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Ni, A. M.

Publications and source records attributed to Ni, A. M..

6 recordsLinked to original sources

Guided by Noise: Correlated Variability Channels Task-Relevant Information in Sensory Neurons

Shared trial-to-trial variability across sensory neurons is reliably reduced when perceptual performance improves, yet this variability is low-dimensional, so it could be ignored by an optimal readout mechanism. Why then is it so consistently related to behavior? We propose that shared variability both reflects circuit structure and reveals the information communicated to downstream areas. In this framework, the same connectivity that shapes signal propagation also shapes shared variability. Using a circuit model, we show that when sensory signals align with shared variability, behaviorally relevant information is amplified without compromising coding fidelity. Analyses of neural population recordings from multiple brain areas and tasks reveal that the dominant axis of shared variability consistently aligns with task-relevant stimulus features and action plans. Finally, the behavioral impact of microstimulation can be explained by the extent to which it changes projections onto the shared variability axis. These findings suggest that shared variability may illuminate, rather than obscure, the neural dimensions that guide behavior. Significance StatementThe brains ability to use different features of sensory information flexibly across many tasks is essential for complex decision-making. Our study reveals that the correlated variability in neural responses in mid-level visual areas indicates the visual feature that is relevant for behavior. Our biologically plausible network model predicted that it is beneficial for the representation of behaviorally relevant visual information to be aligned with the correlated variability in neurons. We tested and confirmed this in five independent neural data sets. Our results suggest that trial-by-trial variability does not affect the information encoded in sensory neurons but instead is a valuable signal for us to understand which combination of the encoded features is being used by the brain to guide choices.

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Orthogonal neural representations support perceptual judgements of natural stimuli

In natural behavior, observers must separate relevant information from a barrage of irrelevant information. Many studies have investigated the neural underpinnings of this ability using artificial stimuli presented on simple backgrounds. Natural viewing, however, carries a set of challenges that are inaccessible using artificial stimuli, including neural responses to background objects that are task-irrelevant. An emerging body of evidence suggests that the visual abilities of humans and animals can be modeled through the linear decoding of task-relevant information from visual cortex. This idea suggests the hypothesis that irrelevant features of a natural scene should impair performance on a visual task only if their neural representations intrude on the linear readout of the task relevant feature, as would occur if the representations of task-relevant and irrelevant features are not orthogonal in the underlying neural population. We tested this hypothesis using human psychophysics and monkey neurophysiology, in response to parametrically variable naturalistic stimuli. We demonstrate that 1) the neural representation of one feature (the position of a central object) in visual area V4 is orthogonal to those of several background features, 2) the ability of human observers to precisely judge object position was largely unaffected by task-irrelevant variation in those background features, and 3) many features of the object and the background are orthogonally represented by V4 neural responses. Our observations are consistent with the hypothesis that orthogonal neural representations can support stable perception of objects and features despite the tremendous richness of natural visual scenes. Significance StatementWe studied how the structure of the mid-level neural representation of multiple visual features supports robust perceptual decisions. We combined array recording with parametrically controlled naturalistic images to demonstrate that the representation of a central objects position in monkey visual area V4 is orthogonal to that of several background features. In addition, we used human psychophysics with the same stimulus set to show that observers ability to judge a central objects position is largely unaffected by variation in the same background features. This result supports the hypothesis that orthogonal neural representations can enable stable and robust perception in naturalistic visual environments and advances our understanding of how visual processing operates in the real world.

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Topological insights into the neural basis of flexible behavior

It is widely accepted that there is an inextricable link between neural computations, biological mechanisms, and behavior, but it is challenging to simultaneously relate all three. Here, we show that topological data analysis (TDA) provides an important bridge between these approaches to studying how brains mediate behavior. We demonstrate that cognitive processes change the topological description of the shared activity of populations of visual neurons. These topological changes constrain and distinguish between competing mechanistic models, are connected to subjects performance on a visual change detection task, and, via a link with network control theory, reveal a tradeoff between improving sensitivity to subtle visual stimulus changes and increasing the chance that the subject will stray off task. These connections provide a blueprint for using TDA to uncover the biological and computational mechanisms by which cognition affects behavior in health and disease. Significance StatementAs the fields of systems, computational, and cognitive neuroscience strive to establish links between computations, biology, and behavior, there is an increasing need for an analysis framework to bridge levels of analysis. We demonstrate that topological data analysis (TDA) of the shared activity of populations of neurons provides that link. TDA allows us to distinguish between competing mechanistic models and to answer longstanding questions in cognitive neuroscience, such as why there is a tradeoff between visual sensitivity and staying on task. These results and analysis framework have applications to many systems within neuroscience and beyond.

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Methylphenidate as a causal test of translational and basic neural coding hypotheses

Most systems neuroscience studies fall into one of two categories: basic science work aimed at understanding the relationship between neurons and behavior, or translational work aimed at developing treatments for neuropsychiatric disorders. Here we use these two approaches to inform and enhance each other. Our study both tests hypotheses about basic science neural coding principles and elucidates the neuronal mechanisms underlying new, clinically relevant behavioral effects of systemically administered methylphenidate (Ritalin). We discovered that orally administered methylphenidate, used clinically to treat Attention Deficit Hyperactivity Disorder (ADHD) and generally to enhance cognition (Lakhan & Kirchgessner, 2012; Maher, 2008), increases spatially selective visual attention, enhancing visual performance at only the attended location. And as predicted by our previous work (Ni et al., 2018), we found that this causal manipulation enhances vision in rhesus macaques specifically when it decreases the mean correlated variability of neurons in visual area V4. Our findings demonstrate that the visual system is a platform for understanding the neural underpinnings of both complex cognitive processes (basic science) and neuropsychiatric disorders (translation). Addressing basic science hypotheses, our results are consistent with a scenario in which methylphenidate has cognitively specific effects by working through naturally selective cognitive mechanisms. Clinically, our findings suggest that the often staggeringly specific symptoms of neuropsychiatric disorders may be caused and treated by leveraging general mechanisms.

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A general decoding strategy explains the relationship between behavior and correlated variability

Improvements in perception are frequently accompanied by decreases in correlated variability in sensory cortex. This relationship is puzzling because overall changes in correlated variability should minimally affect optimal information coding. We hypothesize that this relationship arises because instead of using optimal strategies for decoding the specific stimuli at hand, observers prioritize generality: a single set of neuronal weights to decode any stimuli. We tested this using a combination of multineuron recordings in the visual cortex of behaving rhesus monkeys and a cortical circuit model. We found that general decoders optimized for broad rather than narrow sets of visual stimuli better matched the animals decoding strategy, and that their performance was more related to the magnitude of correlated variability. In conclusion, the inverse relationship between perceptual performance and correlated variability can be explained by observers using a general decoding strategy, capable of decoding neuronal responses to the variety of stimuli encountered in natural vision. IMPACT STATEMENTThe frequently observed relationship between perceptual performance and correlated variability in sensory cortex can be explained by observers using a decoding strategy that prioritizes generality for many stimuli over precision.

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Learning And Attention Reveal A General Relationship Between Neuronal Variability And Perception

The trial-to-trial response variability that is shared between pairs of neurons (termed spike count correlations1 or rSC) has been the subject of many recent studies largely because it might limit the amount of information that can be encoded by neuronal populations. Spike count correlations are flexible and change depending on task demands2-7. However, the relationship between correlated variability and information coding is a matter of current debate2-14. This debate has been difficult to resolve because testing the theoretical predictions would require simultaneous recordings from an experimentally unfeasible number of neurons. We hypothesized that if correlated variability limits population coding, then spike count correlations in visual cortex should a) covary with subjects performance on visually guided tasks and b) lie along the dimensions in neuronal population space that contain information that is used to guide behavior. We focused on two processes that are known to improve visual performance: visual attention, which allows observers to focus on important parts of a visual scene15-17, and perceptual learning, which slowly improves observers ability to discriminate specific, well-practiced stimuli18-20. Both attention and learning improve performance on visually guided tasks, but the two processes operate on very different timescales and are typically studied using different perceptual tasks. Here, by manipulating attention and learning in the same task, subjects, trials, and neuronal populations, we show that there is a single, robust relationship between correlated variability in populations of visual neurons and performance on a change-detection task. We also propose an explanation for the mystery of how correlated variability might affect performance: it is oriented along the dimensions of population space used by the animal to make perceptual decisions. Our results suggest that attention and learning affect the same aspects of the neuronal population activity in visual cortex, which may be responsible for learning- and attention-related improvements in behavioral performance. More generally, our study provides a framework for leveraging the activity of simultaneously recorded populations of neurons, cognitive factors, and perceptual decisions to understand the neuronal underpinnings of behavior.

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