Neuronal Response Latencies Encode First Odor Identity Information across Subjects (original) (raw)
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Sensory Memory for Odors Is Encoded in Spontaneous Correlated Activity Between Olfactory Glomeruli
Neural Computation, 2006
Sensory memory is a short-lived persistence of a sensory stimulus in the nervous system, such as iconic memory in the visual system. However, little is known about the mechanisms underlying olfactory sensory memory. We have therefore analyzed the effect of odor stimuli on the first odor-processing network in the honeybee brain, the antennal lobe, which corresponds to the vertebrate olfactory bulb. We stained output neurons with a calcium-sensitive dye and measured across-glomerular patterns of spontaneous activity before and after a stimulus. Such a single-odor presentation changed the relative timing of spontaneous activity across glomeruli in accordance with Hebb's theory of learning. Moreover, during the first few minutes after odor presentation, correlations between the spontaneous activity fluctuations suffice to reconstruct the stimulus. As spontaneous activity is ubiquitous in the brain, modifiable fluctuations could provide an ideal substrate for Hebbian reverberations a...
Decorrelation of odor representations via spike timing dependent plasticity
Frontiers in Computational Neuroscience, 2010
The non-topographical representation of odor quality space differentiates early olfactory representations from those in other sensory systems. Decorrelation among olfactory representations with respect to physical odorant similarities has been proposed to rely upon local feed-forward inhibitory circuits in the glomerular layer that decorrelate odor representations with respect to the intrinsically high-dimensional space of ligand-receptor potency relationships. A second stage of decorrelation is likely to be mediated by the circuitry of the olfactory bulb external plexiform layer. Computations in this layer, or in the analogous interneuronal network of the insect antennal lobe, are dependent on fast network oscillations that regulate the timing of mitral cell and projection neuron (MC/PN) action potentials; this suggests a largely spike timingdependent metric for representing odor information, here proposed to be a precedence code. We first illustrate how the rate coding metric of the glomerular layer can be transformed into a spike precedence code in MC/PNs. We then show how this mechanism of representation, combined with spike timing-dependent plasticity at MC/PN output synapses, can progressively decorrelate high-dimensional, non-topographical odor representations in third-layer olfactory neurons. Reducing MC/PN oscillations abolishes the spike precedence code and blocks this progressive decorrelation, demonstrating the learning network's selectivity for these sparsely synchronized MC/PN spikes even in the presence of temporally disorganized background activity. Finally, we apply this model to odor representations derived from calcium imaging in the honeybee antennal lobe, and show how odor learning progressively decorrelates odor representations, and how the abolition of PN oscillations impairs odor discrimination.
Frontiers in cellular neuroscience, 2015
As odor concentration increases, primary olfactory network representations expand in spatial distribution, temporal complexity and duration. However, the direct relationship between concentration dependent odor representations and the psychophysical thresholds of detection and discrimination is poorly understood. This relationship is absolutely critical as thresholds signify transition points whereby representations become meaningful to the organism. Here, we matched stimulus protocols for psychophysical assays and intracellular recordings of antennal lobe (AL) projection neurons (PNs) in the moth Manduca sexta to directly compare psychophysical thresholds and the output representations they elicit. We first behaviorally identified odor detection and discrimination thresholds across an odor dilution series for a panel of structurally similar odors. We then characterized spatiotemporal spiking patterns across a population of individually filled and identified AL PNs in response to th...
Journal of Insect Physiology, 2000
Stimulation with odours has been shown to elicit characteristic patterns of activated glomeruli in the antennal lobe (AL) of honeybees. In this study we show that these patterns are dynamic in a time window of 2-3 s after stimulus onset. We measured changes in the averaged membrane potential of all cells in the glomerular neuropil by optical imaging of the voltage-sensitive dye RH795 using a slow scan CCD camera (3 frames/s). The four substances 1-hexanol, hexanal, citral and clove-oil as well as the binary mixtures hexanol+hexanal and hexanol+citral were used as stimuli (2 s stimulus duration). We found that: (1) every odour elicited an odour-specific activity pattern, and conversely every glomerulus had a characteristic odour response profile; (2) some glomeruli had a tonic, some a phasic-tonic, and some a slow phasic response pattern; (3) the difference between the glomerular response patterns increased within 2 s of stimulus presentation, which suggests that odour representations became more characteristic over stimulus time; and (4) the responses to odorant mixtures were complex and glomerulus-dependent: some responses correspond to the sum of the compounds' responses, some to the response of one of the components.
Journal of Neuroscience, 2010
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.
Journal of Neuroscience, 2004
In the insect antennal lobe, odor discrimination depends on the ability of the brain to read neural activity patterns across arrays of uniquely identifiable olfactory glomeruli. Less is understood about the complex temporal dynamics and interglomerular interactions that underlie these spatial patterns. Using neural-ensemble recording, we show that the evoked firing patterns within and between groups of glomeruli are odor dependent and organized in both space and time. Simultaneous recordings from up to 15 units per ensemble were obtained from four zones of glomerular neuropil in response to four classes of odorants: pheromones, monoterpenoids, aromatics, and aliphatics. Each odor class evoked a different pattern of excitation and inhibition across recording zones. The excitatory response field for each class was spatially defined, but inhibitory activity was spread across the antennal lobe, reflecting a center-surround organization. Some chemically related odorants were not easily distinguished by their spatial patterns, but each odorant evoked transient synchronous firing across a uniquely different subset of ensemble units. Examination of 535 cell pairs revealed a strong relationship between their recording positions, temporal correlations, and similarity of odor response profiles. These findings provide the first definitive support for a nested architecture in the insect olfactory system that uses both spatial and temporal coordination of firing to encode chemosensory signals. The spatial extent of the representation is defined by a stereotyped focus of glomerular activity for each odorant class, whereas the transient temporal correlations embedded within the ensemble provide a second coding dimension that can facilitate discrimination between chemically similar volatiles.
Neural Encoding of Rapidly Fluctuating Odors
Neuron, 2009
Olfactory processing in the insect antennal lobe is a highly dynamic process, yet it has been studied primarily with static step stimuli. To approximate the rapid odor fluctuations encountered in nature, we presented flickering ''white-noise'' odor stimuli to the antenna of the locust and recorded spike trains from antennal lobe projection neurons (PNs). The responses varied greatly across PNs and across odors for the same PN. Surprisingly, this diversity across the population was highly constrained, and most responses were captured by a quantitative model with just 3 parameters. Individual PNs were found to communicate odor information at rates up to 4bits/s.AsmallgroupofPNswassufficienttoprovideanaccuraterepresentationofthedynamicodortimecourse,whosequalitywasmaximalforfluctuationsoffrequency4 bits/s. A small group of PNs was sufficient to provide an accurate representation of the dynamic odor time course, whose quality was maximal for fluctuations of frequency 4bits/s.AsmallgroupofPNswassufficienttoprovideanaccuraterepresentationofthedynamicodortimecourse,whosequalitywasmaximalforfluctuationsoffrequency0.8 Hz. We develop a simple model for the encoding of dynamic odor stimuli that accounts for many prior observations on the population response.
Associative conditioning tunes transient dynamics of early olfactory processing
The Journal of …, 2009
Odors evoke complex spatiotemporal responses in the insect antennal lobe (AL) and mammalian olfactory bulb. However, the behavioral relevance of spatiotemporal coding remains unclear. In the present work we combined behavioral analyses with calcium imaging of odor induced activity in the honeybee AL to evaluate the relevance of this temporal dimension in the olfactory code. We used a new way for evaluation of odor similarity of binary mixtures in behavioral studies, which involved testing whether a match of odor-sampling time is necessary between training and testing conditions for odor recognition during associative learning. Using graded changes in the similarity of the mixture ratios, we found high correlations between the behavioral generalization across those mixtures and a gradient of activation in AL output. Furthermore, short odor stimuli of 500 ms or less affected how well odors were matched with a memory template, and this time corresponded to a shift from a sampling-time-dependent to a sampling-time-independent memory. Accordingly, 375 ms corresponded to the time required for spatiotemporal AL activity patterns to reach maximal separation according to imaging studies. Finally, we compared spatiotemporal representations of binary mixtures in trained and untrained animals. AL activity was modified by conditioning to improve separation of odor representations. These data suggest that one role of reinforcement is to "tune" the AL such that relevant odors become more discriminable.