Jenna Kelly

Right hemifield deficits in judging simultaneity: a perceptual learning study.

Prior reports demonstrate that simultaneity is judged less precisely in the right visual field (RVF) than in the left visual field (LVF). The present psychophysical study was conducted to provide new information about why and when (i.e., the visual information stage at which) RVF deficits arise in simultaneity judgments. In Experiment 1, participants judged either the simultaneity or the relative spatial frequency of Gabor targets in the right or left hemifield while distractors were randomly absent or present. When attention was not needed to exclude distractors, signal detection theory analyses revealed an RVF simultaneity deficit with an error pattern that implicates low RVF temporal acuity, not excessive RVF neural noise. Adding attentionally demanding distractors introduced a separate, significant RVF simultaneity deficit with error patterns that implicate the inappropriate integration of temporal asynchronies from distractor locations. Neither the distractor-independent RVF acuity deficit nor the distractor-induced RVF excessive spatial integration occurred for spatial frequency discrimination at the same retinal locations. In Experiment 2, a perceptual learning procedure significantly improved RVF simultaneity judgments. The learning was task-specific but generalized to the untrained (left) visual field and to novel retinal locations. This observation implicates the simultaneity decision as the visual information stage that sets the limit on performance.

Bilateral attentional advantage on elementary visual tasks

We examined interactions between and within the left and right visual hemifields using elementary visual tasks. Each trial required identifying a letter at fixation and then either discriminating the orientation of (experiment 1) or detecting (experiment 2) peripheral Gabor targets. On half the trials Gabor distracters were presented between the Gabor targets, and were either restricted to one lateral hemifield (unilateral condition) or presented across the left and right hemifields (bilateral condition). Orientation discrimination and detection each exhibited bilateral superiority only when distracters were present. The results confirm bilateral superiority in attentional selection, even on these most elementary visual tasks.

Population representation of visual information in areas V1 and V2 of amblyopic macaques

Amblyopia is a developmental disorder resulting in poor vision in one eye. The mechanism by which input to the affected eye is prevented from reaching the level of awareness remains poorly understood. We recorded simultaneously from large populations of neurons in the supragranular layers of areas V1 and V2 in 6 macaques that were made amblyopic by rearing with artificial strabismus or anisometropia, and 1 normally reared control. In agreement with previous reports, we found that cortical neuronal signals driven through the amblyopic eyes were reduced, and that cortical neurons were on average more strongly driven by the non-amblyopic than by the amblyopic eyes. We analyzed multiunit recordings using standard population decoding methods, and found that visual signals from the amblyopic eye, while weakened, were not degraded enough to explain the behavioral deficits. Thus additional losses must arise in downstream processing. We tested the idea that under monocular viewing conditions, only signals from neurons dominated by - rather than driven by - the open eye might be used. This reduces the proportion of neuronal signals available from the amblyopic eye, and amplifies the interocular difference observed at the level of single neurons. We conclude that amblyopia might arise in part from degradation in the neuronal signals from the amblyopic eye, and in part from a reduction in the number of signals processed by downstream areas.

Asymmetric dichoptic masking in visual cortex of amblyopic macaque monkeys

In amblyopia, abnormal visual experience leads to an extreme form of eye dominance, in which vision through the nondominant eye is degraded. A key aspect of this disorder is perceptual suppression: the image seen by the stronger eye often dominates during binocular viewing, blocking the image of the weaker eye from reaching awareness. Interocular suppression is the focus of ongoing work aimed at understanding and treating amblyopia, yet its physiological basis remains unknown. We measured binocular interactions in visual cortex of anesthetized amblyopic monkeys (female Macaca nemestrina), using 96-channel “Utah” arrays to record from populations of neurons in V1 and V2. In an experiment reported recently (Hallum et al., 2017), we found that reduced excitatory input from the amblyopic eye (AE) revealed a form of balanced binocular suppression that is unaltered in amblyopia. Here, we report on the modulation of the gain of excitatory signals from the AE by signals from its dominant fellow eye (FE). Using a dichoptic masking technique, we found that AE responses to grating stimuli were attenuated by the presentation of a noise mask to the FE, as in a normal control animal. Responses to FE stimuli, by contrast, could not be masked from the AE. We conclude that a weakened ability of the amblyopic eye to modulate cortical response gain creates an imbalance of suppression that favors the dominant eye. SIGNIFICANCE STATEMENT In amblyopia, vision in one eye is impaired as a result of abnormal early visual experience. Behavioral observations in humans with amblyopia suggest that much of their visual loss is due to active suppression of their amblyopic eye. Here we describe experiments in which we studied binocular interactions in macaques with experimentally induced amblyopia. In normal monkeys, the gain of neuronal response to stimulation of one eye is modulated by contrast in the other eye, but in monkeys with amblyopia the balance of gain modulation is altered so that the weaker, amblyopic eye has little effect while the stronger fellow eye has a strong effect. This asymmetric suppression may be a key component of the perceptual losses in amblyopia.

Attentional oblique effect when judging simultaneity.

We extended the investigation of the oblique effect in two novel ways: from stimulus-driven vision to visual attention and from space to time. Participants fixated the center of briefly flashed displays that contained a temporally varying Gabor stimulus in each of the four peripheral quadrants. Across trial blocks, we manipulated which two of the four peripheral stimuli were to be selected for a simultaneity judgment. Simultaneity judgments were significantly worse for obliquely (diagonally) attended targets than for cardinally (horizontally or vertically) attended targets, despite identical retinal stimulation across all attentional conditions. The impairment in judging the simultaneity of obliquely attended targets occurred between and within lateral hemifields, despite significantly greater temporal acuity for the left hemifield. The oblique effect in simultaneity judgments disappeared when the same targets were presented without temporally varying stimuli at distractor locations-a finding that implicates selective attention. Intriguingly, the oblique effect in excluding stimuli at distractor locations also disappeared when participants viewed the original displays but attended to spatial frequency rather than to simultaneity. These findings raise the possibility of different spatial integration windows when attending to spatial versus temporal features, even when those features are co-presented in space and time.

Altered Balance of Receptive Field Excitation and Suppression in Visual Cortex of Amblyopic Macaque Monkeys

In amblyopia, a visual disorder caused by abnormal visual experience during development, the amblyopic eye (AE) loses visual sensitivity whereas the fellow eye (FE) is largely unaffected. Binocular vision in amblyopes is often disrupted by interocular suppression. We used 96-electrode arrays to record neurons and neuronal groups in areas V1 and V2 of six female macaque monkeys (Macaca nemestrina) made amblyopic by artificial strabismus or anisometropia in early life, as well as two visually normal female controls. To measure suppressive binocular interactions directly, we recorded neuronal responses to dichoptic stimulation. We stimulated both eyes simultaneously with large sinusoidal gratings, controlling their contrast independently with raised-cosine modulators of different orientations and spatial frequencies. We modeled each eyes receptive field at each cortical site using a difference of Gaussian envelopes and derived estimates of the strength of central excitation and surround suppression. We used these estimates to calculate ocular dominance separately for excitation and suppression. Excitatory drive from the FE dominated amblyopic visual cortex, especially in more severe amblyopes, but suppression from both the FE and AEs was prevalent in all animals. This imbalance created strong interocular suppression in deep amblyopes: increasing contrast in the AE decreased responses at binocular cortical sites. These response patterns reveal mechanisms that likely contribute to the interocular suppression that disrupts vision in amblyopes. SIGNIFICANCE STATEMENT Amblyopia is a developmental visual disorder that alters both monocular vision and binocular interaction. Using microelectrode arrays, we examined binocular interaction in primary visual cortex and V2 of six amblyopic macaque monkeys (Macaca nemestrina) and two visually normal controls. By stimulating the eyes dichoptically, we showed that, in amblyopic cortex, the binocular combination of signals is altered. The excitatory influence of the two eyes is imbalanced to a degree that can be predicted from the severity of amblyopia, whereas suppression from both eyes is prevalent in all animals. This altered balance of excitation and suppression reflects mechanisms that may contribute to the interocular perceptual suppression that disrupts vision in amblyopes.

Major Feedforward Thalamic Input Into Layer 4C of Primary Visual Cortex in Primate

One of the underlying principles of how mammalian circuits are constructed is the relative influence of feedforward to recurrent synaptic drive. It has been dogma in sensory systems that the thalamic feedforward input is relatively weak and that there is a large amplification of the input signal by recurrent feedback. Here we show that in trichromatic primates there is a major feedforward input to layer 4C of primary visual cortex. Using a combination of 3D-electron-microscopy and 3D-confocal imaging of thalamic boutons we found that the average feedforward contribution was about 20% of the total excitatory input in the parvocellular (P) pathway, about 3 times the currently accepted values for primates. In the magnocellular (M) pathway it was around 15%, nearly twice the currently accepted values. New methods showed the total synaptic and cell densities were as much as 150% of currently accepted values. The new estimates of contributions of feedforward synaptic inputs into visual cortex call for a major revision of the design of the canonical cortical circuit.

Densities and Laminar Distributions of Kv3.1b-, PV-, GABA-, and SMI-32-Immunoreactive Neurons in Macaque Area V1

The Kv3.1b potassium channel subunit is associated with narrow spike widths and fast-spiking properties. In macaque primary visual cortex (V1), subsets of neurons have previously been found to be Kv3.1b-immunoreactive (ir) but not parvalbumin (PV)-ir or not GABA-ir, suggesting that they may be both fast-spiking and excitatory. This population includes Meynert cells, the large layer 5/6 pyramidal neurons that are also labeled by the neurofilament antibody SMI-32. In the present study, triple immunofluorescence labeling and confocal microscopy were used to measure the distribution of Kv3.1b-ir, non-PV-ir, non-GABA-ir neurons across cortical depth in V1, and to determine whether, like the Meynert cells, other Kv3.1b-ir excitatory neurons were also SMI-32-ir pyramidal neurons. We found that Kv3.1b-ir, non-PV-ir, non-GABA-ir neurons were most prevalent in the M pathway-associated layers 4 Cα and 4B. GABAergic neurons accounted for a smaller fraction (11%) of the total neuronal population across layers 1-6 than has previously been reported. Of Kv3.1b-ir neurons, PV expression reliably indicated GABA expression. Kv3.1b-ir, non-PV-ir neurons varied in SMI-32 coimmunoreactivity. The results suggest the existence of a heterogeneous population of excitatory neurons in macaque V1 with the potential for sustained high firing rates, and these neurons were particularly abundant in layers 4B and 4 Cα.