Binocular Responses Research Articles

Ocular dominance-dependent binocular combination of monocular neuronal responses in macaque V1

Primates rely on two eyes to perceive depth, while maintaining stable vision when either one eye or both eyes are open. Although psychophysical and modeling studies have investigated how monocular signals are combined to form binocular vision, the underlying neuronal mechanisms, particularly in V1 where most neurons exhibit binocularity with varying eye preferences, remain poorly understood. Here, we used two-photon calcium imaging to compare the monocular and binocular responses of thousands of simultaneously recorded V1 superficial-layer neurons in three awake macaques. During monocular stimulation, neurons preferring the stimulated eye exhibited significantly stronger responses compared to those preferring both eyes. However, during binocular stimulation, the responses of neurons preferring either eye were suppressed on the average, while those preferring both eyes were enhanced, resulting in similar neuronal responses irrespective of their eye preferences, and an overall response level similar to that with monocular viewing. A neuronally realistic model of binocular combination, which incorporates ocular dominance-dependent divisive interocular inhibition and binocular summation, is proposed to account for these findings.

Ocular dominance-dependent binocular combination of monocular neuronal responses in macaque V1.

Primates rely on two eyes to perceive depth, while maintaining stable vision when either one eye or both eyes are open. Although psychophysical and modeling studies have investigated how monocular signals are combined to form binocular vision, the underlying neuronal mechanisms, particularly in V1 where most neurons exhibit binocularity with varying eye preferences, remain poorly understood. Here, we used two-photon calcium imaging to compare the monocular and binocular responses of thousands of simultaneously recorded V1 superficial-layer neurons in three awake macaques. During monocular stimulation, neurons preferring the stimulated eye exhibited significantly stronger responses compared to those preferring both eyes. However, during binocular stimulation, the responses of neurons preferring either eye were suppressed on the average, while those preferring both eyes were enhanced, resulting in similar neuronal responses irrespective of their eye preferences, and an overall response level similar to that with monocular viewing. A neuronally realistic model of binocular combination, which incorporates ocular dominance-dependent divisive interocular inhibition and binocular summation, is proposed to account for these findings.

Structural and Functional Organization of Visual Responses in the Inferior Olive of Larval Zebrafish.

The olivo-cerebellar system plays an important role in vertebrate sensorimotor control. Here, we investigate sensory representations in the inferior olive (IO) of larval zebrafish and their spatial organization. Using single-cell labeling of genetically identified IO neurons, we find that they can be divided into at least two distinct groups based on their spatial location, dendritic morphology, and axonal projection patterns. In the same genetically targeted population, we recorded calcium activity in response to a set of visual stimuli using two-photon imaging. We found that most IO neurons showed direction-selective and binocular responses to visual stimuli and that the functional properties were spatially organized within the IO. Light-sheet functional imaging that allowed for simultaneous activity recordings at the soma and axonal level revealed tight coupling between functional properties, soma location, and axonal projection patterns of IO neurons. Taken together, our results suggest that anatomically defined classes of IO neurons correspond to distinct functional types, and that topographic connections between IO and cerebellum contribute to organization of the cerebellum into distinct functional zones.

Widespread and Multifaceted Binocular Integration in the Mouse Primary Visual Cortex.

The brain combines two-dimensional images received from the two eyes to form a percept of three-dimensional surroundings. This process of binocular integration in the primary visual cortex (V1) serves as a useful model for studying how neural circuits generate emergent properties from multiple input signals. Here, we perform a thorough characterization of binocular integration using electrophysiological recordings in the V1 of awake adult male and female mice by systematically varying the orientation and phase disparity of monocular and binocular stimuli. We reveal widespread binocular integration in mouse V1 and demonstrate that the three commonly studied binocular properties-ocular dominance, interocular matching, and disparity selectivity-are independent of each other. For individual neurons, the responses to monocular stimulation can predict the average amplitude of binocular response but not its selectivity. Finally, the extensive and independent binocular integration of monocular inputs is seen across cortical layers in both regular-spiking and fast-spiking neurons, regardless of stimulus design. Our data indicate that the current model of simple feedforward convergence is inadequate to account for binocular integration in mouse V1, thus suggesting an indispensable role played by intracortical circuits in binocular computation.SIGNIFICANCE STATEMENT Binocular integration is an important step of visual processing that takes place in the visual cortex. Studying the process by which V1 neurons become selective for certain binocular disparities is informative about how neural circuits integrate multiple information streams at a more general level. Here, we systematically characterize binocular integration in mice. Our data demonstrate more widespread and complex binocular integration in mouse V1 than previously reported. Binocular responses cannot be explained by a simple convergence of monocular responses, contrary to the prevailing model of binocular integration. These findings thus indicate that intracortical circuits must be involved in the exquisite computation of binocular disparity, which would endow brain circuits with the plasticity needed for binocular development and processing.

Ocularity-contingent monocular and binocular responses and ocularity functional organizations of V1 superficial-layer neurons in macaques

Ocularity-contingent monocular and binocular responses and ocularity functional organizations of V1 superficial-layer neurons in macaques

Enriched binocular experience followed by sleep optimally restores binocular visual cortical responses in a mouse model of amblyopia

Studies of primary visual cortex have furthered our understanding of amblyopia, long-lasting visual impairment caused by imbalanced input from the two eyes during childhood, which is commonly treated by patching the dominant eye. However, the relative impacts of monocular vs. binocular visual experiences on recovery from amblyopia are unclear. Moreover, while sleep promotes visual cortex plasticity following loss of input from one eye, its role in recovering binocular visual function is unknown. Using monocular deprivation in juvenile male mice to model amblyopia, we compared recovery of cortical neurons’ visual responses after identical-duration, identical-quality binocular or monocular visual experiences. We demonstrate that binocular experience is quantitatively superior in restoring binocular responses in visual cortex neurons. However, this recovery was seen only in freely-sleeping mice; post-experience sleep deprivation prevented functional recovery. Thus, both binocular visual experience and subsequent sleep help to optimally renormalize bV1 responses in a mouse model of amblyopia.

Binocular visual experience drives the maturation of response variability and reliability in the visual cortex

SummaryA fundamental challenge of neuroscience is to understand how a single neuron responds to multiple synaptic inputs effectively and reliably. In primary visual cortex, repeated stimuli to one eye elicit neuronal responses of inherent variability and reliability. However, it remains unclear how this monocular variability and reliability contribute to the establishment of effective and reliable binocular responses and what drives this development. In this study, using in vivo multichannel extracellular recordings, we demonstrate binocular responses in adult mouse visual cortex exhibit low variability and high reliability. This response characteristic is immature during the critical period of binocular vision development. In amblyopic mice, the maturation of binocular variability and reliability is disrupted, and this defect can be partially rescued by enhancing cortical plasticity via dark exposure. In conclusion, the development of cortical response variability and reliability depends on the normal binocular visual experience, which is further regulated by cortical plasticity.

Development of the horizontal optocollic reflex in juvenile barn owls (Tyto furcata pratincola)

Adult barn owls and primates possess an almost symmetric monocular rotational horizontal optocollic reflex. In primates, the reflex is initially asymmetric and becomes symmetric with time after birth. The condition in barn owls has not been studied so far. Here, we present data on the development of this reflex in this bird. We tested juvenile barn owls from the time before they open their eyes after hatching to the time they reach adult feather length. Wide-field visual patterns served as stimuli. They were presented at different rotational speeds in binocular and monocular settings. The binocular horizontal optocollic responses of juvenile barn owls were symmetric and adult-like on the first day that the birds responded to the stimulus. The monocular responses showed different rates of development in respect to stimulus velocity and stimulus direction. For velocities up to 20 deg/s, the monocular reflex was also adult-like on the first day that the birds responded to the stimulus. An initially higher asymmetry for 30 deg/s compared to adults disappeared within about two weeks. The development at even higher velocities remained unclear.

Binocular Integration in the Primate Primary Visual Cortex

binocular vision, binocular fusion, binocular combination, LGN, V1.

Accommodative Lag Persistence in Treated Anisometropic, Strabismic, and Mixed Amblyopia.

Background Amblyopic eyes typically exhibit greater lag of accommodation. Whether this improves after amblyopia treatment is inconclusive. The aim of this study is to report post-treatment accommodative response in amblyopia and to investigate if the lag is associated with visual acuity, treatment duration, and amblyopia type. Methods Monocular and binocular accommodative responses were measured using Nott's method of dynamic retinoscopy in amblyopia of anisometropic, strabismic, and combined anisometropic-strabismic types and age-matched controls with normal vision. The results were compared using the nonparametric Wilcoxon signed ranks test. Linear regression analysis was used to examine association of the lag to refractive error, duration of therapy, and visual acuity. Results Mean ± SD age of 46 amblyopic and 20 control subjects were 6.9 ± 1.8 and 6.9 ± 2.2 years, respectively. At the time of the study, 30 amblyopic subjects were receiving patching therapy and ceased in the remainder. In amblyopic eyes, mean ± SD monocular and binocular lags were 1.2 ± 0.6D and 1.0 ± 0.5D (p < 0.001), respectively, compared to 0.6 ± 0.3D and 0.5 ± 0.2D (p < 0.005), respectively, in nonamblyopic eyes and 0.4 ± 0.2D and 0.3 ± 0.2D (p=0.093), respectively, in the controls. By types, the monocular lag was significantly higher than the binocular lag (p=0.001) in mixed amblyopia (p=0.004); they were similar in anisometropic (p=0.283) and strabismic (p=0.743) amblyopia. Monocular lag was significantly correlated to BCVA (r = 0.46; p=0.001) and refraction (r = 0.42; p=0.001) but not to patching duration (r = 0.1; p=0.280). Conclusion Inadequate accommodative response, a higher lag, persists in amblyopic eyes even after the treatment. Impaired accommodative response is partly determined by posttherapy visual acuity. Further studies investigating the effect of accommodative lag on visual recovery and whether optical correction of the deficiency may improve visual outcome of the treatment are recommended.

Stimulating both eyes with matching stimuli enhances V1 responses

SummaryNeurons in the primary visual cortex (V1) of primates play a key role in combining monocular inputs to form a binocular response. Although much has been gleaned from studying how V1 responds to discrepant (dichoptic) images, equally important is to understand how V1 responds to concordant (dioptic) images in the two eyes. Here, we investigated the extent to which concordant, balanced, zero-disparity binocular stimulation modifies V1 responses to varying stimulus contrast using intracranial multielectrode arrays. On average, binocular stimuli evoked stronger V1 activity than their monocular counterparts. This binocular facilitation scaled most proportionately with contrast during the initial transient. As V1 responses evolved, additional contrast-mediated dynamics emerged. Specifically, responses exhibited longer maintenance of facilitation for lower contrast and binocular suppression at high contrast. These results suggest that V1 processes concordant stimulation of both eyes in at least two sequential steps: initial response enhancement followed by contrast-dependent control of excitation.

The impact of scleral contact lenses correction of keratoconus on wave-front and accommodation parameters

Purpose: to evaluate the wave-front and accommodation changes in various stages of keratoconus corrected by scleral contact lenses.Material and methods. 20 patients (39 eyes) aged 18–37 with keratoconus of various stages (8 eyes with stage I, 3 eyes with stage II, 12 eyes stage II/III and 16 eyes with stage III wore OneFit or OneFitMed scleral lenses, made of hard gas-permeable material Contamac (Great Britain) with Dk 100 and mean thickness of 200–220 μm. All patients were examined using refractometry before and after cycloplegia, tested for uncorrected and best corrected visual acuity, relative accommodation reserve (RAR), binocular and monocular accommodation response (with Grand Seiko Binocular Open Field Autorefkeratometer WR-5100K, Japan) for full spectacle correction and scleral contact lens correction. 17 patients (34 eyes) were tested for corneal aberrations with OPD Scan III aberrometer (Nidek) without correction and with scleral contact lenses.Results. Patients with keratoconus demonstrated a manifest form of refraction -5.26 ± 0.45 D (by sphere equivalent) and a cycloplegic refraction of -4.75 ± 0.33 D. Uncorrected visual acuity averaged 0.26 ± 0.05, increasing with full spectacled correction to 0.54 ± 0.07 and with scleral contact lenses correction to 0.95 ± 0.08. Keratoconus patients demonstrated binocular accommodative response (BAR) of +4.5 to -6.12 D averaging -1.43 ± 0.34 D with full spectacled correction diopters and of -0.5 to -8.13 D averaging - 2.83 ± 0.23 D with scleral contact lenses, р ≤ 0.01. We could not measure the BAR in 3 patients with keratoconus stage III. Monocular accommodative response (MAR)with a full correction with glasses averaged -0.98 ± 0.33 D (from + 6.0 to -5.0 D) with full spectacled correction and -2.41 ± 0.27 D (from +1.25 to -5.5 D) with scleral contact lenses, р ≤ 0.02. At the same time monocular accommodative response of 4 patients with keratoconus of the third stage of disease was not available to assess. So, accommodative response significant increased with scleral contact lenses. Positive relative accommodation with a full correction with glasses averaged 1.50 ± 0.35 D, with scleral contact lenses – 2.25 ± 0.29 D, р ≤ 0.01. The level of all aberrations, from lower to higher orders was significantly increased. With scleral contact lenses that correct the shape of the anterior surface of the cornea, the level of all corneal aberrations dropped to nearly normal values, while the coefficient of asphericity dropped below normal values, and the point spread function parameter (PSF) increased by fifteen times (to reach 0.06).Conclusions. Patients with keratoconus demonstrated a generally lower objective accommodative response as compared to normal values, but with the scleral lenses it increases to the normal level. Scleral contact lenses normalize corneal aberrations and increase the quality of vision. All of the above justifies the recommendation to use scleral contact lenses for optical correction of keratoconus to increase the vision, the accommodation response and visual comfort, including that of near-visual work.

The Development of Receptive Field Tuning Properties in Mouse Binocular Primary Visual Cortex.

The mouse primary visual cortex is a model system for understanding the relationship between cortical structure, function, and behavior (Seabrook et al., 2017; Chaplin and Margrie, 2020; Hooks and Chen, 2020; Saleem, 2020; Flossmann and Rochefort, 2021). Binocular neurons in V1 are the cellular basis of binocular vision, which is required for predation (Scholl et al., 2013; Hoy et al., 2016; La Chioma et al., 2020; Berson, 2021; Johnson et al., 2021). The normal development of binocular responses, however, has not been systematically measured. Here, we measure tuning properties of neurons to either eye in awake mice of either sex from eye opening to the closure of the critical period. At eye opening, we find an adult-like fraction of neurons responding to the contralateral-eye stimulation, which are selective for orientation and spatial frequency; few neurons respond to ipsilateral eye, and their tuning is immature. Fraction of ipsilateral-eye responses increases rapidly in the first few days after eye opening and more slowly thereafter, reaching adult levels by critical period closure. Tuning of these responses improves with a similar time course. The development and tuning of binocular responses parallel that of ipsilateral-eye responses. Four days after eye opening, monocular neurons respond to a full range of orientations but become more biased to cardinal orientations. Binocular responses, by contrast, lose their cardinal bias with age. Together, these data provide an in-depth accounting of the development of monocular and binocular responses in the binocular region of mouse V1 using a consistent set of visual stimuli and measurements.SIGNIFICANCE STATEMENT In this manuscript, we present a full accounting of the emergence and refinement of monocular and binocular receptive field tuning properties of thousands of pyramidal neurons in mouse primary visual cortex. Our data reveal new features of monocular and binocular development that revise current models on the emergence of cortical binocularity. Given the recent interest in visually guided behaviors in mice that require binocular vision (e.g., predation), our measures will provide the basis for studies on the emergence of the neural circuitry guiding these behaviors.

A binocular synaptic network supports interocular response alignment in visual cortical neurons

In visual cortex, signals from the two eyes merge to form a coherent binocular representation. Here we investigate the synaptic interactions underlying the binocular representation of stimulus orientation in ferret visual cortex with invivo calcium imaging of layer 2/3 neurons and their dendritic spines. Individual neurons with aligned somatic responses received a mixture of monocular and binocular synaptic inputs. Surprisingly, monocular pathways alone could not account for somatic alignment because ipsilateral monocular inputs poorly matched somatic preference. Binocular inputs exhibited different degrees of interocular alignment, and those with a high degree of alignment (congruent) had greater selectivity and somatic specificity. While congruent inputs were similar to others in measures of strength, simulations show that the number of active congruent inputs predicts aligned somatic output. Our study suggests that coherent binocular responses derive from connectivity biases that support functional amplification of aligned signals within a heterogeneous binocular intracortical network.

Contributed Session III: A Surprisingly Simple Neural-Based Relationship Predicts Binocular Facilitation

Two eyes are better than one - but not by much. Most binocular facilitation models incorporate incomplete binocular summation (e.g., the Minkowski equation). One complication is that the Minkowski exponent for binocular facilitation varies with spatial frequency. We find that a simple alternative models both psychophysical and neural data without taking spatial frequency into account. There are cortical neurons that only fire for one eye, but amplify their firing rates if both eyes are stimulated (Dougherty, 2019). We find that binocular amplification for these monocular neurons follows a power law, with a compressive exponent of 0.84 (r=0.96), remarkably close to power law multisensory interactions (Billock & Havig, 2018). Next, we modeled the relationship between the dominant eye's firing rate and the binocular firing rate in binocular V1 facilitatory neurons. Unexpectedly, the same rule also applies to cortical facilitatory binocular neurons (exponent=0.87, r=0.97); binocular neurons can be approximated as gated amplifiers of dominant monocular responses, if both eyes are stimulated. Finally, the same power law models binocular facilitation of contrast sensitivity in Winterbottom (2016) and our unpublished psychophysical data (pooled data's exponent is 0.89; r=0.98); binocular response is a gated amplification of the more sensitive eye. This unexpected result fits with growing evidence that non-driving modulatory neural interactions affect sensory processing.

Vision-dependent specification of cell types and function in the developing cortex

The role of postnatal experience in sculpting cortical circuitry, while long appreciated, is poorly understood at the level of cell types. We explore this in the mouse primary visual cortex (V1) using single-nucleus RNA sequencing, visual deprivation, genetics, and functional imaging. We find that vision selectively drives the specification of glutamatergic cell types in upper layers (L) (L2/3/4), while deeper-layer glutamatergic, GABAergic, and non-neuronal cell types are established prior to eye opening. L2/3 cell types form an experience-dependent spatial continuum defined by the graded expression of ∼200 genes, including regulators of cell adhesion and synapse formation. One of these genes, Igsf9b, a vision-dependent gene encoding an inhibitory synaptic cell adhesion molecule, is required for the normal development of binocular responses in L2/3. In summary, vision preferentially regulates the development of upper-layer glutamatergic cell types through the regulation of cell-type-specific gene expression programs.

Quantification of Pupillary Dynamics and Accommodative Response in Adie’s Tonic Pupil: A Case Report

Background: Objective quantification of pupillary dynamics in a clinical setting is of worth importance to rule out any pupillary abnormalities. However, despite normal binocular vision findings, a quantitative measurement of pupillary response and accommodation provides a better insight to understand the mechanism. Case Report: This case report illustrates the clinical presentation, binocular vision parameters, Pupillary dynamics and accommodative response in a 33-year-old diagnosed with Adie’s Tonic pupil following trauma. Conclusion: This report explains the role of the pupillometer and open field autorefractor in quantitative analysis of pupillary and accommodative function.

Binocular integration of retinal motion information underlies optic flow processing by the cortex

SummaryLocomotion creates various patterns of optic flow on the retina, which provide the observer with information about their movement relative to the environment. However, it is unclear how these optic flow patterns are encoded by the cortex. Here, we use two-photon calcium imaging in awake mice to systematically map monocular and binocular responses to horizontal motion in four areas of the visual cortex. We find that neurons selective to translational or rotational optic flow are abundant in higher visual areas, whereas neurons suppressed by binocular motion are more common in the primary visual cortex. Disruption of retinal direction selectivity in Frmd7 mutant mice reduces the number of translation-selective neurons in the primary visual cortex and translation- and rotation-selective neurons as well as binocular direction-selective neurons in the rostrolateral and anterior visual cortex, blurring the functional distinction between primary and higher visual areas. Thus, optic flow representations in specific areas of the visual cortex rely on binocular integration of motion information from the retina.

The Effect of Myopia and Hyperopic Anisometropia to Binocular Accommodative Response

Purpose : The purpose of this study was to measure binocular accommodative response when hyperopic and myopic anisometropia were induced on non-dominatn eye.Methods : Twenty participants (mean age: 24.05±1.73) who had corrected visual acuity more than 0.0 logMAR and no eye disease or systemic disease were recruited. The contact lenses with +1.00, +2.00, -1.00, -2.00 D were monocularly worn on non-dominant eye. The accommodative responses were measured by a binocular open-field autorefractometer when participant fixates target (accommodative stimulus) at 300, 40, and 20 cm.Results : As the accommodative stimulus distance decreased, the amount of accommodative response increased in both eyes (p<0.050). There was significant difference of accommodative responses by different degree of anisometropia (p<0.050). When –2.00 D hyperopic anisometropia was induced, both eyes showed the highest accommodative responses at 40 cm (dominant eye 1.50±0.11 D, non dominant-eye 1.71±0.09 D). When comparing accommodative responses by the type of anisometropia, there was a significant differences in both the dominant and nondominant eyes at 20 cm when inducing 1.00 and 2.00 D in myopic and hyperopic anisometropia (p<0.050). At 40 cm, there was a significant differences in both the dominant and non-dominant eyes when inducing 1.00 in myopic and hyperopic anisometropia (p<0.050). In addition it showed that the higher the degree of myopia and hyperopia, the higher the difference in accommodative response on both eyes and the difference was significant between 40 and 20 cm (p<0.050).Conclusion : There is a difference in the amount of accommodative response between dominant and non-dominant eye when anisometropia was induced. Regardless of the type, the environment that causes the difference in the amount of accommodative response between both eyes causes eye fatigue, so to prevent such a situation, not only the examination on accommodative response of both eyes, but also regular and continuous management is necessary. Also, a prescription for glasses and addition considering the difference between the two eyes is required.

Comparative Analysis of the Wave Front Aberrations and Ophthalmoergonomic Parameters after Excimer Laser and Orthokeratological Correction of Myopia in Patients over 35 Years

Purpose. Comparative analysis of the wavefront aberrations and ophthalmoergonomic parameters after excimer laser and orthokeratological correction of myopia in patients aged over 35 years.Patients and methods. The study included 21 patients: 12 (24 eyes) after excimer laser correction of myopia (group 1) and 9 (18 eyes) after orthokeratology (group 2). The average age of patients after excimer laser surgery was 38.5 years, after orthokeratological correction 46.1 years. Special studies included ophthalmoergonomical tests: far and near distance visual acuity, capacity of the visual analyzer, visual productivity, reading velocity, mesopic vision, relative accommodation reserves, objective accommodative response, pseudo-accommodation volume. Wavefront aberrations were conducted on the OPD-scan 3.Results. The spherical equivalent of residual refraction was –0.625 ± 0.08D in the excimer group, and –1.58 ± 0.24D in orthokeratological group. Despite the difference in refraction, values of distance binocular and monocular visual acuity were the same in both groups: in group 1 monocular visual acuity was 0.74 ± 0.03, binocular 0.85 ± 0.03; in group 2 — 0.71 ± 0.06 and 0.89 ± 0.05 respectively. The parameters of both monocular and binocular accommodative response measured on Grand Seiko were 50 % higher in the excimer group compared to those in the orthokeratological group. Relative accommodation reserves appeared to be two times more in the excimer group. The volume of pseudo-accommodation was 2.375 ± 0.12D in group 1, which appeared to be 20 % more than in the group 2 (p = 0.0414). The level of wavefront aberrations was significantly higher in orthokeratological group with the exception of vertical aberrations and, especially horizontal coma, which were significantly higher after excimer laser surgery. Generally, the dynamics of aberrations in both groups correlates with changes of the corneal topography.Conclusion. Excimer laser surgery with hypocorrection is more recommended for patients aged 35–40, and orthokeratological correction for patients over 45 years old.