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1.
Nat Neurosci ; 26(12): 2063-2072, 2023 Dec.
Article in English | MEDLINE | ID: mdl-37996525

ABSTRACT

The Bayesian brain hypothesis is one of the most influential ideas in neuroscience. However, unstated differences in how Bayesian ideas are operationalized make it difficult to draw general conclusions about how Bayesian computations map onto neural circuits. Here, we identify one such unstated difference: some theories ask how neural circuits could recover information about the world from sensory neural activity (Bayesian decoding), whereas others ask how neural circuits could implement inference in an internal model (Bayesian encoding). These two approaches require profoundly different assumptions and lead to different interpretations of empirical data. We contrast them in terms of motivations, empirical support and relationship to neural data. We also use a simple model to argue that encoding and decoding models are complementary rather than competing. Appreciating the distinction between Bayesian encoding and Bayesian decoding will help to organize future work and enable stronger empirical tests about the nature of inference in the brain.


Subject(s)
Models, Neurological , Neurosciences , Bayes Theorem , Brain
2.
J Neurophysiol ; 129(5): 1021-1044, 2023 05 01.
Article in English | MEDLINE | ID: mdl-36947884

ABSTRACT

A central goal of systems neuroscience is to understand how populations of sensory neurons encode and relay information to the rest of the brain. Three key quantities of interest are 1) how mean neural activity depends on the stimulus (sensitivity), 2) how neural activity (co)varies around the mean (noise correlations), and 3) how predictive these variations are of the subject's behavior (choice probability). Previous empirical work suggests that both choice probability and noise correlations are affected by task training, with decision-related information fed back to sensory areas and aligned to neural sensitivity on a task-by-task basis. We used Utah arrays to record activity from populations of primary visual cortex (V1) neurons from two macaque monkeys that were trained to switch between two coarse orientation-discrimination tasks. Surprisingly, we find no evidence for significant trial-by-trial changes in noise covariance between tasks, nor do we find a consistent relationship between neural sensitivity and choice probability, despite recording from well-tuned task-sensitive neurons, many of which were histologically confirmed to be in supragranular V1, and despite behavioral evidence that the monkeys switched their strategy between tasks. Thus our data at best provide weak support for the hypothesis that trial-by-trial task-switching induces changes to noise correlations and choice probabilities in V1. However, our data agree with a recent finding of a single "choice axis" across tasks. They also raise the intriguing possibility that choice-related signals in early sensory areas are less indicative of task learning per se and instead reflect perceptual learning that occurs in highly overtrained subjects.NEW & NOTEWORTHY Converging evidence suggests that decision processes affect sensory neural activity, and this has informed numerous theories of neural processing. We set out to replicate and extend previous results on decision-related information and noise correlations in V1 of macaque monkeys. However, in our data, we find little evidence for a number of expected effects. Our null results therefore call attention to differences in task training, stimulus design, recording, and analysis techniques between our and prior studies.


Subject(s)
Visual Cortex , Animals , Visual Cortex/physiology , Macaca mulatta/physiology , Learning , Neurons/physiology , Neurons, Afferent
3.
PLoS Comput Biol ; 18(3): e1009557, 2022 03.
Article in English | MEDLINE | ID: mdl-35259152

ABSTRACT

Perception is often characterized computationally as an inference process in which uncertain or ambiguous sensory inputs are combined with prior expectations. Although behavioral studies have shown that observers can change their prior expectations in the context of a task, robust neural signatures of task-specific priors have been elusive. Here, we analytically derive such signatures under the general assumption that the responses of sensory neurons encode posterior beliefs that combine sensory inputs with task-specific expectations. Specifically, we derive predictions for the task-dependence of correlated neural variability and decision-related signals in sensory neurons. The qualitative aspects of our results are parameter-free and specific to the statistics of each task. The predictions for correlated variability also differ from predictions of classic feedforward models of sensory processing and are therefore a strong test of theories of hierarchical Bayesian inference in the brain. Importantly, we find that Bayesian learning predicts an increase in so-called "differential correlations" as the observer's internal model learns the stimulus distribution, and the observer's behavioral performance improves. This stands in contrast to classic feedforward encoding/decoding models of sensory processing, since such correlations are fundamentally information-limiting. We find support for our predictions in data from existing neurophysiological studies across a variety of tasks and brain areas. Finally, we show in simulation how measurements of sensory neural responses can reveal information about a subject's internal beliefs about the task. Taken together, our results reinterpret task-dependent sources of neural covariability as signatures of Bayesian inference and provide new insights into their cause and their function.


Subject(s)
Learning , Sensation , Bayes Theorem , Brain , Computer Simulation , Learning/physiology , Models, Neurological
4.
PLoS Comput Biol ; 17(11): e1009517, 2021 11.
Article in English | MEDLINE | ID: mdl-34843452

ABSTRACT

Making good decisions requires updating beliefs according to new evidence. This is a dynamical process that is prone to biases: in some cases, beliefs become entrenched and resistant to new evidence (leading to primacy effects), while in other cases, beliefs fade over time and rely primarily on later evidence (leading to recency effects). How and why either type of bias dominates in a given context is an important open question. Here, we study this question in classic perceptual decision-making tasks, where, puzzlingly, previous empirical studies differ in the kinds of biases they observe, ranging from primacy to recency, despite seemingly equivalent tasks. We present a new model, based on hierarchical approximate inference and derived from normative principles, that not only explains both primacy and recency effects in existing studies, but also predicts how the type of bias should depend on the statistics of stimuli in a given task. We verify this prediction in a novel visual discrimination task with human observers, finding that each observer's temporal bias changed as the result of changing the key stimulus statistics identified by our model. The key dynamic that leads to a primacy bias in our model is an overweighting of new sensory information that agrees with the observer's existing belief-a type of 'confirmation bias'. By fitting an extended drift-diffusion model to our data we rule out an alternative explanation for primacy effects due to bounded integration. Taken together, our results resolve a major discrepancy among existing perceptual decision-making studies, and suggest that a key source of bias in human decision-making is approximate hierarchical inference.


Subject(s)
Bias , Decision Making , Perception , Humans , Models, Psychological
5.
Curr Opin Neurobiol ; 46: 84-89, 2017 10.
Article in English | MEDLINE | ID: mdl-28841439

ABSTRACT

The concept of a tuning curve has been central for our understanding of how the responses of cortical neurons depend on external stimuli. Here, we describe how the influence of unobserved internal variables on sensory responses, in particular correlated neural variability, can be understood in a similar framework. We suggest that this will lead to deeper insights into the relationship between stimulus, sensory responses, and behavior. We review related recent work and discuss its implication for distinguishing feedforward from feedback influences on sensory responses, and for the information contained in those responses.


Subject(s)
Brain/physiology , Models, Neurological , Sensory Receptor Cells/physiology , Animals , Humans
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