Sensory and Choice Responses in MT Distinct from Motion Encoding.

The macaque middle temporal (MT) area is well known for its visual motion selectivity and relevance to motion perception, but the possibility of it also reflecting higher-level cognitive functions has largely been ignored. We tested for effects of task performance distinct from sensory encoding by manipulating subjects' temporal evidence-weighting strategy during a direction discrimination task while performing electrophysiological recordings from groups of MT neurons in rhesus macaques (one male, one female). This revealed multiple components of MT responses that were, surprisingly, not interpretable as behaviorally relevant modulations of motion encoding, or as bottom-up consequences of the readout of motion direction from MT. The time-varying motion-driven responses of MT were strongly affected by our strategic manipulation-but with time courses opposite the subjects' temporal weighting strategies. Furthermore, large choice-correlated signals were represented in population activity distinct from its motion responses, with multiple phases that lagged psychophysical readout and even continued after the stimulus (but which preceded motor responses). In summary, a novel experimental manipulation of strategy allowed us to control the time course of readout to challenge the correlation between sensory responses and choices, and population-level analyses of simultaneously recorded ensembles allowed us to identify strong signals that were so distinct from direction encoding that conventional, single-neuron-centric analyses could not have revealed or properly characterized them. Together, these approaches revealed multiple cognitive contributions to MT responses that are task related but not functionally relevant to encoding or decoding of motion for psychophysical direction discrimination, providing a new perspective on the assumed status of MT as a simple sensory area.SIGNIFICANCE STATEMENT This study extends understanding of the middle temporal (MT) area beyond its representation of visual motion. Combining multineuron recordings, population-level analyses, and controlled manipulation of task strategy, we exposed signals that depended on changes in temporal weighting strategy, but did not manifest as feedforward effects on behavior. This was demonstrated by (1) an inverse relationship between temporal dynamics of behavioral readout and sensory encoding, (2) a choice-correlated signal that always lagged the stimulus time points most correlated with decisions, and (3) a distinct choice-correlated signal after the stimulus. These findings invite re-evaluation of MT for functions outside of its established sensory role and highlight the power of experimenter-controlled changes in temporal strategy, coupled with recording and analysis approaches that transcend the single-neuron perspective.

Stimulus-choice (mis)alignment in primate area MT.

For stimuli near perceptual threshold, the trial-by-trial activity of single neurons in many sensory areas is correlated with the animal's perceptual report. This phenomenon has often been attributed to feedforward readout of the neural activity by the downstream decision-making circuits. The interpretation of choice-correlated activity is quite ambiguous, but its meaning can be better understood in the light of population-wide correlations among sensory neurons. Using a statistical nonlinear dimensionality reduction technique on single-trial ensemble recordings from the middle temporal (MT) area during perceptual-decision-making, we extracted low-dimensional latent factors that captured the population-wide fluctuations. We dissected the particular contributions of sensory-driven versus choice-correlated activity in the low-dimensional population code. We found that the latent factors strongly encoded the direction of the stimulus in single dimension with a temporal signature similar to that of single MT neurons. If the downstream circuit were optimally utilizing this information, choice-correlated signals should be aligned with this stimulus encoding dimension. Surprisingly, we found that a large component of the choice information resides in the subspace orthogonal to the stimulus representation inconsistent with the optimal readout view. This misaligned choice information allows the feedforward sensory information to coexist with the decision-making process. The time course of these signals suggest that this misaligned contribution likely is feedback from the downstream areas. We hypothesize that this non-corrupting choice-correlated feedback might be related to learning or reinforcing sensory-motor relations in the sensory population.

A simple linear readout of MT supports motion direction-discrimination performance.

Motion discrimination is a well-established model system for investigating how sensory signals are used to form perceptual decisions. Classic studies relating single-neuron activity in the middle temporal area (MT) to perceptual decisions have suggested that a simple linear readout could underlie motion discrimination behavior. A theoretically optimal readout, in contrast, would take into account the correlations between neurons and the sensitivity of individual neurons at each time point. However, it remains unknown how sophisticated the readout needs to be to support actual motion-discrimination behavior or to approach optimal performance. In this study, we evaluated the performance of various neurally plausible decoders, trained to discriminate motion direction from small ensembles of simultaneously recorded MT neurons. We found that decoding the stimulus without knowledge of the interneuronal correlations was sufficient to match an optimal (correlation aware) decoder. Additionally, a decoder could match the psychophysical performance of the animals with flat integration of up to half the stimulus and inherited temporal dynamics from the time-varying MT responses. These results demonstrate that simple, linear decoders operating on small ensembles of neurons can match both psychophysical performance and optimal sensitivity without taking correlations into account and that such simple read-out mechanisms can exhibit complex temporal properties inherited from the sensory dynamics themselves.NEW & NOTEWORTHY Motion perception depends on the ability to decode the activity of neurons in the middle temporal area. Theoretically optimal decoding requires knowledge of the sensitivity of neurons and interneuronal correlations. We report that a simple correlation-blind decoder performs as well as the optimal decoder for coarse motion discrimination. Additionally, the decoder could match the psychophysical performance with moderate temporal integration and dynamics inherited from sensory responses.

Is improved contrast sensitivity a natural consequence of visual training?

Many studies have shown that training and testing conditions modulate specificity of visual learning to trained stimuli and tasks. In visually impaired populations, generalizability of visual learning to untrained stimuli/tasks is almost always reported, with contrast sensitivity (CS) featuring prominently among these collaterally-improved functions. To understand factors underlying this difference, we measured CS for direction and orientation discrimination in the visual periphery of three groups of visually-intact subjects. Group 1 trained on an orientation discrimination task with static Gabors whose luminance contrast was decreased as performance improved. Group 2 trained on a global direction discrimination task using high-contrast random dot stimuli previously used to recover motion perception in cortically blind patients. Group 3 underwent no training. Both forms of training improved CS with some degree of specificity for basic attributes of the trained stimulus/task. Group 1's largest enhancement was in CS around the trained spatial/temporal frequencies; similarly, Group 2's largest improvements occurred in CS for discriminating moving and flickering stimuli. Group 3 saw no significant CS changes. These results indicate that CS improvements may be a natural consequence of multiple forms of visual training in visually intact humans, albeit with some specificity to the trained visual domain(s).

Interpreting temporal dynamics during sensory decision-making.

Perceptual decisions are informed by the accumulation of sensory evidence over time, but the form of this fundamental temporal computation is not fully understood. Characterizations of the temporal integration of sensory stimuli in behavior and neural activity are usually conceived with separate stages for sensory encoding and downstream integration for accumulating the sensory evidence. Sensory and decision stages can each have their own temporal dynamics that affect the time course of perception and action. Here, we discuss recent work using temporal signatures of behavior in the context of traditional two-stage models. This discussion highlights shortcomings of two stage sensory/decision frameworks, points towards how modern techniques can provide more realistic characterizations of temporal integration, and in turn motivates a richer philosophical framework for building models of how sensory data might be interpreted by the brain to produce actions.

Strategic and Dynamic Temporal Weighting for Perceptual Decisions in Humans and Macaques.

Perceptual decision-making is often modeled as the accumulation of sensory evidence over time. Recent studies using psychophysical reverse correlation have shown that even though the sensory evidence is stationary over time, subjects may exhibit a time-varying weighting strategy, weighting some stimulus epochs more heavily than others. While previous work has explained time-varying weighting as a consequence of static decision mechanisms (e.g., decision bound or leak), here we show that time-varying weighting can reflect strategic adaptation to stimulus statistics, and thus can readily take a number of forms. We characterized the temporal weighting strategies of humans and macaques performing a motion discrimination task in which the amount of information carried by the motion stimulus was manipulated over time. Both species could adapt their temporal weighting strategy to match the time-varying statistics of the sensory stimulus. When early stimulus epochs had higher mean motion strength than late, subjects adopted a pronounced early weighting strategy, where early information was weighted more heavily in guiding perceptual decisions. When the mean motion strength was greater in later stimulus epochs, in contrast, subjects shifted to a marked late weighting strategy. These results demonstrate that perceptual decisions involve a temporally flexible weighting process in both humans and monkeys, and introduce a paradigm with which to manipulate sensory weighting in decision-making tasks.