also suggest that ventral pulvinar plays an important and previously unappreciated role in sustaining visual plasticity through adulthood.

Acknowledgements: European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program, grant n. 801715 (PUPILTRAITS) and n. 832813 (GenPercept); Italian Ministry of University and Research under the PRIN2017 program (grant n. 2017HMH8FA and n. 2017SBCPZY) and FARE-2 (grant SMILY).

Talk 5, 11:45 am, 52.25

How do early blind individuals experience auditory motion?

Woon Ju Park1 (), Ione Fine1; 1Department of Psychology, University of Washington

INTRODUCTION: Previous studies have shown that hMT+, well-known for its non-separable spatiotemporal selectivity for visual motion in sighted individuals, responds to auditory motion following early blindness. However, it is not yet known how this recruitment of hMT+ alters auditory motion processing in early blind individuals. METHODS: A psychophysical reverse correlation paradigm was used to estimate the auditory motion filters in 8 sighted and 8 early blind participants. Participants discriminated the direction of signal motion (left/right; 62.5 °/s). The signal was embedded in broadband noise bursts sampled over a 10x10 grid in space (-/+30 °) and time (0-800 ms). Staircases were used to adjust the signal amplitude. We measured the amplitude thresholds for discriminating the signal and estimated the auditory motion filters by characterizing the influence of spatiotemporal noise on performance. RESULTS: In sighted individuals, in contrast to visual motion, auditory motion discrimination was based on separable filters with broad spatial tuning to opposite hemifields. In early blind individuals, auditory motion discrimination similarly relied on separable filters tuned to opposite hemifields – the recruitment of hMT+ did not result in a qualitative shift in auditory motion processing towards non-separable spatiotemporal tuning. Early blind individuals did show significantly lower amplitude thresholds, with filters that were better tuned to signal onsets/offsets. An ideal observer model assuming broad spatial tuning and separable onset/offset filters predicted better performance than the one based on a non-separable spatiotemporal filter, suggesting that early blind individuals were performing close to optimally, given the poor spatial resolution of auditory input. CONCLUSIONS: The computations underlying auditory motion processing in early blind individuals are not qualitatively altered; instead, the recruitment of hMT+ to extract auditory motion involves significant modification of its normal computational operations to make optimal use of the novel auditory input.

Acknowledgements: Weill Neurohub Postdoctoral Fellowship to WP; NEI R01 EY014645 to IF.

Talk 6, 12:00 pm, 52.26

Motor and visual plasticity interact in adult humans

Izel Sari1 (), Claudia Lunghi1; 1Laboratoire des systèmes perceptifs, Département d’études cognitives, École normale supérieure, PSL University, CNRS, Paris, France.

The adult brain retains plasticity in the motor system, while sensory systems are thought to lose their plastic potential in adulthood. This led to a modular view on neuroplasticity: different brain regions have their own plasticity mechanisms that do not depend or translate on others. However, growing evidence indicates that the adult visual cortex retains a high level of homeostatic plasticity as short-term (2-2.5h) monocular deprivation (MD) shifts ocular dominance in favor of the deprived eye in adult humans (Lunghi et al. 2011). Moreover, visual and motor plasticity share some common neural mechanisms, such as a modulation of GABAergic inhibition (Lunghi, et al. 2015, Stagg et al. 2011). Here, we investigated for the first time the direct interaction between visual and motor plasticity in a group of adult volunteers (N=31) using short-term MD and motor sequence learning (Karni et al. 1995) to elicit each form of plasticity. Motor plasticity was quantified as the reaction time decrease in the finger tapping task, and visual plasticity as the ocular dominance change (measured by binocular rivalry) after 2.5 h of MD. We designed a combined task in which visual and motor plasticity are induced at the same time and compared visual and motor plasticity in this condition to simple tasks in which either form of plasticity was induced on its own. We found that inducing visual and motor plasticity at the same time impairs visual plasticity (F(1,30) = 14.4 , p = 0.001, partial eta-squared = 0.32) while motor plasticity is spared (F(1,30) = 0. 01, p > 0.05, partial eta-squared = 0.0). This interruptive influence of motor plasticity on visual plasticity might reflect a resource allocation problem due to competition for limited metabolic resources. We conclude that neuroplasticity is likely a global, rather than a local mechanism in the brain.

Acknowledgements: This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme and from the French National Research Agency (ANR), and in part from FrontCog grant.

Talk 7, 12:15 pm, 52.27

Visually guided reaching requires early-life experience with an arm, evidence from artificial arm use

Roni Maimon-Mor1 (), Hunter Schone1,2, David Henderson Slater1, A Aldo Faisal4, Tamar Makin1; 1University College London, 2University of Oxford, 3Nuffield Orthopaedic Centre, Oxford, UK, 4Imperial College London

The study of artificial arms provides a unique opportunity to address long-standing questions on visuomotor plasticity and development. Learning to use an artificial arm requires an interplay between vision, sensation, and movement to form the fundamental building blocks of body representation across early life experience. To uncover these processes, we tested how early experience with an artificial or biological arm shapes visually guided reaching behaviour. We did this by testing artificial arm motor-control with and without visual feedback in two adult populations with upper-limb deficiencies: a congenital group – individuals who were born with a partial arm, and an acquired group – who lost their arm following amputation in adulthood. Brain plasticity research teaches us that the earlier we train to acquire new skills (or use a new technology) the better we benefit from this practice as adults. Instead, we found that although the congenital group started using an artificial arm as toddlers, they produced increased error noise and directional errors when reaching with visual feedback, relative to the acquired group who performed similarly to controls. However, the earlier an individual with a congenital limb-difference was fitted with an artificial arm, the better their motor control was. We found no group differences between the amputee and congenital group when reaching without visual feedback. We also found that the group differences in visually guided reaching could not be explained by present artificial-arm use, passive proprioception, or speed-accuracy trade-offs. This suggests that the ability to perform efficient visual-based corrective movements is highly dependent on either biological or artificial arm experience at a very young age, but subsequently, opportunities for visuomotor plasticity become more limited.

Acknowledgements: This work was supported by an ERC Starting Grant (715022 EmbodiedTech), awarded to TRM, who was further funded by a Wellcome Trust Senior Research Fellowship (215575/Z/19/Z). R.O.M.M. is supported by the Clarendon scholarship and University College, Oxford.