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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.

The breadth and complexity of natural behaviors inspires awe. Understanding how our perceptions, actions, and internal thoughts arise from evolved circuits in the brain has motivated neuroscientists for generations. Researchers have traditionally approached this question by focusing on stereotyped behaviors, either natural or trained, in a limited number of model species. This approach has allowed for the isolation and systematic study of specific brain operations, which has greatly advanced our understanding of the circuits involved. At the same time, the emphasis on experimental reductionism has left most aspects of the natural behaviors that have shaped the evolution of the brain largely unexplored. However, emerging technologies and analytical tools make it possible to comprehensively link natural behaviors to neural activity across a broad range of ethological contexts and timescales, heralding new modes of neuroscience focused on natural behaviors. Here we describe a three-part roadmap that aims to leverage the wealth of behaviors in their naturally occurring distributions, linking their variance with that of underlying neural processes to understand how the brain is able to successfully navigate the everyday challenges of animals' social and ecological landscapes. To achieve this aim, experimenters must harness one challenge faced by all neurobiological systems, namely variability, in order to gain new insights into the language of the brain.

During decision making, neurons in multiple brain regions exhibit responses that are correlated with decisions (1-6). However, it remains uncertain whether or not various forms of decision-related activity are causally [...]

Mental imagery is thought to share properties with perception. To what extent does the process of imagining a scene share neural circuits and computational mechanisms with actually perceiving the same scene? Here, we investigated whether mental imagery of motion in a particular direction recruits neural circuits tuned to the same direction of perceptual motion. To address this question we made use of a visual illusion, the motion aftereffect. We found that following prolonged imagery of motion in one direction, people are more likely to perceive real motion test probes as moving in the direction opposite to the direction of motion imagery. The transfer of adaptation from imagined to perceived motion provides evidence that motion imagery and motion perception recruit shared direction-selective neural circuitry. Even in the absence of any visual stimuli, people can selectively recruit specific low-level sensory neurons through mental imagery. (Contains 4 figures.)