Biology subjects

Ryu, S. I.

Publications and source records attributed to Ryu, S. I..

7 recordsLinked to original sources

bioRxiv2022

Learning alters neural activity to simultaneously support memory and action

How are we able to learn new behaviors without disrupting previously learned ones? To understand how the brain achieves this, we used a brain-computer interface (BCI) learning paradigm, which enables us to detect the presence of a memory of one behavior while performing another. We found that learning to use a new BCI map altered the neural activity that monkeys produced when they returned to using a familiar BCI map, in a way that was specific to the learning experience. That is, learning left a "memory trace." This memory trace co-existed with proficient performance under the familiar map, primarily by altering dimensions of neural activity that did not impact behavior. Such a memory trace could provide the neural underpinning for the joint learning of multiple motor behaviors without interference.

neuroscience↗

bioRxiv2020

Learning is shaped by abrupt changes in neural engagement

Internal states such as arousal, attention, and motivation are known to modulate brain-wide neural activity, but how these processes interact with learning is not well understood. During learning, the brain must modify the neural activity it produces to improve behavioral performance. How do internal states affect the evolution of this learning process? Using a brain-computer interface (BCI) learning paradigm in non-human primates, we identified large fluctuations in neural population activity in motor cortex (M1) indicative of arousal-like internal state changes. These fluctuations drove population activity along dimensions we term neural engagement axes. Neural engagement increased abruptly at the start of learning, and then gradually retreated. In a BCI, the causal relationship between neural activity and behavior is known. This allowed us to understand how these changes impacted behavioral performance for different task goals. We found that neural engagement interacted with learning, helping to explain why animals learned some task goals more quickly than others.

neuroscience↗

bioRxiv2020

Skill-specific changes in cortical preparatory activity during motor learning

Animals have a remarkable capacity to learn new motor skills, but it remains an open question as to how learning changes neural population dynamics underlying movement1. Specifically, we asked whether changes in neural population dynamics relate purely to newly learned movements or if additional patterns are generated that facilitate learning without matching motor output. We trained rhesus monkeys to learn a curl force field2 task that elicited new arm-movement kinetics for some but not all reach directions3,4. We found that along certain neural dimensions, preparatory activity in motor cortex reassociated existing activity patterns with new movements. These systematic changes were observed only for learning-altered reaches. Surprisingly, we also found prominent shifts of preparatory activity along a nearly orthogonal neural dimension. These changes in preparatory activity were observed uniformly for all reaches including those unaltered by learning. This uniform shift during learning implies formation of new neural activity patterns, which was not observed in other short-term learning contexts5-8. During a washout period when the curl field was removed, movement kinetics gradually reverted, but the learning-induced uniform shift of preparatory activity persisted and a second, orthogonal uniform shift occurred. This persistent shift may retain a motor memory of the learned field9-11, consistent with faster relearning of the same curl field observed behaviorally and neurally. When multiple different curl fields were learned sequentially, we found distinct uniform shifts, each reflecting the identity of the field applied and potentially separating the associated motor memories12,13. The neural geometry of these shifts in preparatory activity could serve to organize skill-specific changes in movement production, facilitating the acquisition and retention of a broad motor repertoire.

neuroscience↗

bioRxiv2019

Decoding and perturbing decision states in real time

In dynamic environments, subjects often integrate multiple samples of a signal and combine them to reach a categorical judgment. The process of deliberation on the evidence can be described by a time-varying decision variable (DV), decoded from neural activity, that predicts a subjects decision at the end of a trial. However, within trials, large moment-to-moment fluctuations of the DV are observed. The behavioral significance of these fluctuations and their role in the decision process remain unclear. Here we show that within-trial DV fluctuations decoded in real time from motor cortex are tightly linked to choice behavior, and that robust changes in DV sign have the statistical regularities expected from behavioral studies of changes-of-mind. Furthermore, we find single-trial evidence for absorbing decision bounds. As the DV builds up, heavily favoring one or the other choice, moment-to-moment variability in the DV is reduced, and both neural DV and behavioral decisions become resistant to additional pulses of sensory evidence as predicted by diffusion-to-bound and attractor models of the decision process.

neuroscience↗

bioRxiv2018

Population dynamics of choice representation in dorsal premotor and primary motor cortex

Studies in multiple species have revealed the existence of neural signals that lawfully co-vary with different aspects of the decision-making process, including choice, sensory evidence that supports the choice, and reaction time. These signals, often interpreted as the representation of a decision variable (DV), have been identified in several motor preparation circuits and provide insight about mechanisms underlying the decision-making process. However, single-trial dynamics of this process or its representation at the neural population level remain poorly understood. Here, we examine the representation of the DV in simultaneously recorded neural populations of dorsal premotor (PMd) and primary motor (M1) cortices of monkeys performing a random dots direction discrimination task with arm movements as the behavioral report. We show that single-trial DVs covary with stimulus difficulty in both areas but are stronger and appear earlier in PMd compared to M1 when the stimulus duration is fixed and predictable. When temporal uncertainty is introduced by making the stimulus duration variable, single-trial DV dynamics are accelerated across the board and the two areas become largely indistinguishable throughout the entire trial. These effects are not trivially explained by the faster emergence of motor kinematic signals in PMd and M1. All key aspects of the data were replicated by a computational model that relies on progressive recruitment of units with stable choice-related modulation of neural population activity. In contrast with several recent results in rodents, decision signals in PMd and M1 are not carried by short sequences of activity in non-overlapping groups of neurons but are instead distributed across many neurons, which once recruited, represent the decision stably during individual behavioral epochs of the trial.

neuroscience↗

bioRxiv2017

Unsupervised discovery of demixed, low-dimensional neural dynamics across multiple timescales through tensor components analysis

Perceptions, thoughts and actions unfold over millisecond timescales, while learned behaviors can require many days to mature. While recent experimental advances enable large-scale and long-term neural recordings with high temporal fidelity, it remains a formidable challenge to extract unbiased and interpretable descriptions of how rapid single-trial circuit dynamics change slowly over many trials to mediate learning. We demonstrate a simple tensor components analysis (TCA) can meet this challenge by extracting three interconnected low dimensional descriptions of neural data: neuron factors, reflecting cell assemblies; temporal factors, reflecting rapid circuit dynamics mediating perceptions, thoughts, and actions within each trial; and trial factors, describing both long-term learning and trial-to-trial changes in cognitive state. We demonstrate the broad applicability of TCA by revealing insights into diverse datasets derived from artificial neural networks, large-scale calcium imaging of rodent prefrontal cortex during maze navigation, and multielectrode recordings of macaque motor cortex during brain machine interface learning.

neuroscience↗

bioRxiv2017

Inferring single-trial neural population dynamics using sequential auto-encoders

Neuroscience is experiencing a data revolution in which simultaneous recording of many hundreds or thousands of neurons is revealing structure in population activity that is not apparent from single-neuron responses. This structure is typically extracted from trial-averaged data. Single-trial analyses are challenging due to incomplete sampling of the neural population, trial-to-trial variability, and fluctuations in action potential timing. Here we introduce Latent Factor Analysis via Dynamical Systems (LFADS), a deep learning method to infer latent dynamics from single-trial neural spiking data. LFADS uses a nonlinear dynamical system (a recurrent neural network) to infer the dynamics underlying observed population activity and to extract de-noised single-trial firing rates from neural spiking data. We apply LFADS to a variety of monkey and human motor cortical datasets, demonstrating its ability to predict observed behavioral variables with unprecedented accuracy, extract precise estimates of neural dynamics on single trials, infer perturbations to those dynamics that correlate with behavioral choices, and combine data from non-overlapping recording sessions (spanning months) to improve inference of underlying dynamics. In summary, LFADS leverages all observations of a neural populations activity to accurately model its dynamics on single trials, opening the door to a detailed understanding of the role of dynamics in performing computation and ultimately driving behavior.

neuroscience↗