Associative conditioning tunes transient dynamics of early olfactory processing (original) (raw)
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F1000 - Post-publication peer review of the biomedical literature, 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.
Associative learning modifies neural representations of odors in the insect brain
Nature Neuroscience, 1999
nature neuroscience • volume 2 no 1 • january 1999 articles Learning and memory are crucial for establishing and storing predictive relationships between stimuli, which can serve as the basis for adaptive behavior. As a prerequisite, learning should lead to structural and functional changes in the brain, which may occur at primary sensory centers as well as at central and efferent brain structures 1-6 . Recordings of single central neurons in vertebrates and invertebrates show that associative learning can change cellular response properties 7-10 . However, the consequences of learning for neural networks in vivo are less well understood. A possible approach to the study of learning-based modifications in neural networks involves imaging techniques 1,3 , which can record many neurons in parallel and may thus be used to investigate whole neural networks. Here we used optical imaging to distinguish neural representations for different stimuli during associative conditioning, to study whether associative learning induces persistent changes in sensory networks and, if so, how neural stimulus representations are altered in a sensory center.
Journal of Comparative Physiology A, 2006
Odors elicit spatio-temporal patterns of activity in the olfactory bulb of vertebrates and the antennal lobe of insects. There have been several reports of changes in these patterns following olfactory learning. These studies pose a conundrum: how can an animal learn to efficiently respond to a particular odor with an adequate response, if its primary representation already changes during this process? In this study, we offer a possible solution for this problem. We measured odor-evoked calcium responses in a subpopulation of uniglomerular AL output neurons in honeybees. We show that their responses to odors are remarkably resistant to plasticity following a variety of appetitive olfactory learning paradigms. There was no significant difference in the changes of odor-evoked activity between single and multiple trial forward or backward conditioning, differential conditioning, or unrewarded successive odor stimulation. In a behavioral learning experiment we show that these neurons are necessary for conditioned odor responses. We conclude that these uniglomerular projection neurons are necessary for reliable odor coding and are not modified by learning in this paradigm. The role that other projection neurons play in olfactory learning remains to be investigated.
Neural correlates of odor learning in the honeybee antennal lobe
European Journal of Neuroscience, 2010
Extracellular spiking activity and local field potentials (LFP) were recorded via tetrodes at the output of the antennal lobe (AL) in the honeybee brain during olfactory conditioning. Odors induce reliable rate responses that consist of either phasic-tonic responses, or complex responses with odor-specific profiles. In addition, odors evoke consistent responses of LFP oscillations in the 50-Hz band during the phasic ON-response to odor stimulation, and variable LFP responses at other frequency bands during the sustained response. A principal component analysis of the ensemble activity during differential conditioning consistently indicates the largest changes in response to the learned odor (conditioned stimulus; CS+). Relative LFP power increases for CS+ in the 15-40-Hz frequency band during the sustained response, and decreases for frequencies above 45 Hz. To quantify the relationship between these population responses given by the ensemble spiking activity and LFP, we show that for CS+ the learning-related changes in the degree of the phase-locked spiking activity correlate with the power changes in the corresponding frequency bands. Our results indicate associative plasticity in the AL of the bee leading to both enhancement and decrease of neuronal response rates. LFP power changes and the correlated changes in the locking between spikes and LFP at different frequencies observed for the learned odor serve as further evidence for a learning-induced restructuring of temporal ensemble representations.
Learning modifies odor mixture processing to improve detection of relevant components
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2015
Honey bees have a rich repertoire of olfactory learning behaviors, and they therefore are an excellent model to study plasticity in olfactory circuits. Recent behavioral, physiological, and molecular evidence suggested that the antennal lobe, the first relay of the olfactory system in insects and analog to the olfactory bulb in vertebrates, is involved in associative and nonassociative olfactory learning. Here we use calcium imaging to reveal how responses across antennal lobe projection neurons change after association of an input odor with appetitive reinforcement. After appetitive conditioning to 1-hexanol, the representation of an odor mixture containing 1-hexanol becomes more similar to this odor and less similar to the background odor acetophenone. We then apply computational modeling to investigate how changes in synaptic connectivity can account for the observed plasticity. Our study suggests that experience-dependent modulation of inhibitory interactions in the antennal lob...
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.
Learning Modulates the Ensemble Representations for Odors In Primary Olfactory Networks
Proceedings of the …, 2004
Recent evidence suggests that odor-driven responses in the insect antennal lobe (AL) can be modified by associative and nonassociative processes, as has been shown in the vertebrate olfactory bulb. However, the specific network changes that occur in response to olfactory learning remain unknown. To characterize changes in AL network activity during learning, we developed an in vivo protocol in Manduca sexta that allows continuous monitoring of neural ensembles and feeding behavior over the course of olfactory conditioning. Here, we show that Pavlovian conditioning produced a net recruitment of responsive neural units across the AL that persisted after conditioning. Recruitment only occurred when odor reliably predicted food. Conversely, when odor did not predict food, a net loss of responsive units occurred. Simultaneous measures of feeding responses indicated that the treatment-specific patterns of neural recruitment were positively correlated with changes in the insect's behavioral response to odor. In addition to recruitment, conditioning also produced consistent and profound shifts in the temporal responses of 16% of recorded units. These results show that odor representations in the AL are dynamic and related to olfactory memory consolidation. We furthermore provide evidence that the basis of the learningdependent changes in the AL is not simply an increase in activity in the neural network representing an odorant. Rather, learning produces a restructuring of spatial and temporal components of network responses to odor in the AL.
Behavioral Neuroscience, 2009
Animals sample sensory stimuli for longer periods when they must perform difficult discrimination tasks, implying that the brain's ability to represent stimuli improves as a function of time. Though it is true in other senses, few studies have examined whether increasing sampling time improves olfactory discrimination. In the experiments reported here, we controlled odor sampling time with the goal of testing whether odor concentration affected a honeybee's ability to learn, recognize, and discriminate odors. We observed that increasing sampling time during conditioning and testing improved a honeybee's ability to learn, recognize, and differentiate low concentration (0.0002M) odors. For intermediate (0.02M) concentration odors, both acquisition and recognition improved when stimulus duration was longer, but discrimination was unaffected. Having longer to sample a high concentration (2.0M) stimulus also improved acquisition, but it did not affect the ability to recognize or differentiate odors. Differences in the time taken to respond to the conditioned and novel odors during the test period depended upon the difficulty of the discrimination task. Our results suggest that the sensory coding of molecular identity takes longer for low concentration odors.
A network model for learning-induced changes in odor representation in the antennal lobe
2008
The antennal lobe (AL) is the insect homologue of the olfactory bulb in mammals. As such, it is the first processing station in the insect olfactory system. It has been shown previously that odorant representations change during associative odor learning [1], but contradictory findings have also been published [2]. We recorded Ca 2+-activity of uniglomerular projection neurons (PNs) in the AL of the honeybee Apis mellifera during differential olfactory conditioning. Our results indicate that the activity pattern of PNs in response to odorants can change for the conditioned odor, for the unconditioned odor and for control odors which were not presented during conditioning. We designed a computational model of the glomerular network that can explain the apparent contradiction between the findings we present here and the results reported in [2].
The Journal of experimental biology, 1997
Stimulus intensity is an important determinant for perception, learning and behaviour. We studied the effects of odorant concentration on classical conditioning involving odorants and odorant-mechanosensory compounds using the proboscis-extension reflex in the honeybee. Our results show that high concentrations of odorant (a) support better discrimination in a feature-positive task using rewarded odorant-mechanosensory compounds versus unrewarded mechanosensory stimuli, (b) have a stronger capacity to overshadow learning of a simultaneously trained mechanosensory stimulus, and (c) induce better memory consolidation. Furthermore, honeybees were trained discriminatively to two different concentrations of one odorant. Honeybees are not able to solve this task when presented with rewarded low versus unrewarded high concentrations. Taken together, our results suggest that high concentrations of odorant support stronger associations (are more 'salient') than low concentrations. Ou...