Baranidharan Raman

Sparse odor representation and olfactory learning.

Sensory systems create neural representations of environmental stimuli and these representations can be associated with other stimuli through learning. Are spike patterns the neural representations that get directly associated with reinforcement during conditioning? In the moth Manduca sexta, we found that odor presentations that support associative conditioning elicited only one or two spikes on the odors onset (and sometimes offset) in each of a small fraction of Kenyon cells. Using associative conditioning procedures that effectively induced learning and varying the timing of reinforcement relative to spiking in Kenyon cells, we found that odor-elicited spiking in these cells ended well before the reinforcement was delivered. Furthermore, increasing the temporal overlap between spiking in Kenyon cells and reinforcement presentation actually reduced the efficacy of learning. Thus, spikes in Kenyon cells do not constitute the odor representation that coincides with reinforcement, and Hebbian spike timing–dependent plasticity in Kenyon cells alone cannot underlie this learning.

Temporally Diverse Firing Patterns in Olfactory Receptor Neurons Underlie Spatiotemporal Neural Codes for Odors

Odorants are represented as spatiotemporal patterns of spikes in neurons of the antennal lobe (AL; insects) and olfactory bulb (OB; vertebrates). These response patterns have been thought to arise primarily from interactions within the AL/OB, an idea supported, in part, by the assumption that olfactory receptor neurons (ORNs) respond to odorants with simple firing patterns. However, activating the AL directly with simple pulses of current evoked responses in AL neurons that were much less diverse, complex, and enduring than responses elicited by odorants. Similarly, models of the AL driven by simplistic inputs generated relatively simple output. How then are dynamic neural codes for odors generated? Consistent with recent results from several other species, our recordings from locust ORNs showed a great diversity of temporal structure. Furthermore, we found that, viewed as a population, many response features of ORNs were remarkably similar to those observed within the AL. Using a set of computational models constrained by our electrophysiological recordings, we found that the temporal heterogeneity of responses of ORNs critically underlies the generation of spatiotemporal odor codes in the AL. A test then performed in vivo confirmed that, given temporally homogeneous input, the AL cannot create diverse spatiotemporal patterns on its own; however, given temporally heterogeneous input, the AL generated realistic firing patterns. Finally, given the temporally structured input provided by ORNs, we clarified several separate, additional contributions of the AL to olfactory information processing. Thus, our results demonstrate the origin and subsequent reformatting of spatiotemporal neural codes for odors.

Frequency Transitions in Odor-Evoked Neural Oscillations

In many species, sensory stimuli elicit the oscillatory synchronization of groups of neurons. What determines the properties of these oscillations? In the olfactory system of the moth, we found that odors elicited oscillatory synchronization through a neural mechanism like that described in locust and Drosophila. During responses to long odor pulses, oscillations suddenly slowed as net olfactory receptor neuron (ORN) output decreased; thus, stimulus intensity appeared to determine oscillation frequency. However, changing the concentration of the odor had little effect upon oscillatory frequency. Our recordings in vivo and computational models based on these results suggested that the main effect of increasing odor concentration was to recruit additional, less well-tuned ORNs whose firing rates were tightly constrained by adaptation and saturation. Thus, in the periphery, concentration is encoded mainly by the size of the responsive ORN population, and oscillation frequency is set by the adaptation and saturation of this response.

A spatiotemporal coding mechanism for background-invariant odor recognition

Sensory stimuli evoke neural activity that evolves over time. What features of these spatiotemporal responses allow the robust encoding of stimulus identity in a multistimulus environment? Here we examined this issue in the locust (Schistocerca americana) olfactory system. We found that sensory responses evoked by an odorant (foreground) varied when presented atop or after an ongoing stimulus (background). These inconsistent sensory inputs triggered dynamic reorganization of ensemble activity in the downstream antennal lobe. As a result, partial pattern matches between neural representations encoding the same foreground stimulus across conditions were achieved. The degree and segments of response overlaps varied; however, any overlap observed was sufficient to drive background-independent responses in the downstream neural population. Notably, recognition performance of locusts in behavioral assays correlated well with our physiological findings. Hence, our results reveal how background-independent recognition of odors can be achieved using spatiotemporal patterns of neural activity.

Detecting Chemical Hazards with Temperature-Programmed Microsensors: Overcoming Complex Analytical Problems with Multidimensional Databases*

Complex analytical problems, such as detecting trace quantities of hazardous chemicals in challenging environments, require solutions that most effectively extract relevant information about a samples composition. This review presents a chemiresistive microarray-based approach to identifying targets that combines temperature-programmed elements capable of rapidly generating analytically rich data sets with statistical pattern recognition algorithms for extracting multivariate chemical fingerprints. We describe the chemical-microsensor platform and discuss its ability to generate orthogonal data through materials selection and temperature programming. Visual inspection of data sets reveals device selectivity, but statistical analyses are required to perform more complex identification tasks. Finally, we discuss recent advances in both devices and algorithms necessary to deal with practical issues involved in long-term deployment. These issues include identification and correction of signal drift, challenges surrounding real-time unsupervised operation, repeatable device manufacturability, and hierarchical classification schemes designed to deduce the chemical composition of untrained analyte species.

Processing of chemical sensor arrays with a biologically inspired model of olfactory coding

This paper presents a computational model for chemical sensor arrays inspired by the first two stages in the olfactory pathway: distributed coding with olfactory receptor neurons and chemotopic convergence onto glomerular units. We propose a monotonic concentration-response model that maps conventional sensor-array inputs into a distributed activation pattern across a large population of neuroreceptors. Projection onto glomerular units in the olfactory bulb is then simulated with a self-organizing model of chemotopic convergence. The pattern recognition performance of the model is characterized using a database of odor patterns from an array of temperature modulated chemical sensors. The chemotopic code achieved by the proposed model is shown to improve the signal-to-noise ratio available at the sensor inputs while being consistent with results from neurobiology.

Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications

In this paper, we present recent work on bioinspired polarization imaging sensors and their applications in biomedicine. In particular, we focus on three different aspects of these sensors. First, we describe the electro-optical challenges in realizing a bioinspired polarization imager, and in particular, we provide a detailed description of a recent low-power complementary metal-oxide-semiconductor (CMOS) polarization imager. Second, we focus on signal processing algorithms tailored for this new class of bioinspired polarization imaging sensors, such as calibration and interpolation. Third, the emergence of these sensors has enabled rapid progress in characterizing polarization signals and environmental parameters in nature, as well as several biomedical areas, such as label-free optical neural recording, dynamic tissue strength analysis, and early diagnosis of flat cancerous lesions in a murine colorectal tumor model. We highlight results obtained from these three areas and discuss future applications for these sensors.

Olfactory learning and spike timing dependent plasticity

Hebbian spike-timing-dependent plasticity (STDP) is widely observed in organisms ranging from insects to humans and may provide a cellular mechanism for associative learning. STDP requires a millisecond scale temporal correlation of spiking activity in pre- and postsynaptic neurons. However, animals can learn to associate a sensory cue and a reward that are presented seconds apart. Thus, for STDP to mediate associative learning, the brain must retain information about the sensory cue as spiking activity until the reinforcement signal arrives. In our recent study, we tested this requirement in the moth Manduca sexta. We characterized the odor responses of Kenyon cells, a key neuronal population for insect olfactory learning, and conditioned moths to associate an odor with a sugar water reward. By varying the amount of overlap between odor-evoked spikes and the reward presentation, we found that the most learning occurred when spiking activity had no overlap with the reward presentation; further, increasing the overlap actually decreased the learning efficacy. Thus, STDP alone cannot mediate the olfactory learning in Kenyon cells. Here, we discuss possible cellular mechanisms that could bridge the temporal gap between physiological and behavioral time scales.

Sensor-based machine olfaction with a neurodynamics model of the olfactory bulb

We propose a biologically inspired model of olfactory processing for chemosensor arrays. The model captures three functions in the early olfactory pathway: chemotopic convergence of receptor neurons onto the olfactory bulb, center on-off surround lateral interactions, and adaptation to sustained stimuli. The projection of ORNs onto glomerular units is simulated with a self-organizing model of chemotopic convergence, which leads to odor specific spatial patterning. This information serves as an input to a network of mitral cells with center on-off surround lateral inhibition, which enhances the initial contrast among odors and decouples odor identity from intensity. Finally, slow adaptation of mitral cells adds a temporal dimension to the spatial patterns that further enhances odor discrimination. The model is validated using experimental data from an array of temperature-modulated metal-oxide sensors.

Behavioural correlates of combinatorial versus temporal features of odour codes

Most sensory stimuli evoke spiking responses that are distributed across neurons and are temporally structured. Whether the temporal structure of ensemble activity is modulated to facilitate different neural computations is not known. Here, we investigated this issue in the insect olfactory system. We found that an odourant can generate synchronous or asynchronous spiking activity across a neural ensemble in the antennal lobe circuit depending on its relative novelty with respect to a preceding stimulus. Regardless of variations in temporal spiking patterns, the activated combinations of neurons robustly represented stimulus identity. Consistent with this interpretation, locusts reliably recognized both solitary and sequential introductions of trained odourants in a quantitative behavioural assay. However, predictable behavioural responses across locusts were observed only to novel stimuli that evoked synchronized spiking patterns across neural ensembles. Hence, our results indicate that the combinatorial ensemble response encodes for stimulus identity, whereas the temporal structure of the ensemble response selectively emphasizes novel stimuli.