Neuronal and Behavioral Responses to Naturalistic Texture Images in Macaque Monkeys.

The visual world is richly adorned with texture, which can serve to delineate important elements of natural scenes. In anesthetized macaque monkeys, selectivity for the statistical features of natural texture is weak in V1, but substantial in V2, suggesting that neuronal activity in V2 might directly support texture perception. To test this, we investigated the relation between single cell activity in macaque V1 and V2 and simultaneously measured behavioral judgments of texture. We generated stimuli along a continuum between naturalistic texture and phase-randomized noise and trained two macaque monkeys to judge whether a sample texture more closely resembled one or the other extreme. Analysis of responses revealed that individual V1 and V2 neurons carried much less information about texture naturalness than behavioral reports. However, the sensitivity of V2 neurons, especially those preferring naturalistic textures, was significantly closer to that of behavior compared with V1. The firing of both V1 and V2 neurons predicted perceptual choices in response to repeated presentations of the same ambiguous stimulus in one monkey, despite low individual neural sensitivity. However, neither population predicted choice in the second monkey. We conclude that neural responses supporting texture perception likely continue to develop downstream of V2. Further, combined with neural data recorded while the same two monkeys performed an orientation discrimination task, our results demonstrate that choice-correlated neural activity in early sensory cortex is unstable across observers and tasks, untethered from neuronal sensitivity, and therefore unlikely to directly reflect the formation of perceptual decisions.

Mixing novel and familiar cues modifies representations of familiar visual images and affects behavior.

While visual responses to familiar and novel stimuli have been extensively studied, it is unknown how neuronal representations of familiar stimuli are affected when they are interleaved with novel images. We examined a large-scale dataset from mice performing a visual go/no-go change detection task. After training with eight images, six novel images were interleaved with two familiar ones. Unexpectedly, we found that the behavioral performance in response to familiar images was impaired when they were mixed with novel images. When familiar images were interleaved with novel ones, the dimensionality of their representation increased, indicating a perturbation of their neuronal responses. Furthermore, responses to familiar images in the primary visual cortex were less predictive of responses in higher-order areas, indicating less efficient communication. Spontaneous correlations between neurons were predictive of responses to novel images, but less so to familiar ones. Our study demonstrates the modification of representations of familiar images by novelty.

Responses to visual motion of neurons in the extrastriate visual cortex of macaque monkeys with experimental amblyopia.

Amblyopia is a developmental disorder that results from abnormal visual experience in early life. Amblyopia typically reduces visual performance in one eye. We studied the representation of visual motion information in area MT and nearby extrastriate visual areas in two monkeys made amblyopic by creating an artificial strabismus in early life, and in a single age-matched control monkey. Tested monocularly, cortical responses to moving dot patterns, gratings, and plaids were qualitatively normal in awake, fixating amblyopic monkeys, with primarily subtle differences between the eyes. However, the number of binocularly driven neurons was substantially lower than normal; of the neurons driven predominantly by one eye, the great majority responded only to stimuli presented to the fellow eye. The small population driven by the amblyopic eye showed reduced coherence sensitivity and a preference for faster speeds in much the same way as behavioral deficits. We conclude that, while we do find important differences between neurons driven by the two eyes, amblyopia does not lead to a large scale reorganization of visual receptive fields in the dorsal stream when tested through the amblyopic eye, but rather creates a substantial shift in eye preference toward the fellow eye.

Developmentally stable representations of naturalistic image structure in macaque visual cortex.

To determine whether post-natal improvements in form vision result from changes in mid-level visual cortex, we studied neuronal and behavioral responses to texture stimuli that were matched in local spectral content but varied in "naturalistic" structure. We made longitudinal measurements of visual behavior from 16 to 95 weeks of age, and of neural responses from 20 to 56 weeks. We also measured behavioral and neural responses in near-adult animals more than 3 years old. Behavioral sensitivity reached half-maximum around 25 weeks of age, but neural sensitivities remained stable through all ages tested. Neural sensitivity to naturalistic structure was highest in V4, lower in V2 and inferotemporal cortex (IT), and barely discernible in V1. Our results show a dissociation between stable neural performance and improving behavioral performance, which may reflect improved processing capacity in circuits downstream of visual cortex.

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.

Development of radial frequency pattern perception in macaque monkeys.

Infant primates see poorly, and most perceptual functions mature steadily beyond early infancy. Behavioral studies on human and macaque infants show that global form perception, as measured by the ability to integrate contour information into a coherent percept, improves dramatically throughout the first several years after birth. However, it is unknown when sensitivity to curvature and shape emerges in early life or how it develops. We studied the development of shape sensitivity in 18 macaques, aged 2 months to 10 years. Using radial frequency stimuli, circular targets whose radii are modulated sinusoidally, we tested monkeys' ability to radial frequency stimuli from circles as a function of the depth and frequency of sinusoidal modulation. We implemented a new four-choice oddity task and compared the resulting data with that from a traditional two-alternative forced choice task. We found that radial frequency pattern perception was measurable at the youngest age tested (2 months). Behavioral performance at all radial frequencies improved with age. Performance was better for higher radial frequencies, suggesting the developing visual system prioritizes processing of fine visual details that are ecologically relevant. By using two complementary methods, we were able to capture a comprehensive developmental trajectory for shape perception.

Brain representations of motion and position in the double-drift illusion.

In the 'double-drift' illusion, local motion within a window moving in the periphery of the visual field alters the window's perceived path. The illusion is strong even when the eyes track a target whose motion matches the window so that the stimulus remains stable on the retina. This implies that the illusion involves the integration of retinal signals with non-retinal eye-movement signals. To identify where in the brain this integration occurs, we measured BOLD fMRI responses in visual cortex while subjects experienced the double-drift illusion. We then used a combination of univariate and multivariate decoding analyses to identify (1) which brain areas were sensitive to the illusion and (2) whether these brain areas contained information about the illusory stimulus trajectory. We identified a number of cortical areas that responded more strongly during the illusion than a control condition that was matched for low-level stimulus properties. Only in area hMT+ was it possible to decode the illusory trajectory. We additionally performed a number of important controls that rule out possible low-level confounds. Concurrent eye tracking confirmed that subjects accurately tracked the moving target; we were unable to decode the illusion trajectory using eye position measurements recorded during fMRI scanning, ruling out explanations based on differences in oculomotor behavior. Our results provide evidence for a perceptual representation in human visual cortex that incorporates extraretinal information.

Neuronal and behavioral responses to naturalistic texture images in macaque monkeys.

The visual world is richly adorned with texture, which can serve to delineate important elements of natural scenes. In anesthetized macaque monkeys, selectivity for the statistical features of natural texture is weak in V1, but substantial in V2, suggesting that neuronal activity in V2 might directly support texture perception. To test this, we investigated the relation between single cell activity in macaque V1 and V2 and simultaneously measured behavioral judgments of texture. We generated stimuli along a continuum between naturalistic texture and phase-randomized noise and trained two macaque monkeys to judge whether a sample texture more closely resembled one or the other extreme. Analysis of responses revealed that individual V1 and V2 neurons carried much less information about texture naturalness than behavioral reports. However, the sensitivity of V2 neurons, especially those preferring naturalistic textures, was significantly closer to that of behavior compared with V1. The firing of both V1 and V2 neurons predicted perceptual choices in response to repeated presentations of the same ambiguous stimulus in one monkey, despite low individual neural sensitivity. However, neither population predicted choice in the second monkey. We conclude that neural responses supporting texture perception likely continue to develop downstream of V2. Further, combined with neural data recorded while the same two monkeys performed an orientation discrimination task, our results demonstrate that choice-correlated neural activity in early sensory cortex is unstable across observers and tasks, untethered from neuronal sensitivity, and thus unlikely to reflect a critical aspect of the formation of perceptual decisions. Significance statement: As visual signals propagate along the cortical hierarchy, they encode increasingly complex aspects of the sensory environment and likely have a more direct relationship with perceptual experience. We replicate and extend previous results from anesthetized monkeys differentiating the selectivity of neurons along the first step in cortical vision from area V1 to V2. However, our results further complicate efforts to establish neural signatures that reveal the relationship between perception and the neuronal activity of sensory populations. We find that choice-correlated activity in V1 and V2 is unstable across different observers and tasks, and also untethered from neuronal sensitivity and other features of nonsensory response modulation.

Developmentally stable representations of naturalistic image structure in macaque visual cortex.

We studied visual development in macaque monkeys using texture stimuli, matched in local spectral content but varying in "naturalistic" structure. In adult monkeys, naturalistic textures preferentially drive neurons in areas V2 and V4, but not V1. We paired behavioral measurements of naturalness sensitivity with separately-obtained neuronal population recordings from neurons in areas V1, V2, V4, and inferotemporal cortex (IT). We made behavioral measurements from 16 weeks of age and physiological measurements as early as 20 weeks, and continued through 56 weeks. Behavioral sensitivity reached half of maximum at roughly 25 weeks of age. Neural sensitivities remained stable from the earliest ages tested. As in adults, neural sensitivity to naturalistic structure increased from V1 to V2 to V4. While sensitivities in V2 and IT were similar, the dimensionality of the IT representation was more similar to V4's than to V2's.

Foundations of visual form selectivity for neurons in macaque V1 and V2.

We have measured the visually evoked activity of single neurons recorded in areas V1 and V2 of awake, fixating macaque monkeys, and captured their responses with a common computational model. We used a stimulus set composed of "droplets" of localized contrast, band-limited in orientation and spatial frequency; each brief stimulus contained a random superposition of droplets presented in and near the mapped receptive field. We accounted for neuronal responses with a 2-layer linear-nonlinear model, representing each receptive field by a combination of orientation- and scale-selective filters. We fit the data by jointly optimizing the model parameters to enforce sparsity and to prevent overfitting. We visualized and interpreted the fits in terms of an "afferent field" of nonlinearly combined inputs, dispersed in the 4 dimensions of space and spatial frequency. The resulting fits generally give a good account of the responses of neurons in both V1 and V2, capturing an average of 40% of the explainable variance in neuronal firing. Moreover, the resulting models predict neuronal responses to image families outside the test set, such as gratings of different orientations and spatial frequencies. Our results offer a common framework for understanding processing in the early visual cortex, and also demonstrate the ways in which the distributions of neuronal responses in V1 and V2 are similar but not identical.

DREDge: robust motion correction for high-density extracellular recordings across species.

High-density microelectrode arrays (MEAs) have opened new possibilities for systems neuroscience in human and non-human animals, but brain tissue motion relative to the array poses a challenge for downstream analyses, particularly in human recordings. We introduce DREDge (Decentralized Registration of Electrophysiology Data), a robust algorithm which is well suited for the registration of noisy, nonstationary extracellular electrophysiology recordings. In addition to estimating motion from spikes in the action potential (AP) frequency band, DREDge enables automated tracking of motion at high temporal resolution in the local field potential (LFP) frequency band. In human intraoperative recordings, which often feature fast (period <1s) motion, DREDge correction in the LFP band enabled reliable recovery of evoked potentials, and significantly reduced single-unit spike shape variability and spike sorting error. Applying DREDge to recordings made during deep probe insertions in nonhuman primates demonstrated the possibility of tracking probe motion of centimeters across several brain regions while simultaneously mapping single unit electrophysiological features. DREDge reliably delivered improved motion correction in acute mouse recordings, especially in those made with an recent ultra-high density probe. We also implemented a procedure for applying DREDge to recordings made across tens of days in chronic implantations in mice, reliably yielding stable motion tracking despite changes in neural activity across experimental sessions. Together, these advances enable automated, scalable registration of electrophysiological data across multiple species, probe types, and drift cases, providing a stable foundation for downstream scientific analyses of these rich datasets.

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.

Contrast and Luminance Gain Control in the Macaque's Lateral Geniculate Nucleus.

There is substantial variation in the mean and variance of light levels (luminance and contrast) in natural visual scenes. Retinal ganglion cells maintain their sensitivity despite this variation using two adaptive mechanisms, which control how responses depend on luminance and on contrast. However, the nature of each mechanism and their interactions downstream of the retina are unknown. We recorded neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus (LGN) in anesthetized adult male macaques and characterized how their responses adapt to changes in contrast and luminance. As contrast increases, neurons in the magnocellular layers maintain sensitivity to high temporal frequency stimuli but attenuate sensitivity to low-temporal frequency stimuli. Neurons in the parvocellular layers do not adapt to changes in contrast. As luminance increases, both magnocellular and parvocellular cells increase their sensitivity to high-temporal frequency stimuli. Adaptation to luminance is independent of adaptation to contrast, as previously reported for LGN neurons in the cat. Our results are similar to those previously reported for macaque retinal ganglion cells, suggesting that adaptation to luminance and contrast result from two independent mechanisms that are retinal in origin.

Sensitivity to naturalistic texture relies primarily on high spatial frequencies.

Natural images contain information at multiple spatial scales. Though we understand how early visual mechanisms split multiscale images into distinct spatial frequency channels, we do not know how the outputs of these channels are processed further by mid-level visual mechanisms. We have recently developed a texture discrimination task that uses synthetic, multi-scale, "naturalistic" textures to isolate these mid-level mechanisms. Here, we use three experimental manipulations (image blur, image rescaling, and eccentric viewing) to show that perceptual sensitivity to naturalistic structure is strongly dependent on features at high object spatial frequencies (measured in cycles/image). As a result, sensitivity depends on a texture acuity limit, a property of the visual system that sets the highest retinal spatial frequency (measured in cycles/degree) at which observers can detect naturalistic features. Analysis of the texture images using a model observer analysis shows that naturalistic image features at high object spatial frequencies carry more task-relevant information than those at low object spatial frequencies. That is, the dependence of sensitivity on high object spatial frequencies is a property of the texture images, rather than a property of the visual system. Accordingly, we find human observers' ability to extract naturalistic information (their efficiency) is similar for all object spatial frequencies. We conclude that the mid-level mechanisms that underlie perceptual sensitivity effectively extract information from all image features below the texture acuity limit, regardless of their retinal and object spatial frequency.

Laminar Differences in Responses to Naturalistic Texture in Macaque V1 and V2.

Most single units recorded from macaque secondary visual cortex (V2) respond with higher firing rates to synthetic texture images containing "naturalistic" higher-order statistics than to spectrally matched "noise" images lacking these statistics. In contrast, few single units in V1 show this property. We explored how the strength and dynamics of response vary across the different layers of visual cortex by recording multiunit (defined as high-frequency power in the local field potential) and gamma-band activity evoked by brief presentations of naturalistic and noise images in V1 and V2 of anesthetized macaque monkeys of both sexes. As previously reported, recordings in V2 showed consistently stronger responses to naturalistic texture than to spectrally matched noise. In contrast to single-unit recordings, V1 multiunit activity showed a preference for images with naturalistic statistics, and in gamma-band activity this preference was comparable across V1 and V2. Sensitivity to naturalistic image structure was strongest in the supragranular and infragranular layers of V1, but weak in granular layers, suggesting that it might reflect feedback from V2. Response timing was consistent with this idea. Visual responses appeared first in V1, followed by V2. Sensitivity to naturalistic texture emerged first in V2, followed by the supragranular and infragranular layers of V1, and finally in the granular layers of V1. Our results demonstrate laminar differences in the encoding of higher-order statistics of natural texture, and suggest that this sensitivity first arises in V2 and is fed back to modulate activity in V1.SIGNIFICANCE STATEMENT The circuit mechanisms responsible for visual representations of intermediate complexity are largely unknown. We used a well validated set of synthetic texture stimuli to probe the temporal and laminar profile of sensitivity to the higher-order statistical structure of natural images. We found that this sensitivity emerges first and most strongly in V2 but soon after in V1. However, sensitivity in V1 is higher in the laminae (extragranular) and recording modalities (local field potential) most likely affected by V2 connections, suggesting a feedback origin. Our results show how sensitivity to naturalistic image structure emerges across time and circuitry in the early visual cortex.

Compound Stimuli Reveal the Structure of Visual Motion Selectivity in Macaque MT Neurons.

Motion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency ("frequency-separable"). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed ("velocity-separable"). This construction explains "pattern direction-selective" MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. We designed a set of experiments to distinguish frequency-separable and velocity-separable models and executed them with single-unit recordings in macaque V1 and MT. Surprisingly, when tested with single drifting gratings, most MT neurons' responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions.

Responses of neurons in macaque MT to unikinetic plaids.

Response properties of MT neurons are often studied with "bikinetic" plaid stimuli, which consist of two superimposed sine wave gratings moving in different directions. Oculomotor studies using "unikinetic plaids" in which only one of the two superimposed gratings moves suggest that the eyes first move reflexively in the direction of the moving grating and only later converge on the perceived direction of the moving pattern. MT has been implicated as the source of visual signals that drives these responses. We wanted to know whether stationary gratings, which have little effect on MT cells when presented alone, would influence MT responses when paired with a moving grating. We recorded extracellularly from neurons in area MT and measured responses to stationary and moving gratings, and to their sums: bikinetic and unikinetic plaids. As expected, stationary gratings presented alone had a very modest influence on the activity of MT neurons. Responses to moving gratings and bikinetic plaids were similar to those previously reported and revealed cells selective for the motion of plaid patterns and of their components (pattern and component cells). When these neurons were probed with unikinetic plaids, pattern cells shifted their direction preferences in a way that revealed the influence of the static grating. Component cell preferences shifted little or not at all. These results support the notion that pattern-selective neurons in area MT integrate component motions that differ widely in speed, and that they do so in a way that is consistent with an intersection-of-constraints model.NEW & NOTEWORTHY Human perceptual and eye movement responses to moving gratings are influenced by adding a second, static grating to create a "unikinetic" plaid. Cells in MT do not respond to static gratings, but those gratings still influence the direction selectivity of some MT cells. The cells influenced by static gratings are those tuned for the motion of global patterns, but not those tuned only for the individual components of moving targets.

Altered functional interactions between neurons in primary visual cortex of macaque monkeys with experimental amblyopia.

Amblyopia, a disorder in which vision through one of the eyes is degraded, arises because of defective processing of information by the visual system. Amblyopia often develops in humans after early misalignment of the eyes (strabismus) and can be simulated in macaque monkeys by artificially inducing strabismus. In such amblyopic animals, single-unit responses in primary visual cortex (V1) are appreciably reduced when evoked by the amblyopic eye compared with the other (fellow) eye. However, this degradation in single V1 neuron responsivity is not commensurate with the marked losses in visual sensitivity and resolution measured behaviorally. Here we explored the idea that changes in patterns of coordinated activity across populations of V1 neurons may contribute to degraded visual representations in amblyopia, potentially making it more difficult to read out evoked activity to support perceptual decisions. We studied the visually evoked activity of V1 neuronal populations in three macaques (Macaca nemestrina) with strabismic amblyopia and in one control animal. Activity driven through the amblyopic eye was diminished, and these responses also showed more interneuronal correlation at all stimulus contrasts than responses driven through the fellow eye or responses in the control animal. A decoding analysis showed that responses driven through the amblyopic eye carried less visual information than other responses. Our results suggest that part of the reduced visual capacity of amblyopes may be due to changes in the patterns of functional interaction among neurons in V1.NEW & NOTEWORTHY Previous work on the neurophysiological basis of amblyopia has largely focused on relating behavioral deficits to changes in visual processing by single neurons in visual cortex. In this study, we recorded simultaneously from populations of primary visual cortical (V1) neurons in macaques with amblyopia. We found changes in the strength and pattern of shared response variability between neurons. These changes in neuronal interactions could impair the visual representations of V1 populations driven by the amblyopic eye.

A Conversation with Jacob Nachmias.

We are sad to report that Professor Jacob (Jack) Nachmias passed away on March 2, 2019. Nachmias was born in Athens, Greece, on June 9, 1928. To escape the Nazis, he and his family came to the United States in 1939. He received his undergraduate degree from Cornell University and then an MA from Swarthmore College, where he worked with Hans Wallach and Wolfgang Kohler; his PhD in Psychology was from Harvard University. Nachmias spent the majority of his career as a Professor of Psychology at the University of Pennsylvania. He made fundamental contributions to our understanding of vision, most notably through the study of eye movements, the development of signal detection theory and forced-choice psychophysical methods, and the psychophysical characterization of spatial-frequency-selective visual channels. Nachmias' work was recognized by his election to the National Academy of Sciences and receipt of the Optical Society's Tillyer Award.