Pattern and component responses of primate MT neurons recorded with multi-contact electrodes, stimulated with 1D and 2D noise patterns.

Direction selective neurons in primary visual cortex (area V1) are affected by the aperture problem, i.e., they are only sensitive to motion orthogonal to their preferred orientation. A solution to this problem first emerges in the middle temporal (MT) area, where a subset of neurons (called pattern cells) combine motion information across multiple orientations and directions, becoming sensitive to pattern motion direction. These cells are expected to play a prominent role in subsequent neural processing, but they are intermixed with cells that behave like V1 cells (component cells), and others that do not clearly fall in either group. The picture is further complicated by the finding that cells that behave like pattern cells with one type of pattern, might behave like component cells for another. We recorded from macaque MT neurons using multi-contact electrodes while presenting both type I and unikinetic plaids, in which the components were 1D noise patterns. We found that the indices that have been used in the past to classify neurons as pattern or component cells work poorly when the properties of the stimulus are not optimized for the cell being recorded, as is always the case with multi-contact arrays. We thus propose alternative measures, which considerably ameliorate the problem, and allow us to gain insights in the signals carried by individual MT neurons. We conclude that arranging cells along a component-to-pattern continuum is an oversimplification, and that the signals carried by individual cells only make sense when embodied in larger populations.

Task Demands Change Motion Information Coding in Area MT of the Macaque

Neurons in the primate Middle Temporal (MT) area signal information about visual motion and work together with the lateral prefrontal cortex (LPFC) to support memory-guided comparisons of visual motion direction. These areas are reciprocally connected and both contain neurons that signal visual motion direction in the strength of their responses. Previously, LPFC was shown to display marked changes in stimulus coding with altered task demands. Since MT and LPFC work together, we sought to determine if MT neurons display similar changes with heightened task demands. We hypothesized that heightened working-memory task demands would improve the task-relevant information and precipitate memory-related signals in MT. Here we show that engagement in a motion direction comparison task altered non-sensory activity and improved stimulus encoding by MT neurons. We found that this improvement in stimulus information transmission was largely due to preferential reduction in trial-to-trial variability within a sub-population of highly direction-selective neurons. We also found that a divisive normalization mechanism accounted for seemingly contradictory effects of task-demands on a heterogeneous population of neurons.

Dynamic divisive normalization circuits explain and predict change detection in monkey area MT

Sudden changes in visual scenes often indicate important events for behavior. For their quick and reliable detection, the brain must be capable to process these changes as independently as possible from its current activation state. In motion-selective area MT, neurons respond to instantaneous speed changes with pronounced transients, often far exceeding the expected response as derived from their speed tuning profile. We here show that this complex, non-linear behavior emerges from the combined temporal dynamics of excitation and divisive inhibition, and provide a comprehensive mathematical analysis. A central prediction derived from this investigation is that attention increases the steepness of the transient response irrespective of the activation state prior to a stimulus change, and irrespective of the sign of the change (i.e. irrespective of whether the stimulus is accelerating or decelerating). Extracellular recordings of attention-dependent representation of both speed increments and decrements confirmed this prediction and suggest that improved change detection derives from basic computations in a canonical cortical circuitry.

Speed tuning in head coordinates as an alternative explanation of depth selectivity from motion parallax in area MT

There are two distinct sources of retinal image motion: motion of objects in the world and movement of the observer. In cases where an object moves in a scene and the eyes also move, a coordinate transformation that involves smooth eye movements and retinal motion will be needed in order to estimate object motion in world coordinates. More recently, interactions between retinal and eye velocity signals have also been suggested to generate depth selectivity from motion parallax (MP) in the macaque middle temporal (MT) area. We explored whether the nature of the interaction between eye and retinal velocities in MT neurons favors one of these two possibilities or a mixture of both. We analyzed responses of MT neurons to retinal and eye velocities in a viewing context in which the observer translates laterally while maintaining visual fixation on a world-fixed target. In this scenario, the depth of an object can be inferred from the ratio between retinal velocity and eye velocity, according to the motion-pursuit law. Previous studies have shown that MT responses to retinal motion are gain-modulated by the direction of eye movement, suggesting a potential mechanism for depth tuning from MP. However, our analysis of the joint tuning profile for retinal and eye velocities reveals that some MT neurons show a partial coordinate transformation toward head coordinates. We formalized a series of computational models to predict neural spike trains as well as selectivity for depth, and we used factorial model comparisons to quantify the relative importance of each model component. Our findings for many MT neurons reveal that the data are equally well explained by gain modulation or a partial coordinate transformation toward head coordinates, although some responses can only be well fit by the coordinate transform model. Our results highlight the potential role of MT neurons in representing multiple higher-level sensory variables, including depth from MP and object motion in the world.

Attention improves information flow between neuronal populations without changing the communication subspace

Visual attention allows observers to flexibly use or ignore visual information, suggesting that information can be flexibly routed between visual cortex and neurons involved in decision-making. We investigated the neural substrate of flexible information routing by analyzing the activity of populations of visual neurons in the medial temporal area (MT) and oculomotor neurons in the superior colliculus (SC) while rhesus monkeys switched spatial attention. We demonstrated that attention increases the efficacy of visuomotor communication: trial-to-trial variability of the population of SC neurons was better predicted by the activity of MT neurons (and vice versa) when attention was directed toward their joint receptive fields. Surprisingly, this improvement in prediction was not explained or accompanied by changes in the dimensionality of the shared subspace or in local or shared pairwise noise correlations. These results suggest a mechanism by which visual attention can affect perceptual decision-making without altering local neuronal representations.

Specialized contributions of mid-tier stages of dorsal and ventral pathways to stereoscopic processing in macaque

The division of labor between the dorsal and ventral visual pathways has been well studied, but not often with direct comparison at the single-neuron resolution with matched stimuli. Here we directly compared how single neurons in MT and V4, mid-tier areas of the two pathways, process binocular disparity, a powerful cue for 3D perception and actions. We found that MT neurons transmitted disparity signals more quickly and robustly, whereas V4 or its upstream neurons transformed the signals into sophisticated representations more prominently. Therefore, signaling speed and robustness were traded for transformation between the dorsal and ventral pathways. The key factor in this tradeoff was disparity-tuning shape: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, the tuning symmetry predicted the degree of signal transformation across neurons similarly within each area, implying a general role of tuning symmetry in the stereoscopic processing by the two pathways.

A simple canonical circuitry for non-stationary normalization by inhibition to explain and predict change detection in monkey area MT

Sudden changes in visual scenes often indicate important events for behavior. For their quick and reliable detection, the brain must be capable to process these changes as independent as possible from its current activation state. In motion-selective area MT, neurons respond to instantaneous speed changes with pronounced transients, often far exceeding the expected response as derived from their speed tuning profile. We here show that this complex, non-linear behavior emerges from the combined temporal dynamics of excitation and divisive inhibition, and provide a comprehensive formal analysis. A central prediction derived from this investigation is that attention increases the steepness of the transient response irrespective of the activation state prior to a stimulus change, and irrespective of the sign of the change. Extracellular recordings of attention-dependent representation of both speed increments and decrements confirmed this prediction and suggest that improved change detection derives from basic computations in a canonical cortical circuitry.

Specialization of mid-tier stages of dorsal and ventral pathways in stereoscopic processing

The division of labor between the dorsal and ventral visual pathways is an influential model of parallel information processing in the cerebral cortex. However, direct comparison of the two pathways at the single-neuron resolution has been scarce. Here we compare how MT and V4, mid-tier areas of the two pathways in the monkey, process binocular disparity, a powerful cue for depth perception and visually guided actions. We report a novel tradeoff where MT neurons transmit disparity signals quickly and robustly, whereas V4 neurons markedly transform the nature of the signals with extra time to solve the stereo correspondence problem. Therefore, signaling speed and robustness are traded for computational complexity. The key factor in this tradeoff was the shape of disparity tuning: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, this correlation between tuning shape and signal transformation was present across individual neurons within both MT and V4. Overall, our results reveal both distinct signaling advantages and common tuning-curve features of the dorsal and ventral pathways in stereoscopic processing.