Shared Mechanisms Drive Ocular Following and Motion Perception.

How features of complex visual patterns are combined to drive perception and eye movements is not well understood. Here we simultaneously assessed human observers' perceptual direction estimates and ocular following responses (OFR) evoked by moving plaids made from two summed gratings with varying contrast ratios. When the gratings were of equal contrast, observers' eye movements and perceptual reports followed the motion of the plaid pattern. However, when the contrasts were unequal, eye movements and reports during early phases of the OFR were biased toward the direction of the high-contrast grating component; during later phases, both responses followed the plaid pattern direction. The shift from component- to pattern-driven behavior resembles the shift in tuning seen under similar conditions in neuronal responses recorded from monkey MT. Moreover, for some conditions, pattern tracking and perceptual reports were correlated on a trial-by-trial basis. The OFR may therefore provide a precise behavioral readout of the dynamics of neural motion integration for complex visual patterns.

Shared mechanisms drive ocular following and motion perception.

How features of complex visual patterns combine to drive perception and eye movements is not well understood. We simultaneously assessed human observers' perceptual direction estimates and ocular following responses (OFR) evoked by moving plaids made from two summed gratings with varying contrast ratios. When the gratings were of equal contrast, observers' eye movements and perceptual reports followed the motion of the plaid pattern. However, when the contrasts were unequal, eye movements and reports during early phases of the OFR were biased toward the direction of the high-contrast grating component; during later phases, both responses more closely followed the plaid pattern direction. The shift from component- to pattern-driven behavior resembles the shift in tuning seen under similar conditions in neuronal responses recorded from monkey MT. Moreover, for some conditions, pattern tracking and perceptual reports were correlated on a trial-by-trial basis. The OFR may therefore provide a precise behavioural read-out of the dynamics of neural motion integration for complex visual patterns.

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.

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 eye's 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.

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.

Temporal and spatial limits of pattern motion sensitivity in macaque MT neurons.

Many neurons in visual cortical area MT signal the direction of motion of complex visual patterns, such as plaids composed of two superimposed drifting gratings. To compute the direction of pattern motion, MT neurons combine component motion signals over time and space. To determine the spatial and temporal limits of signal integration, we measured the responses of single MT neurons to a novel set of "pseudoplaid" stimuli in which the component gratings were alternated in time or space. As the temporal or spatial separation of the component gratings increased, neuronal selectivity for the direction of pattern motion decreased. Using descriptive models of signal integration, we inferred the temporal and spatial structure of the mechanisms that compute pattern direction selectivity. The median time constant for integration was roughly 10 ms, a timescale characteristic of integration by single cortical pyramidal neurons. The median spatial integration field was roughly one-third of the MT receptive field diameter, suggesting that the spatial limits are set by stages of processing in earlier areas of visual cortex where receptive fields are smaller than in MT. Interestingly, pattern direction-selective neurons had shorter temporal integration times than component direction-selective neurons but similar spatial integration windows. We conclude that pattern motion can only be signaled by MT neurons when the component motion signals co-occur within relatively narrow spatial and temporal limits. We interpret these results in the framework of recent hierarchical models of MT.

Visual response properties of V1 neurons projecting to V2 in macaque.

Visual area V2 of the primate cortex receives the largest projection from area V1. V2 is thought to use its striate inputs as the basis for computations that are important for visual form processing, such as signaling angles, object borders, illusory contours, and relative binocular disparity. However, it remains unclear how selectivity for these stimulus properties emerges in V2, in part because the functional properties of the inputs are unknown. We used antidromic electrical stimulation to identify V1 neurons that project directly to V2 (10% of all V1 neurons recorded) and characterized their electrical and visual responses. V2-projecting neurons were concentrated in the superficial and middle layers of striate cortex, consistent with the known anatomy of this cortico-cortical circuit. Most were fast conducting and temporally precise in their electrical responses, and had broad spike waveforms consistent with pyramidal regular-spiking excitatory neurons. Overall, projection neurons were functionally diverse. Most, however, were tuned for orientation and binocular disparity and were strongly suppressed by large stimuli. Projection neurons included those selective and invariant to spatial phase, with roughly equal proportions. Projection neurons found in superficial layers had longer conduction times, broader spike waveforms, and were more responsive to chromatic stimuli; those found in middle layers were more strongly selective for motion direction and binocular disparity. Collectively, these response properties may be well suited for generating complex feature selectivity in and beyond V2.

Cellular mechanisms of temporal sensitivity in visual cortex neurons.

The ability of cortical neurons to accurately encode the temporal pattern of their inputs has important consequences for cortical function and perceptual acuity. Here we identify cellular mechanisms underlying the sensitivity of cortical neurons to the timing of sensory-evoked synaptic inputs. We find that temporally coincident inputs to layer 4 neurons in primary visual cortex evoke an increase in spike precision and supralinear spike summation. Underlying this nonlinear summation are changes in the evoked excitatory conductance and the associated membrane potential response, and a lengthening of the window between excitation and inhibition. Furthermore, fast-spiking inhibitory interneurons in layer 4 exhibit a shorter window of temporal sensitivity compared with excitatory neurons. In contrast to the enhanced response to synchronous inputs by layer 4 neurons, sensory input integration in downstream cortical layers is more linear and less sensitive to timing. Neurons in the input layer of cortex are thus uniquely optimized to detect and encode synchronous sensory-evoked inputs.

Precision, reliability, and information-theoretic analysis of visual thalamocortical neurons.

High-order statistics of neural responses allow one to gain insight into neural function that may not be evident from firing rate alone. In this study, we compared the precision, reliability, and information content of spike trains from X- and Y-cells in the lateral geniculate nucleus (LGN) and layer IV simple cells of area 17 in the cat. To a stochastic, contrast-modulated Gabor patch, layer IV simple cells responded as precisely as their primary inputs, LGN X-cells, but less reliably. LGN Y-cells were more precise and reliable than LGN X-cells. Also, within each LGN cell type, 1) responses to the same stimulus were nearly identical if they shared the same center sign and 2) responses of neurons with the same center sign were nearly identical to the responses of neurons of opposite center sign if the stimulus' contrasts were inverted. These results suggest simple cells receive highly precise and synchronous LGN input, resulting in precise responses. Nonetheless, the response precision of simple cells was greater than expected. Finally, information-theoretic calculations of our cell responses revealed that 1) LGN X-cells encoded information at half the rate of LGN Y-cells but 2.5 times the rate of layer IV simple cells; 2) LGN cells encoded information in their responses using temporal patterns, whereas simple cells did not; and 3) simple cells used more of their information capacity than LGN X-cells. We propose mechanisms that simple cells might use to ensure high precision.