Cong Yu

Continuous flash suppression (CFS), in which a dynamic masker presented to one eye suppresses awareness of a stimulus in the other eye, is widely used to study visual subconsciousness. Although some studies report preserved high-level processing under CFS, these effects have been increasingly questioned and may partly reflect residual low-level feature processing. A key unresolved issue is how strongly neuronal responses in V1, where inputs from the two eyes first converge, are affected by CFS, and how much the remaining signals can support downstream processing. Here, we used two-photon calcium imaging to record large populations of V1 neurons in awake, fixating macaques while presenting grating stimuli under CFS. CFS strongly suppressed V1 orientation responses in an ocular-dominance-dependent manner, nearly abolishing responses in neurons preferring the masker eye or both eyes, and significantly reducing responses in neurons preferring the grating eye. Modeling analyses further indicated that V1 population activity under CFS may still support coarse orientation classification but not accurate stimulus reconstruction. These results suggest that CFS substantially degrades orientation information in V1. The residual signals may support limited low-level processing but are likely insufficient for downstream higher-level visual and cognitive tasks.

Continuous flash suppression (CFS), a dynamic masker presented to one eye suppressing the conscious perception of a stimulus shown to the other eye, has been extensively used to study visual consciousness. Various studies reported high-level visual and cognitive functions under CFS, which, however, has more recently been questioned and at least partially attributed to low-level stimulus properties. A key but unsettled issue is the extent to which the responses of V1 neurons, where inputs from two eyes first merge, are affected, as severely suppressed V1 responses would not sustain high-level processing. Here, we used two-photon calcium imaging to record the responses of large samples of V1 neurons to a grating stimulus under CFS in awake, fixating macaques. The results revealed that CFS substantially suppressed V1 orientation responses. Ocularity-wise, it nearly completely eliminated the orientation responses of V1 neurons preferring the masker eye or both eyes, while also significantly suppressing the responses of those preferring the grating eye. Modeling analyses suggest that, under CFS, the brain retains the ability of classifying coarse orientations, but may become less capable of reconstructing the grating stimulus. Consequently, while CFS-suppressed orientation information still supports low-level orientation discrimination, it may not suffice for high-level visual and cognitive processing.

Orientation is one of the most fundamental stimulus features in visual perception. In the primary visual cortex (V1), while most neurons are orientation-selective, a small portion exhibits a lack of this selectivity. However, it remains unclear what roles the orientation-untuned V1 neurons play in population orientation discrimination. Here, we analyzed data from a 2-photon calcium imaging study that recorded the responses of thousands of V1 neurons to a grating stimulus at various orientations in awake macaques. Our population analysis reveals that orientation-untuned neurons can independently decode stimulus orientation with accuracy comparable to tuned neurons. Remarkably, we found that the more critical role of orientation-untuned neuronal populations in orientation encoding is to enhance coding robustness, specifically by reducing sensitivity to noise. Moreover, when using artificial neural networks to model the primate ventral visual pathway, we found that the V1-like layer also contains a proportion of orientation-untuned units. Removing these units leads to significant impairments in natural object recognition. Overall, these results indicate that orientation-untuned neurons encode orientation information and play a crucial role in primate visual perception. The study provides compelling evidence for a continuous distribution of visual features across neurons and challenges the notion of highly specialized units.

Continuous flash suppression (CFS), a dynamic masker presented to one eye suppressing the conscious perception of a stimulus shown to the other eye, has been extensively used to study visual consciousness. Various studies reported high-level visual and cognitive functions under CFS, which, however, has more recently been questioned and at least partially attributed to low-level stimulus properties. A key but unsettled issue is the extent to which the responses of V1 neurons, where inputs from two eyes first merge, are affected, as severely suppressed V1 responses would not sustain high-level processing. Here, we used two-photon calcium imaging to record the responses of large samples of V1 neurons to a grating stimulus under CFS in awake, fixating macaques. The results revealed that CFS substantially suppressed V1 orientation responses. Ocularity-wise, it nearly completely eliminated the orientation responses of V1 neurons preferring the masker eye or both eyes, while also significantly suppressing the responses of those preferring the grating eye. Modeling analyses suggest that, under CFS, the brain retains the ability of classifying coarse orientations, but may become less capable of reconstructing the grating stimulus. Consequently, while CFS-suppressed orientation information still supports low-level orientation discrimination, it may not suffice for high-level visual and cognitive processing.

Hubel and Wiesel’s ice-cube model proposed that V1 orientation and ocular dominance functional maps intersect orthogonally to optimize wiring efficiency. Here, we revisited this model and additional arrangements at both cellular and pixel levels in awake macaques using two-photon calcium imaging. The recorded response fields of view were similar in size to hypercolumns, each containing up to 2,000 identified neurons and representing full periods of orientation preferences and ocular dominance. We estimated each neuron/pixel's orientation, ocular dominance, and spatial frequency preferences, constructed respective functional maps, computed geometric gradients of feature preferences, and calculated intersection angles among these gradients. At the cellular level, the intersection angles among functional maps were nearly evenly distributed. Nonetheless, pixel-based maps after Gaussian smoothing displayed orientation-ocular dominance and orientation–spatial frequency orthogonality, as well as ocular dominance–spatial frequency parallelism, in alignment with previous results, even though the trends were weak and highly variable. However, these Gaussian smoothing effects were not observed in cellular maps, indicating that the pixel-based trends may not accurately represent the relationships among feature-tuning properties of V1 neurons. We suggest that the widely distributed intersections among cellular maps can ensure that multiple stimulus features are represented within a hypercolumn, and no pair of features is represented with the least economical wiring (e.g. parallel intersections).

Subsecond temporal processing is crucial for activities requiring precise timing. Here, we investigated perceptual learning of crossmodal (auditory–visual or visual–auditory) temporal interval discrimination (TID) and its impacts on unimodal (visual or auditory) TID performance. The research purpose was to test whether learning is based on a more abstract and conceptual representation of subsecond time, which would predict crossmodal to unimodal learning transfer. The experiments revealed that learning to discriminate a 200-ms crossmodal temporal interval, defined by a pair of visual and auditory stimuli, significantly reduced crossmodal TID thresholds. Moreover, the crossmodal TID training also minimized unimodal TID thresholds with a pair of visual or auditory stimuli at the same interval, even if crossmodal TID thresholds are multiple times higher than unimodal TID thresholds. Subsequent training on unimodal TID failed to reduce unimodal TID thresholds further. These results indicate that learning of high-threshold crossmodal TID tasks can benefit low-threshold unimodal temporal processing, which may be achieved through training-induced improvement of a conceptual representation of subsecond time in the brain.