Temporal-to-spatial dynamic mapping,flexible recognition,and temporal correlations in an olfactory cortex model

 This paper proposes temporal-to-spatial dynamic mapping inspired by neural dynamics of the olfactory cortex. In our model the temporal structure of olfactory-bulb patterns is mapped to the spatial dynamics of the ensemble of cortical neurons. This mapping is based on the following biological mechanism: while anterior part of piriform cortex can be excited by the afferent input alone, the posterior areas require both afferent and association signals, which are temporally correlated in a specific way. One of the functional types of the neurons in our model corresponds to the cortical spatial dynamics and encodes odor components, and another represents temporal activity of association-fiber signals, which, we suggest, may be relevant to the encoding of odor concentrations. The temporal-to-spatial mapping and distributed representation of the model enable simultaneous rough cluster classification and fine recognition of patterns within a cluster as parts of the same dynamic process. The model is able to extract and segment the components of complex odor patterns which are spatiotemporal sequences of neural activity. Received: 16 October 2001 / Accepted in revised form: 7 February 2002     

Friends and foes from an ant brain's point of view--neuronal correlates of colony odors in a social insect

Background

Successful cooperation depends on reliable identification of friends and foes. Social insects discriminate colony members (nestmates/friends) from foreign workers (non-nestmates/foes) by colony-specific, multi-component colony odors. Traditionally, complex processing in the brain has been regarded as crucial for colony recognition. Odor information is represented as spatial patterns of activity and processed in the primary olfactory neuropile, the antennal lobe (AL) of insects, which is analogous to the vertebrate olfactory bulb. Correlative evidence indicates that the spatial activity patterns reflect odor-quality, i.e., how an odor is perceived. For colony odors, alternatively, a sensory filter in the peripheral nervous system was suggested, causing specific anosmia to nestmate colony odors. Here, we investigate neuronal correlates of colony odors in the brain of a social insect to directly test whether they are anosmic to nestmate colony odors and whether spatial activity patterns in the AL can predict how odor qualities like “friend” and “foe” are attributed to colony odors.

Methodology/Principal Findings

Using ant dummies that mimic natural conditions, we presented colony odors and investigated their neuronal representation in the ant Camponotus floridanus. Nestmate and non-nestmate colony odors elicited neuronal activity: In the periphery, we recorded sensory responses of olfactory receptor neurons (electroantennography), and in the brain, we measured colony odor specific spatial activity patterns in the AL (calcium imaging). Surprisingly, upon repeated stimulation with the same colony odor, spatial activity patterns were variable, and as variable as activity patterns elicited by different colony odors.

Conclusions

Ants are not anosmic to nestmate colony odors. However, spatial activity patterns in the AL alone do not provide sufficient information for colony odor discrimination and this finding challenges the current notion of how odor quality is coded. Our result illustrates the enormous challenge for the nervous system to classify multi-component odors and indicates that other neuronal parameters, e.g., precise timing of neuronal activity, are likely necessary for attribution of odor quality to multi-component odors.     

A neural mechanism of hierarchical discrimination of odors in the olfactory cortex based on spatiotemporal encoding of odor information

We propose a neural mechanism for discrimination of different complex odors in the olfactory cortex based on the dynamical encoding scheme. Both constituent molecules of the odor and their mixing ratios are encoded simultaneously into a spatiotemporal activity pattern (limit cycle attractor) in the olfactory bulb [Hoshino O, Kashimori Y, Kambara T (1998) Biol Cybern 79:109–120]. We present a functional model of the olfactory cortex consisting of some dynamical mapping modules. Each dynamical map is represented by itinerancy among the limit cycle attractors. When a temporal sequence of spatial activity patterns corresponding to a complex odor is injected from the bulb to the network of the olfactory cortex, the neural activity state of each mapping module is fixed to a relevant spatial pattern injected. Recognition of an odor is accomplished by a combination of firing patterns fixed in all the mapping modules. The stronger the response strength of the component, the earlier the component is recognized. The hierarchical discrimination of an odor is made by recognizing the components in order of decreasing response strengths. Received: 28 November 1998 / Accepted in revised form: 17 December 1999     

An olfactory recognition model based on spatio-temporal encoding of odor quality in the olfactory bulb

In order to study the problem how the olfactory neural system processes the odorant molecular information for constructing the olfactory image of each object, we present a dynamic model of the olfactory bulb constructed on the basis of well-established experimental and theoretical results. The information relevant to a single odor, i.e. its constituent odorant molecules and their mixing ratios, are encoded into a spatio-temporal pattern of neural activity in the olfactory bulb, where the activity pattern corresponds to a limit cycle attractor in the mitral cell network. The spatio-temporal pattern consists of a temporal sequence of spatial firing patterns: each constituent molecule is encoded into a single spatial pattern, and the order of magnitude of the mixing ratio is encoded into the temporal sequence. The formation of a limit cycle attractor under the application of a novel odor is carried out based on the intensity-to-time-delay encoding scheme. The dynamic state of the olfactory bulb, which has learned many odors, becomes a randomly itinerant state in which the current firing state of the bulb itinerates randomly among limit cycle attractors corresponding to the learned odors. The recognition of an odor is generated by the dynamic transition in the network from the randomly itinerant state to a limit cycle attractor state relevant to the odor, where the transition is induced by the short-term synaptic changes made according to the Hebbian rule under the application of the odor stimulus. Received: 28 July 1997 / Accepted in revised form: 6 May 1998     

Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb

We explored the spatio-temporal dynamics of odor-evoked activity in the rat and mouse main olfactory bulb (MOB) using voltage-sensitive dye imaging (VSDI) with a new probe. The high temporal resolution of VSDI revealed odor-specific sequences of glomerular activation. Increasing odor concentrations reduced response latencies, increased response amplitudes, and recruited new glomerular units. However, the sequence of glomerular activation was maintained. Furthermore, we found distributed MOB activity locked to the nasal respiration cycle. The spatial distribution of its amplitude and phase was heterogeneous and changed by sensory input in an odor-specific manner. Our data show that in the mammalian olfactory bulb, odor identity and concentration are represented by spatio-temporal patterns, rather than spatial patterns alone.     

Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb

Input from olfactory receptor neurons is first organized and processed in the glomerular layer of the olfactory bulb. Olfactory glomeruli serve as functional units in coding olfactory information and contain a complex network of synaptic connections. Odor information has long been thought to be represented by spatial patterns of glomerular activation; recent work has, additionally, shown that these patterns are temporally dynamic. At the same time, recent advances in our understanding of the glomerular network suggest that glomerular processing serves to temporally sharpen these dynamics and to modulate spatial patterns of glomerular activity. We speculate that odor representations and their postsynaptic processing are tuned to and shaped by the sniffing behavior of the animal.     

Genetic manipulation of the odor-evoked distributed neural activity in the Drosophila mushroom body

Odor-induced neural activity was recorded by Ca2+ imaging in the cell body region of the Drosophila mushroom body (MB), which is the second relay of the olfactory central nervous system. The signals recorded are mainly from the cell layers on the brain surface because of the limited penetration of Ca2+-sensitive dyes. The densely packed cell bodies and their accessibility allow visualization of odor-induced population neural activity. It is revealed that odors evoke diffused neural activities in the MB. Although the signals cannot be attributed to individual neurons, patterns of the population neural activity can be analyzed. The activity pattern, but not the amplitude, of an odor-induced population response is specific for the chemical identity of an odor and its concentration. The distribution pattern of neural activity can be altered specifically by genetic manipulation of an odor binding protein and this alteration is closely associated with a behavioral defect of odor preference. These results suggest that the spatial pattern of the distributed neural activity may contribute to coding of odor information at the second relay of the olfactory system.     

Neural and behavioral changes in rats following continuous exposure to an odor

Summary Continuous exposure of young rats to the almond-like odor of acetophenone or cyclohexanone for up to 4 months, resulted in distinct but similar patterns of degenerating mitral cells in their olfactory bulbs. Rats favored their exposure odor in olfactory preference tests (Fig. 2) and their acuity for it was not altered (Fig. 3). However, they appeared to exhibit a deficit in detecting a similar but novel odor. The results suggest that the remaining normal mitral cells in the bulbs of these animals are those stimulated by the exposure odor. Cells which show signs of degeneration (Fig. 4) may receive little or no input from the periphery. Controls exposed to a similar but non-odorous environment showed evidence of non-selective mitral cell degeneration. In addition they had a lower acuity for acetophenone and cyclohexanone than animals reared in a normal rat colony (Fig. 3). Anatomical and behavioral data from odor exposed and control groups, suggest that partial regeneration of altered mitral cells may have occurred during a 5 month period following exposure. Overall the results provide further evidence for a topographical projection of the olfactory receptor epithelium onto the olfactory bulb and spatial coding of different odors in the bulb.     

Adjusting neurophysiological computations in the adult olfactory bulb

The olfactory bulb receives signals from olfactory sensory neurons and conveys them to higher centers. The mapping of the sensory inputs generates a reproducible spatial pattern in the glomerular layer of the olfactory bulb for each odorant. Then, this restricted activation is transformed into highly distributed patterns by lateral interactions between relay neurons and local interneurons. Thus, odor information processing requires the spatial patterning of both sensory inputs and synaptic interactions. In other words, odor representation is highly dynamic and temporally orchestrated. Here, we describe how the local inhibitory network shapes the global oscillations and the precise synchronization of relay neurons. We discuss how local inhibitory interneurons transpose the spatial dimension into temporal patterning. Remarkably, this transposition is not fixed but highly flexible to continuously optimize olfactory information processing.     

Representation of the glomerular olfactory map in the Drosophila brain

We explored how the odor map in the Drosophila antennal lobe is represented in higher olfactory centers, the mushroom body and lateral horn. Systematic single-cell tracing of projection neurons (PNs) that send dendrites to specific glomeruli in the antennal lobe revealed their stereotypical axon branching patterns and terminal fields in the lateral horn. PNs with similar axon terminal fields tend to receive input from neighboring glomeruli. The glomerular classes of individual PNs could be accurately predicted based solely on their axon projection patterns. The sum of these patterns defines an "axon map" in higher olfactory centers reflecting which olfactory receptors provide input. This map is characterized by spatial convergence and divergence of PN axons, allowing integration of olfactory information.     

Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment

In the olfactory bulb of vertebrates or the homologous antennal lobe of insects, odor quality is represented by stereotyped patterns of neuronal activity that are reproducible within and between individuals. Using optical imaging to monitor synaptic activity in the Drosophila antennal lobe, we show here that classical conditioning rapidly alters the neural code representing the learned odor by recruiting new synapses into that code. Pairing of an odor-conditioned stimulus with an electric shock-unconditioned stimulus causes new projection neuron synapses to respond to the odor along with those normally activated prior to conditioning. Different odors recruit different groups of projection neurons into the spatial code. The change in odor representation after conditioning appears to be intrinsic to projection neurons. The rapid recruitment by conditioning of new synapses into the representation of sensory information may be a general mechanism underlying many forms of short-term memory.     

Firing pattern and synchronization property analysis in a network model of the olfactory bulb

In the olfactory system, both the temporal spike structure and spatial distribution of neuronal activity are important for processing odor information. In this paper, a biophysically-detailed, spiking neuronal model is used to simulate the activity of olfactory bulb. It is shown that by varying some key parameters such as maximal conductances of Ks and Nap the spike train of single neuron can exhibit various firing patterns. Synchronization in coupled neurons is also investigated as the coupling strength varying in the situation of two neurons and network. It is illustrated that the coupled neurons can exhibit different types of pattern when the coupling strength varies. These results may be instructive to understand information transmission in olfactory system.     

A biophysical model of vertebrate olfactory epithelium and bulb exhibiting gap junction dependent odor-evoked spatiotemporal patterns of activity

This work describes a biophysical model of the initial stages of vertebrate olfactory system containing structures representing the olfactory epithelium and bulb. Its main novelty is the introduction of gap junctions connecting neurons both in the epithelium and bulb, and of biologically detailed dendrodendritic synapses between granule and mitral cells in the bulb. The model was used to simulate the effect of an odor presentation on the neural activity pattern in the epithelium and bulb. During the time for which an odor is presented with a constant concentration, there are spatiotemporal patterns in the epithelium and bulb generated by the couplings due to the gap junctions and/or dendrodendritic synapses. A study varying the strength of the gap junction coupling shows that the spatiotemporal patterns, both in the epithelium and bulb, are dependent of the coupling strength. It is also shown that the olfactory bulb's spatiotemporal pattern depends on the existence of the dendrodendritic connections between mitral and granule cells. If these spatiotemporal patterns really exist in the early processing stages of the olfactory system they may be used for odor coding and the gap junctions and dendrodendritic synapses might have a role on it.     

Decoding olfaction in Drosophila

Recent experiments in Drosophila demonstrate striking stereotypy in the neural architecture of the olfactory system. Functional imaging experiments in mammals and honeybees suggest a mechanism of odor coding that translates discrete patterns of activity in olfactory glomeruli into an odor image. Future experiments in Drosophila may permit a direct test of this odor-coding hypothesis.     

Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons

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.     

Origin of basal activity in mammalian olfactory receptor neurons

Mammalian odorant receptors form a large, diverse group of G protein-coupled receptors that determine the sensitivity and response profile of olfactory receptor neurons. But little is known if odorant receptors control basal and also stimulus-induced cellular properties of olfactory receptor neurons other than ligand specificity. This study demonstrates that different odorant receptors have varying degrees of basal activity, which drives concomitant receptor current fluctuations and basal action potential firing. This basal activity can be suppressed by odorants functioning as inverse agonists. Furthermore, odorant-stimulated olfactory receptor neurons expressing different odorant receptors can have strikingly different response patterns in the later phases of prolonged stimulation. Thus, the influence of odorant receptor choice on response characteristics is much more complex than previously thought, which has important consequences on odor coding and odor information transfer to the brain.     

Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity

How information encoded in neuronal spike trains is used to guide sensory decisions is a fundamental question. In olfaction, a single sniff is sufficient for fine odor discrimination but the neural representations on which olfactory decisions are based are unclear. Here, we recorded neural ensemble activity in the anterior piriform cortex (aPC) of rats performing an odor mixture categorization task. We show that odors evoke transient bursts locked to sniff onset and that odor identity can be better decoded using burst spike counts than by spike latencies or temporal patterns. Surprisingly, aPC ensembles also exhibited near-zero noise correlations during odor stimulation. Consequently, fewer than 100 aPC neurons provided sufficient information to account for behavioral speed and accuracy, suggesting that behavioral performance limits arise downstream of aPC. These findings demonstrate profound transformations in the dynamics of odor representations from the olfactory bulb to cortex and reveal likely substrates for odor-guided decisions. VIDEO ABSTRACT:     

Receptive fields in the rat piriform cortex.

Current models of odor discrimination in mammals involve molecular feature detection by a large family of diverse olfactory receptors, refinement of molecular feature extraction through precise projections of olfactory receptor neurons to the olfactory bulb to form an odor-specific spatial map of molecular features across glomerular layer, and synthesis of these features into odor objects within the piriform cortex. This review describes our recent work on odor and spatial receptive fields within the anterior piriform cortex and compares these fields with receptive fields of their primary afferent, olfactory bulb mitral/tufted cells. The results suggest that receptive fields in the piriform cortex are ensemble in nature, highly dynamic, and may contribute to odor discrimination and odor memory.     

Cortical processing of odor objects

Natural odors, generally composed of many monomolecular components, are analyzed by peripheral receptors into component features and translated into spatiotemporal patterns of neural activity in the olfactory bulb. Here, we will discuss the role of the olfactory cortex in the recognition, separation and completion of those odor-evoked patterns, and how these processes contribute to odor perception. Recent findings regarding the neural architecture, physiology, and plasticity of the olfactory cortex, principally the piriform cortex, will be described in the context of how this paleocortical structure creates odor objects.     

Analysis of training-induced changes in ethyl acetate odor maps using a new computational tool to map the glomerular layer of the olfactory bulb

Odor quality is thought to be encoded by the activation of partially overlapping subsets of glomeruli in the olfactory bulb (odor maps). Mouse genetic studies have demonstrated that olfactory sensory neurons (OSNs) expressing a particular olfactory receptor target their axons to a few individual glomeruli in the bulb. While the specific targeting of OSN axons provides a molecular underpinning for the odor maps, much remains to be understood about the relationship between the functional and molecular maps. In this article, we ask the question whether intensive training of mice in a go/no-go operant conditioning odor discrimination task affects odor maps measured by determining c-fos up-regulation in periglomerular cells. Data analysis is performed using a newly developed suite of computational tools designed to systematically map functional and molecular features of glomeruli in the adult mouse olfactory bulb. This suite provides the necessary tools to process high-resolution digital images, map labeled glomeruli, visualize odor maps, and facilitate statistical analysis of patterns of identified glomeruli in the olfactory bulb. The software generates odor maps (density plots) based on glomerular activity, density, or area. We find that training up-regulates the number of glomeruli that become c-fos positive after stimulation with ethyl acetate.