Coupled Decision Processes Update and Maintain Saccadic Priors in a Dynamic Environment.

Much of what we know about how the brain forms decisions comes from studies of saccadic eye movements. However, saccadic decisions are often studied in isolation, which limits the insights that they can provide about real-world decisions with complex interdependencies. Here, we used a serial reaction time (RT) task to show that prior expectations affect RTs via interdependent, normative decision processes that operate within and across saccades. We found that human subjects performing the task generated saccades that were governed by a rise-to-threshold decision process with a starting point that reflected expected state-dependent transition probabilities. These probabilities depended on decisions about the current state (the correct target) that, under some conditions, required the accumulation of information across saccades. Without additional feedback, this information was provided by each saccadic decision threshold, which represented the total evidence in favor of the chosen target. Therefore, the output of the within-saccade process was used, not only to generate the saccade, but also to provide input to the across-saccade process. This across-saccade process, in turn, helped to set the starting point of the next within-saccade process. These results imply a novel role for functional information-processing loops in optimizing saccade generation in dynamic environments.SIGNIFICANCE STATEMENT Saccades are the rapid, ballistic eye movements that we make approximately three times every second to scan the visual scene for interesting things to look at. The apparent ease with which we produce saccades belies their computational sophistication, which can be studied quantitatively in the laboratory to provide insights into how our brain manages the interplay between sensory input and motor output. The present work is important because we show for the first time how this interplay operates both within and across saccades to ensure that these eye movements are guided effectively by learned expectations in dynamic environments. More generally, this study shows how sensory-motor decision processes, typically studied in isolation, interact via functional information-processing loops in the brain to produce complex, adaptive behaviors.

Flow-field inference from neural data using deep recurrent networks.

Computations involved in processes such as decision-making, working memory, and motor control are thought to emerge from the dynamics governing the collective activity of neurons in large populations. But the estimation of these dynamics remains a significant challenge. Here we introduce Flow-field Inference from Neural Data using deep Recurrent networks (FINDR), an unsupervised deep learning method that can infer low-dimensional nonlinear stochastic dynamics underlying neural population activity. Using population spike train data from frontal brain regions of rats performing an auditory decision-making task, we demonstrate that FINDR outperforms existing methods in capturing the heterogeneous responses of individual neurons. We further show that FINDR can discover interpretable low-dimensional dynamics when it is trained to disentangle task-relevant and irrelevant components of the neural population activity. Importantly, the low-dimensional nature of the learned dynamics allows for explicit visualization of flow fields and attractor structures. We suggest FINDR as a powerful method for revealing the low-dimensional task-relevant dynamics of neural populations and their associated computations.

Transitions in dynamical regime and neural mode underlie perceptual decision-making.

Perceptual decision-making is the process by which an animal uses sensory stimuli to choose an action or mental proposition. This process is thought to be mediated by neurons organized as attractor networks 1,2 . However, whether attractor dynamics underlie decision behavior and the complex neuronal responses remains unclear. Here we use an unsupervised, deep learning-based method to discover decision-related dynamics from the simultaneous activity of neurons in frontal cortex and striatum of rats while they accumulate pulsatile auditory evidence. We show that contrary to prevailing hypotheses, attractors play a role only after a transition from a regime in the dynamics that is strongly driven by inputs to one dominated by the intrinsic dynamics. The initial regime mediates evidence accumulation, and the subsequent intrinsic-dominant regime subserves decision commitment. This regime transition is coupled to a rapid reorganization in the representation of the decision process in the neural population (a change in the "neural mode" along which the process develops). A simplified model approximating the coupled transition in the dynamics and neural mode allows inferring, from each trial's neural activity, the internal decision commitment time in that trial, and captures diverse and complex single-neuron temporal profiles, such as ramping and stepping 3-5 . It also captures trial-averaged curved trajectories 6-8 , and reveals distinctions between brain regions. Our results show that the formation of a perceptual choice involves a rapid, coordinated transition in both the dynamical regime and the neural mode of the decision process, and suggest pairing deep learning and parsimonious models as a promising approach for understanding complex data.