bioRxiv Science⌕ Search

Biology subjects

Masset, P.

Publications and source records attributed to Masset, P..

9 recordsLinked to original sources

Simultaneous detection and estimation in olfactory sensing

The mammalian olfactory system shows an exceptional ability for rapid and accurate decoding of both the identity and concentration of odorants. Previous works have used the theory of compressed sensing to elucidate the algorithmic basis for this capability: decoding odor information from the responses of a restricted repertoire of receptors is possible because only a few relevant odorants are present in any given sensory scene. However, existing circuit models for olfactory decoding still cannot contend with the complexity of naturalistic olfactory scenes; they are limited to detection of a handful of odorants. Here, we propose a model for olfactory compressed sensing inspired by simultaneous localization and mapping algorithms in navigation, in which the set of present odors and their concentrations are inferred separately. We implement this split inference in a biologically-plausible recurrent circuit by introducing separate dynamics matched to the distinct nature of presence and concentration, and drawing on the framework of Mirrored Langevin Dynamics. This model can accurately infer presence and concentration at scale. Moreover, its circuit structure can be mapped onto the primary cell types of the olfactory bulb, giving a possible normative account for functional differences between mitral and tufted cells. Our approach offers a general path towards circuit algorithms for probabilistic inference--in olfactory sensing and beyond--that both perform well in naturalistic environments and make experimentally-testable predictions for neural response dynamics.

neuroscience↗

Combining Sampling Methods with Attractor Dynamics in Spiking Models of Head-Direction Systems

Uncertainty is a fundamental aspect of the natural environment, requiring the brain to infer and integrate noisy signals to guide behavior effectively. Sampling-based inference has been proposed as a mechanism for dealing with uncertainty, particularly in early sensory processing. However, it is unclear how to reconcile sampling-based methods with operational principles of higher-order brain areas, such as attractor dynamics of persistent neural representations. In this study, we present a spiking neural network model for the head-direction (HD) system that combines sampling-based inference with attractor dynamics. To achieve this, we derive the required spiking neural network dynamics and interactions to perform sampling from a large family of probability distributions--including variables encoded with Poisson noise. We then propose a method that allows the network to update its estimate of the current head direction by integrating angular velocity samples--derived from noisy inputs--with a pull towards a circular manifold, thereby maintaining consistent attractor dynamics. This model makes specific, testable predictions about the HD system that can be examined in future neurophysiological experiments: it predicts correlated subthreshold voltage fluctuations; distinctive short- and long-term firing correlations among neurons; and characteristic statistics of the movement of the neural activity "bump" representing the head direction. Overall, our approach extends previous theories on probabilistic sampling with spiking neurons, offers a novel perspective on the computations responsible for orientation and navigation, and supports the hypothesis that sampling-based methods can be combined with attractor dynamics to provide a viable framework for studying neural dynamics across the brain.

neuroscience↗

Perception and neural representation of intermittent odor stimuli in mice

Odor cues in nature are sparse and highly fluctuating due to turbulent transport. To investigate how animals perceive these intermittent cues, we developed a behavioral task in which head-restrained mice made binary decisions based on the total number of discrete odor pulses presented stochastically over several seconds. Mice readily learned this task, and their performance was well-described by widely used decision models. Logistic regression of binary choices against the timing of odor pulses within the respiratory cycle revealed that mice placed higher perceptual weight to stimuli arriving during inhalation than exhalation, a phase dependency that strongly correlated with the magnitude of responses in olfactory sensory neurons. The population response of anterior piriform cortex (APCx) neurons to odor pulses was also modulated by respiration phase, although individual neurons displayed varying levels of phase-dependence. Single APCx neurons responded stochastically and transiently to odor pulses, leading to a representation that carries signatures of sensory evidence, but not its accumulation. Our study reveals that mice can integrate intermittent odor signals across dozens of breaths, but respiratory modulation of sensory inputs imposes limits on information acquisition that cortical circuits cannot overcome to improve behavior.

neuroscience↗

Bounded optimality of time investments in rats, mice, and humans

Time is our scarcest resource. Allocating time optimally presents a universal challenge for all organisms because the future benefits of time investments are uncertain. We developed a normative framework for assessing bounded optimality in time allocation, emphasizing the accuracy of future predictions, independent of subjective costs and benefits. In a common decision task across humans, rats, and mice, we varied uncertainty by titrating ambiguous sensory evidence and measured the time each subject was willing to invest post-decision. We observed that all species and subjects invested more time when they were more likely to be correct, which reflected a statistical confidence of uncertain evidence. Time allocation strategy approached the lower bound of optimality, indicating an accurate decision-by-decision assessment of confidence in the likelihood that waiting will pay off - independent of the subjective payoff values and time costs. We demonstrate that an elementary algorithm based on a drift-diffusion process algorithm can implement this optimal time investment strategy. These results illuminate the computational mechanisms governing rational time investment, showing that humans, rats, and mice can maximize payoffs via confidence-guided time allocation. HighlightsO_LIComputational and behavioral framework to assess bounded optimality of investments. C_LIO_LIHumans, rats, and mice invest more time to obtain more likely payoffs, in proportion to statistical confidence. C_LIO_LITime investment was close to optimal model predictions, reflecting bounded optimality of investments under uncertainty. C_LIO_LIBounded-optimal time investment may be an evolutionary ancient adaptive behavioral strategy. C_LI

animal behavior and cognition↗

Interpretable deep learning for deconvolutional analysis of neural signals

The widespread adoption of deep learning to build models that capture the dynamics of neural populations is typically based on "black-box" approaches that lack an interpretable link between neural activity and network parameters. Here, we propose to apply algorithm unrolling, a method for interpretable deep learning, to design the architecture of sparse deconvolutional neural networks and obtain a direct interpretation of network weights in relation to stimulus-driven single-neuron activity through a generative model. We characterize our method, referred to as deconvolutional unrolled neural learning (DUNL), and show its versatility by applying it to deconvolve single-trial local signals across multiple brain areas and recording modalities. To exemplify use cases of our decomposition method, we uncover multiplexed salience and reward prediction error signals from midbrain dopamine neurons in an unbiased manner, perform simultaneous event detection and characterization in somatosensory thalamus recordings, and characterize the heterogeneity of neural responses in the piriform cortex and in the striatum during unstructured, naturalistic experiments. Our work leverages the advances in interpretable deep learning to gain a mechanistic understanding of neural activity.

neuroscience↗

Multi-timescale reinforcement learning in the brain

To thrive in complex environments, animals and artificial agents must learn to act adaptively to maximize fitness and rewards. Such adaptive behavior can be learned through reinforcement learning1, a class of algorithms that has been successful at training artificial agents2-6 and at characterizing the firing of dopamine neurons in the midbrain7-9. In classical reinforcement learning, agents discount future rewards exponentially according to a single time scale, controlled by the discount factor. Here, we explore the presence of multiple timescales in biological reinforcement learning. We first show that reinforcement agents learning at a multitude of timescales possess distinct computational benefits. Next, we report that dopamine neurons in mice performing two behavioral tasks encode reward prediction error with a diversity of discount time constants. Our model explains the heterogeneity of temporal discounting in both cue-evoked transient responses and slower timescale fluctuations known as dopamine ramps. Crucially, the measured discount factor of individual neurons is correlated across the two tasks suggesting that it is a cell-specific property. Together, our results provide a new paradigm to understand functional heterogeneity in dopamine neurons, a mechanistic basis for the empirical observation that humans and animals use non-exponential discounts in many situations 10-14, and open new avenues for the design of more efficient reinforcement learning algorithms.

neuroscience↗

Neural circuits for fast Poisson compressed sensing in the olfactory bulb

Within a single sniff, the mammalian olfactory system can decode the identity and concentration of odorants wafted on turbulent plumes of air. Yet, it must do so given access only to the noisy, dimensionally-reduced representation of the odor world provided by olfactory receptor neurons. As a result, the olfactory system must solve a compressed sensing problem, relying on the fact that only a handful of the millions of possible odorants are present in a given scene. Inspired by this principle, past works have proposed normative compressed sensing models for olfactory decoding. However, these models have not captured the unique anatomy and physiology of the olfactory bulb, nor have they shown that sensing can be achieved within the 100-millisecond timescale of a single sniff. Here, we propose a rate-based Poisson compressed sensing circuit model for the olfactory bulb. This model maps onto the neuron classes of the olfactory bulb, and recapitulates salient features of their connectivity and physiology. For circuit sizes comparable to the human olfactory bulb, we show that this model can accurately detect tens of odors within the timescale of a single sniff. We also show that this model can perform Bayesian posterior sampling for accurate uncertainty estimation. Fast inference is possible only if the geometry of the neural code is chosen to match receptor properties, yielding a distributed neural code that is not axis-aligned to individual odor identities. Our results illustrate how normative modeling can help us map function onto specific neural circuits to generate new hypotheses.

neuroscience↗

Population geometry enables fast sampling in spiking neural networks

For animals to navigate an uncertain world, their brains need to estimate uncertainty at the timescales of sensations and actions. Sampling-based algorithms afford a theoretically-grounded framework for probabilistic inference in neural circuits, but it remains unknown how one can implement fast sampling algorithms in biologically-plausible spiking networks. Here, we propose to leverage the population geometry, controlled by the neural code and the neural dynamics, to implement fast samplers in spiking neural networks. We first show that two classes of spiking samplers--efficient balanced spiking networks that simulate Langevin sampling, and networks with probabilistic spike rules that implement Metropolis-Hastings sampling--can be unified within a common framework. We then show that careful choice of population geometry, corresponding to the natural space of parameters, enables rapid inference of parameters drawn from strongly-correlated high-dimensional distributions in both networks. Our results suggest design prin-ciples for algorithms for sampling-based probabilistic inference in spiking neural networks, yielding potential inspiration for neuromorphic computing and testable predictions for neurobiology.

neuroscience↗

Apparent sunk cost effect in rational agents

Rational decision makers aim to maximize their gains, but humans and other animals often fail to do so, exhibiting biases and distortions in their choice behavior. In a recent study of economic decisions, humans, mice, and rats have been reported to succumb to the sunk cost fallacy, making decisions based on irrecoverable past investments in detriment of expected future returns. We challenge this interpretation because it is subject to a statistical fallacy, a form of attrition bias, and the observed behavior can be explained without invoking a sunk cost-dependent mechanism. Using a computational model, we illustrate how a rational decision maker with a reward-maximizing decision strategy reproduces the reported behavioral pattern and propose an improved task design to dissociate sunk costs from fluctuations in decision valuation. Similar statistical confounds may be common in analyses of cognitive behaviors, highlighting the need to use causal statistical inference and generative models for interpretation.

animal behavior and cognition↗