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Rinberg, D.

Publications and source records attributed to Rinberg, D..

15 recordsLinked to original sources

Temporal sequence geometry enables odor recognition and generalization

Neural activity sequences are observed throughout the brain, yet their computational roles remain elusive. In mammalian olfaction, olfactory bulb mitral and tufted cells (MTCs) encode odors with precisely timed activity patterns that tile the respiration cycle. While animals can identify odors independently of concentration within the first 100 milliseconds of inhalation, the structure governing these sequences and the role of activity extending beyond this early window remains unclear. Here, using 2-photon calcium imaging with sub-sniff resolution, we show that odor-evoked MTC sequences propagate as wavefronts through a low-dimensional odor tuning space, where timing is predicted by the tuning similarity between neurons rather than physical location. While early portions of these sequences are concentration-invariant, providing a stable anchor for odor identity, later portions systematically co-activate similarly tuned MTCs across odors, tracing the geometry of the tuning manifold. We propose a role for this later sequential activity in training the piriform cortex to learn perceptually generalizable odor representations. Using a model of Hebbian learning through sequences (HeLSeq), we demonstrate that sequential activity can reinforce synaptic connections from similarly tuned MTCs onto common piriform cortical neurons, enabling rapid generalization to novel odors from the earliest moments of inhalation. These findings support a geometric view of activity sequences and establish a general principle by which temporal sequences scaffold unsupervised manifold learning between brain networks.

neuroscience↗

Order code in the olfactory system.

The ability to recognize odor identity across a wide range of concentrations is essential for natural olfactory behaviors. However, how odor identity is represented in the early olfactory system remains an open question. One theory proposes that glomeruli in the olfactory bulb, along with their associated odorant receptors (ORs), are activated by odorants in a temporal order that conveys information about odor identity. This order code is relatively robust to concentration changes, as the rank order of glomerular activation by a given odorant remains similar across concentrations. Alternatively, the primacy coding theory suggests that odor identity is defined by the most sensitive ORs, those that respond first, collectively referred to as the primacy set. To test these theories, we measured glomerular responses to a large set of odorants in the mouse olfactory bulb using calcium imaging. We found that receptor affinities can be embedded in a low-dimensional space (D = 10) with minimal loss of information. Within this space, we identified two clusters of glomeruli with distinct tuning properties that form independent odor representations. These clusters may correspond to the two phylogenetic classes of ORs, as revealed by both their functional characteristics and anatomical locations. In the OR affinity space, odorants evoke orderly activation waves whose directions can be used to define odor identities in the order coding model. Finally, we compared the order code and primacy model in predicting odor identity both across concentrations and across animals. Despite containing less information overall, the primacy model performed comparably to the order code. We confirmed the primacy models prediction that each receptor tends to contribute to the primacy set of at least one odorant. Analysis of binary odor mixtures revealed that mixture responses lie along geodesic lines connecting their component odors. Together, these findings suggest that odor information in the olfactory bulb may be represented through two complementary coding strategies: the primacy and order codes.

neuroscience↗

Mice and humans evaluate odor stimulus strength using common psychophysical principles

Sensory systems translate physical stimuli from the environment--such as light, sound, or chemicals--into signals that the brain can interpret. Across these systems, the amplitude of a stimulus is represented by its perceived intensity. Although previous research has extensively studied how the brain represents physical stimuli, less is known about how it represents perceptual variables such as stimulus intensity. This is primarily due to the difficulty in measuring perceptual responses in animal models, where neural recordings are more accessible. In this study, we use mouse olfaction as a model system to develop a framework for measuring perceived odor intensity. We begin by employing a two-odor concentration classification task to demonstrate that both mice and humans assess stimulus amplitude using a common perceptual scale. We then show that this scale corresponds to intensity. Finally, we apply this method to determine isointense concentrations of different odorants in mice. Our approach offers a powerful tool for testing hypotheses about the neural mechanisms underlying perceived odor intensity, potentially enhancing our understanding of olfactory processing and its neural substrates.

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Data Science in Olfaction

Advances in neural sensing technology are making it possible to observe the olfactory process in great detail. In this paper, we conceptualize smell from a Data Science and AI perspective, that relates the properties of odorants to how they are sensed and analyzed in the olfactory system from the nose to the brain. Drawing distinctions to color vision, we argue that smell presents unique measurement challenges, including the complexity of stimuli, the high dimensionality of the sensory apparatus, as well as what constitutes ground truth. In the face of these challenges, we argue for the centrality of odorant-receptor interactions in developing a theory of olfaction. Such a theory is likely to find widespread industrial applications, and enhance our understanding of smell, and in the longer-term, how it relates to other senses and language. As an initial use case of the data, we present results using machine learning-based classification of neural responses to odors as they are recorded in the mouse olfactory bulb with calcium imaging. Our larger objective is to create the equivalent of an "MNIST database for olfaction," which we call oMNIST, so that researchers are able to work from a standard dataset to further the state of the art, similar to how the availability of standard datasets catalyzed research in computer vision.

neuroscience↗

Across-animal odor decoding by probabilistic manifold alignment

Identifying the common structure of neural dynamics across subjects is key for extracting unifying principles of brain computation and for many brain machine interface applications. Here, we propose a novel probabilistic approach for aligning stimulus-evoked responses from multiple animals in a common low dimensional manifold and use hierarchical inference to identify which stimulus drives neural activity in any given trial. Our probabilistic decoder is robust to a range of features of the neural responses and significantly outperforms existing neural alignment procedures. When applied to recordings from the mouse olfactory bulb, our approach reveals low-dimensional population dynamics that are odor specific and have consistent structure across animals. Thus, our decoder can be used for increasing the robustness and scalability of neural-based chemical detection.

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A behavioral paradigm for measuring perceptual distances in mice

Perceptual similarities between a specific stimulus and other stimuli of the same modality provide valuable information about the structure and geometry of sensory spaces. While typically a subject of behavioral experiments in humans, perceptual similarities, or distances, are rarely measured in other species. However, understanding the neural computations responsible for sensory representations requires the monitoring and sometime manipulating of neural activity, which is more readily achieved in other experimental models. Here we develop a behavioral paradigm that allows for the quantifying of perceptual similarity between sensory stimuli using mouse olfaction as a model system.

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A mouse bio-electronic nose for sensitive and versatile chemical detection

When it comes to simultaneous versatility, speed, and specificity in detecting volatile chemicals, biological olfactory systems far outperform all artificial chemical detection devices. Consequently, the use of trained animals for chemical detection in security, defense, healthcare, agriculture, and other applications has grown astronomically. However, the use of animals in this capacity requires extensive training and behavior-based communication. Here we propose an alternative strategy, a bio-electronic nose, that capitalizes on the superior capability of the mammalian olfactory system, but bypasses behavioral output by reading olfactory information directly from the brain. We engineered a brain-machine interface that captures neuronal signals from an early stage of olfactory processing in awake mice, and used machine learning techniques to form a sensitive and selective chemical detector. We chronically implanted a grid electrode array on the surface of the mouse olfactory bulb and systematically recorded responses to a large battery of odorants and odorant mixtures across a wide range of concentrations. The bio-electronic nose has a comparable sensitivity to the trained animal and can detect odors on a variable background. We also introduce a novel genetic engineering approach designed to improve the sensitivity of our bio-electronic nose for specific chemical targets. Our bio-electronic nose outperforms current detection methods and unlocks a wide spectrum of civil, medical and environmental applications.

bioengineering↗

Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception

How does neural activity generate perception? The spatial identities and temporal latencies of activated units correlate with external sensory features, but finding the principal activity subspace that is consequential for perception, remains challenging. We trained mice to recognize synthetic odors constructed from parametrically-defined patterns of optogenetic activation, then measured perceptual changes during extensive and controlled perturbations across spatio-temporal dimensions. We modelled recognition as the matching of patterns to learned templates, finding that perceptually-meaningful templates are sequences of spatially-identified units, ordered by latencies relative to each other (with minimal effects of sniff). Within templates, individual units contribute additively, with larger contributions from earlier-activated units. Our synthetic approach reveals the fundamental logic of the olfactory code, and provides a general framework for testing links between sensory activity and perception.

neuroscience↗

Discovering precise temporal patterns in large-scale neural recordings through robust and interpretable time warping

Though the temporal precision of neural computation has been studied intensively, a data-driven determination of this precision remains a fundamental challenge. Reproducible spike time patterns may be obscured on single trials by uncontrolled temporal variability in behavior and cognition, or may not even be time locked to measurable signatures in either behavior or local field potentials (LFP). To overcome these challenges, we describe a general-purpose time warping framework that reveals precise spike-time patterns in an unsupervised manner, even when spiking is decoupled from behavior or is temporally stretched across single trials. We demonstrate this method across diverse systems: cued reaching in nonhuman primates, motor sequence production in rats, and olfaction in mice. This approach flexibly uncovers diverse dynamical firing patterns, including pulsatile responses to behavioral events, LFP-aligned oscillatory spiking, and even unanticipated patterns, like 7 Hz oscillations in rat motor cortex that are not time-locked to measured behaviors or LFP.

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Precise optical probing of perceptual detection

Establishing causal links between patterns of neuronal activity and perception is crucial for understanding brain function. Electrical and optogenetic stimulation experiments demonstrated that animals can detect activation of a few neurons. However, these methodologies offer very limited control of ensemble activity and yielded highly divergent thresholds. Here, we use holographic two-photon (2P) optogenetic stimulation to probe the detection of evoked neuronal activity at cellular and single action potential resolution, with millisecond precision. We find that mice can detect single action potentials evoked synchronously across <20 olfactory bulb neurons, while ruling out detection of indirect effects using a novel optical sham-photostimulation technique. Our results demonstrate that mice are acutely attuned to sparse, synchronous ensemble activity signals, introducing order-of-magnitude revisions to earlier estimates of perceptual thresholds.

neuroscience↗

Single olfactory receptors set odor detection thresholds

In many species, survival depends on olfaction, yet the mechanisms that underlie olfactory sensitivity are not well understood. Here, we examine how a conserved subset of olfactory receptors, the trace amine-associated receptors (TAARs) determine odor detection thresholds of mice to amines. We find that deleting all TAARs, or even single TAARs, results in significant odor detection deficits. This finding is not limited to TAARs, as the deletion of a canonical odorant receptor reduced behavioral sensitivity to its preferred ligand. Remarkably, behavioral threshold is set solely by the most sensitive receptor, with no contribution from other highly sensitive receptors. In addition, increasing the number of sensory neurons (and glomeruli) expressing a threshold-determining TAAR does not improve detection, indicating that sensitivity is not limited by the typical complement of sensory neurons. Our findings demonstrate that olfactory thresholds are set by the single highest affinity receptor, and suggest that TAARs are evolutionarily conserved because they determine the sensitivity to a class of biologically relevant chemicals.

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Primacy model and the evolution of the olfactory receptor repertoire

Understanding sensory processing relies on establishing a consistent relationship between the stimulus space, its neural representation, and perceptual quality. In olfaction, the difficulty in establishing these links lies partly in the complexity of the underlying odor input space and perceptual responses. Based on the recently proposed primacy code for concentration invariant odor identity representation and a few assumptions, we have developed a theoretical framework for mapping the odor input space to the response properties of olfactory receptors. We analyze a geometrical structure containing odor representations in a multidimensional space of receptor affinities and describe its low-dimensional implementation, the primacy hull. We propose the implications of the primacy hull for the structure of feedforward connectivity in early olfactory networks. We test the predictions of our theory by comparing the existing receptor-ligand affinity and connectivity data obtained in the fruit fly olfactory system. We find that the Kenyon cells of the insect mushroom body integrate inputs from the high-affinity (primacy) sets of olfactory receptors in agreement with the primacy theory.

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Sniff invariant odor coding

Sampling regulates stimulus intensity and temporal dynamics at the sense organ. Despite variations in sampling behavior, animals must make veridical perceptual judgments about external stimuli. In olfaction, odor sampling varies with respiration, which influences neural responses at the olfactory periphery. Nevertheless, rats were able to perform fine odor intensity judgments despite variations in sniff kinetics. To identify the features of neural activity supporting stable intensity perception, in awake mice we measured responses of Mitral/Tufted (MT) cells to different odors and concentrations across a range of sniff frequencies. Amplitude and latency of the MT cells responses vary with sniff duration. A fluid dynamics (FD) model based on odor concentration kinetics in the intranasal cavity can account for this variability. Eliminating sniff waveform dependence of MT cell responses using the FD model significantly improves concentration decoding. This suggests potential schemes for sniff waveform invariant odor concentration coding.\n\nHighlightsO_LIOdor concentration discrimination does not depend on sniff frequency\nC_LIO_LIAmplitude and latency of MT cell responses vary with sniff frequency\nC_LIO_LIA fluid dynamic based model accounts for sniff dependent variability in the responses\nC_LIO_LITransforming MT cell responses with this model achieves sniff invariant coding\nC_LI

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Stimulus Dependent Diversity And Stereotypy In The Output Of An Olfactory Functional Unit

Olfactory inputs are organized in an array of parallel functional units (glomeruli), each relaying information from sensory neurons that express a given odorant receptor to a small population of output neurons, mitral/tufted (MT) cells. MT cells have complex temporal responses to odorants, but how these diverse responses relate to stimulus features is not known. We recorded in awake mice responses from \"sister\" MT cells that receive input from a functionally-characterized, genetically identified glomerulus, corresponding to a specific receptor (M72). Despite receiving similar inputs, sister MT cells exhibited temporally diverse, concentration variant, excitatory and inhibitory responses to most M72 ligands. In contrast, the strongest known ligand for M72 elicited temporally-stereotyped, early excitatory responses in all sister MT cells that persisted across all odor concentrations. Our data demonstrate that information about ligand affinity is encoded in the collective stereotypy or diversity of activity among sister MT cells within a glomerular functional unit in concentration-independent manner.

neuroscience↗

Concentration invariant odor coding

Humans can identify visual objects independently of view angle and lighting, words independently of volume and pitch, and smells independently of concentration. The computational principles underlying invariant object recognition remain mostly unknown. Here we propose that, in olfaction, a small and relatively stable set made of the earliest activated receptors forms a code for concentration invariant odor identity. One prediction of this \"primacy coding\" scheme is that decisions based on odor identity can be made solely using early odor-evoked neural activity. Using an optogenetic masking paradigm, we define the sensory integration time necessary for odor identification and demonstrate that animals can use information occurring <100 ms after inhalation onset to identify odors. Using multi-electrode array recordings of odor responses in the olfactory bulb, we find that concentration invariant units respond earliest and at latencies that are within this behaviorally-defined time window. We propose a computational model demonstrating how such a code can be read by neural circuits of the olfactory system.

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