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Sensitive and robust chemical detection using an olfactory brain-computer interface

Shor, Erez; Herrero-Vidal, Pedro; Dewan, Adam; Uguz, Ilke; Curto, Vincenzo F; Malliaras, George G; Savin, Cristina; Bozza, Thomas; Rinberg, Dmitry
When it comes to detecting volatile chemicals, biological olfactory systems far outperform all artificial chemical detection devices in their versatility, speed, and specificity. 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-computer interface that captures neuronal signals from an early stage of olfactory processing in awake mice combined with 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 that modifies the relative abundance of particular olfactory receptors in order to improve the sensitivity of our bio-electronic nose for specific chemical targets. Our recordings were stable over months, providing evidence for robust and stable decoding over time. The system also works in freely moving animals, allowing chemical detection to occur in real-world environments. Our bio-electronic nose outperforms current methods in terms of its stability, specificity, and versatility, setting a new standard for chemical detection.
PMID: 34624799
ISSN: 1873-4235
CID: 5037662

Olfaction: Source separation in a single sniff

Harvey, Joshua; Rinberg, Dmitry
A new study finds that mammalian olfaction may be far faster than previously thought. Mice can discriminate between olfactory stimuli that differ in fine temporal structure, at frequencies of up to 40 Hz. But how might mammals achieve high-bandwidth olfaction, and why?
PMID: 34520717
ISSN: 1879-0445
CID: 5061352

Precise Holographic Manipulation of Olfactory Circuits Reveals Coding Features Determining Perceptual Detection

Gill, Jonathan V; Lerman, Gilad M; Zhao, Hetince; Stetler, Benjamin J; Rinberg, Dmitry; Shoham, Shy
Sensory systems transform the external world into time-varying spike trains. What features of spiking activity are used to guide behavior? In the mouse olfactory bulb, inhalation of different odors leads to changes in the set of neurons activated, as well as when neurons are activated relative to each other (synchrony) and the onset of inhalation (latency). To explore the relevance of each mode of information transmission, we probed the sensitivity of mice to perturbations across each stimulus dimension (i.e., rate, synchrony, and latency) using holographic two-photon optogenetic stimulation of olfactory bulb neurons with cellular and single-action-potential resolution. We found that mice can detect single action potentials evoked synchronously across <20 olfactory bulb neurons. Further, we discovered that detection depends strongly on the synchrony of activation across neurons, but not the latency relative to inhalation.
PMID: 32841590
ISSN: 1097-4199
CID: 4606572

Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception

Chong, Edmund; Moroni, Monica; Wilson, Christopher; Shoham, Shy; Panzeri, Stefano; Rinberg, Dmitry
How does neural activity generate perception? Finding the combinations of spatial or temporal activity features (such as neuron identity or latency) that are 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 spatiotemporal dimensions. We modeled recognition as the matching of patterns to learned templates. The templates that best predicted recognition were sequences of spatially identified units, ordered by latencies relative to each other (with minimal effects of sniff). Within templates, individual units contributed 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.
PMID: 32554567
ISSN: 1095-9203
CID: 4486312

Information processing by an olfactory functional unit and a primacy coding hypothesis [Meeting Abstract]

Rinberg, D
Olfactory inputs are organized in an array of functional units (glomeruli), each relaying information from sensory neurons expressing a given odorant receptor to a small population of output neurons, mitral/tufted (MT) cells. MT cells respond heterogeneously to odorants, and how the responses encode stimulus features is unknown. We recorded in awake mice responses from "sister" MT cells that receive input from a functionally- characterized, genetically identifed glomerulus, corresponding to a specifc receptor (M72). Despite receiving similar inputs, sister MT cells exhibit temporally diverse, concentration dependent, excitatory and inhibitory responses to most M72 ligands. In contrast, the strongest known ligand for M72 elicits temporally stereotyped, early excitatory responses in sister MT cells, consistent across a range of concentrations. Our data suggest that information about ligand affnity is encoded in the collective stereotypy or diversity of activity among sister MT cells within a glomerular functional unit. These fndings provide an evidence for spe-cifc network mechanisms, which implement a primacy coding model for concentration invariant odor recognition
EMBASE:631449089
ISSN: 0379-864x
CID: 4384382

Discovering Precise Temporal Patterns in Large-Scale Neural Recordings through Robust and Interpretable Time Warping

Williams, Alex H; Poole, Ben; Maheswaranathan, Niru; Dhawale, Ashesh K; Fisher, Tucker; Wilson, Christopher D; Brann, David H; Trautmann, Eric M; Ryu, Stephen; Shusterman, Roman; Rinberg, Dmitry; Ölveczky, Bence P; Shenoy, Krishna V; Ganguli, Surya
Though the temporal precision of neural computation has been studied intensively, a data-driven determination of this precision remains a fundamental challenge. Reproducible spike patterns may be obscured on single trials by uncontrolled temporal variability in behavior and cognition and may not be time locked to measurable signatures in 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 these patterns are decoupled from behavior or are 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, such as 7 Hz oscillations in rat motor cortex that are not time locked to measured behaviors or LFP.
PMID: 31786013
ISSN: 1097-4199
CID: 4292512

Precise optical probing of perceptual detection in olfactory circuits [Meeting Abstract]

Gill, J V; Lerman, G M; Zhao, H; Stetler, B J; Shoham, S; Rinberg, D
Animals are capable of detecting odorants in a single sniff, at extremely low concentrations. This ability is crucial for survival, yet it is unknown how the olfactory system supports detection at the perceptual limit. In the mouse olfactory bulb, inhalation of different odors leads to changes in the set of neurons activated, as well as when neurons are activated relative to each other (synchrony), and the onset of inhalation (latency). A key question is which features of stimulus evoked activity (e.g. rate, synchrony, or latency) are used to guide detection behavior? Here, we probed the sensitivity of mice to perturbations across each stimulus dimension using holographic two-photon (2P) optogenetic stimulation of olfactory bulb neurons, with cellular and single action potential resolution and millisecond precision. We found that mice can detect single action potentials evoked synchronously across <20 olfactory bulb neurons. Mice exhibited this sensitivity for artificial ensembles of mitral cells, as well as mixed ensembles of mitral and granule cells. Further, we discovered that detection depends strongly on the synchrony of activation across neurons, with detectability falling to near-chance levels with an imposed stimulus spread 3 30 ms, while detection performance was minimally perturbed by changes in the latency of activation relative to inhalation. These results reveal that mice are acutely attuned to single neurons and action potentials in olfactory circuits, and that synchrony across neurons may be a critical feature supporting the perceptibility of sparse ensemble activity signals
EMBASE:633611265
ISSN: 0379-864x
CID: 4710402

Encoding of behaviorally relevant synthetic odor objects in the piriform cortex of the mouse [Meeting Abstract]

Herrero-Vidal, P; Chong, E; Savin, C; Rinberg, D
The piriform cortex is the first area of integration for all peripheral odor information and it is believed to generate a unique and wholistic representation of behavioral relevance, sensory object. However, what properties of the cortical neural population activity define odor objects remains unknown. To address this question, we recorded cortical spiking responses to synthetic odors made of fully parameterized optogenetic activity patterns in the olfactory bulb, enabling independent and precise control of the incoming neural responses unattainable with natural odorants. Then, we measured changes in the neural response to a range of controlled spatial and temporal perturbations of the pattern for which we previously established their behavioral relevance. We developed an experimental approach to systematically probe cortical neural activity and found features of the population code which represent behaviorally relevant information
EMBASE:633610915
ISSN: 0379-864x
CID: 4710422

Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception [Meeting Abstract]

Chong, E; Moroni, M; Shoham, S; Panzeri, S; Rinberg, D
How does neural activity generate perception? The spatial identities and temporal latencies of activated units correlate with external sensory features, but finding the subspace of activity that is consequential for perception, remains challenging. We trained mice to recognize synthetic odors: optogenetically-driven spatiotemporal patterns of glomerular activity in the olfactory bulb. We then performed precise spatial or temporal perturbations on trained patterns and measured how recognition changes. Changes in recognition reflect the perceptual relevance of the modified feature. We modeled recognition as the matching of glomerular activity to learned templates, and uncovered what forms a perceptually-meaningful pattern template: activation sequences ordered by latencies relative to each other, with surprisingly minimal effect of sniff. Within templates, spatially-identified glomeruli contribute additively, with larger contributions from earlier-activated glomeruli. Template matching with these perceptually-meaningful features can account for animals' responses, with the degree of mismatch predicting changes in recognition. The model accurately generalizes to novel spatio-temporal manipulations of patterns, and produces non-linear responses that resemble the non-linear responses in the data. This is the first report to our knowledge, that not only establishes a causal role for neural activity sequences in perception, but also uncovers the perceptually-relevant coding schemes governing these sequences. Our synthetic approach reveals the fundamental logic of the olfactory code, and provides a general framework for testing links between sensory activity and perception
EMBASE:633611307
ISSN: 0379-864x
CID: 4710392

Real-Time In Situ Holographic Optogenetics Confocally Unraveled Sculpting Microscopy

Lerman, Gilad M.; Little, Justin P.; Gill, Jonathan V.; Rinberg, Dmitry; Shoham, Shy
Two-photon (2P) optogenetic stimulation is currently the only method for precise, fast, and non-invasive cellular excitation deep inside brain tissue; it is typically combined with holographic wavefront-shaping techniques to generate distributed light patterns and target them to multiple specific cells in the brain. During propagation in the brain, these light patterns undergo severe distortion, mainly due to scattering, which leads to a discrepancy between the desired and actual light distribution. However, despite its importance, measurement of these tissue-induced distortions and their effects on the light patterns has yet to be demonstrated in situ. To this end, holographic optogenetics confocally unraveled sculpting (HOCUS), a system for real-time in situ evaluation of holographic light patterns, based on confocally descanning the stimulation light's reflection from the brain, is developed. HOCUS measures both tissue and wave propagation properties and enables the real-time measurement and correction of the dimensions and positions of holographic spots relative to neurons targeted for stimulation. It can also be used to measure tissue attenuation length, and thus should facilitate future attempts to optimize the generated hologram to pre-compensate for tissue-induced distortions, thereby improving the reliability of 2P holographic stimulation experiments.
SCOPUS:85070735606
ISSN: 1863-8880
CID: 4099662