Sequential Sparsening by Successive Adaptation in Neural Populations

In the principal cells of the insect mushroom body, the Kenyon cells (KC), olfactory information is represented by a spatially and temporally sparse code. Each odor stimulus will activate only a small portion of neurons and each stimulus leads to only a short phasic response following stimulus onset irrespective of the actual duration of a constant stimulus. The mechanisms responsible for the sparse code in the KCs are yet unresolved. Here, we explore the role of the neuron-intrinsic mechanism of spike-frequency adaptation (SFA) in producing temporally sparse responses to sensory stimulation in higher processing stages. Our single neuron model is defined through a conductance-based integrate-and-fire neuron with spike-frequency adaptation [1]. We study a fully connected feed-forward network architecture in coarse analogy to the insect olfactory pathway. A first layer of ten neurons represents the projection neurons (PNs) of the antenna lobe. All PNs receive a step-like input from the olfactory receptor neurons, which was realized by independent Poisson processes. The second layer represents 100 KCs which converge onto ten neurons in the output layer which represents the population of mushroom body extrinsic neurons (ENs). Our simulation result matches with the experimental observations. In particular, intracellular recordings of PNs show a clear phasic-tonic response that outlasts the stimulus [2] while extracellular recordings from KCs in the locust express sharp transient responses [3]. We conclude that the neuron-intrinsic mechanism is can explain a progressive temporal response sparsening in the insect olfactory system. Further experimental work is needed to test this hypothesis empirically. [1] Muller et. al., Neural Comput, 19(11):2958-3010, 2007. [2] Assisi et. al., Nat Neurosci, 10(9):1176-1184, 2007. [3] Krofczik et. al. Front. Comput. Neurosci., 2(9), 2009.Comment: 5 pages, 2 figures, This manuscript was submitted for review to the Eighteenth Annual Computational Neuroscience Meeting CNS*2009 in Berlin and accepted for oral presentation at the meetin

Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation

Insects have a remarkable ability to identify and track odour sources in multi-odour backgrounds. Recent behavioural experiments show that this ability relies on detecting millisecond stimulus asynchronies between odourants that originate from different sources. Honeybees, Apis mellifera , are able to distinguish mixtures where both odourants arrive at the same time (synchronous mixtures) from those where odourant onsets are staggered (asynchronous mixtures) down to an onset delay of only 6 ms. In this paper we explore this surprising ability in a model of the insects' primary olfactory brain area, the antennal lobe. We hypothesize that a winner-take-all inhibitory network of local neurons in the antennal lobe has a symmetry-breaking effect, such that the response pattern in projection neurons to an asynchronous mixture is different from the response pattern to the corresponding synchronous mixture for an extended period of time beyond the initial odourant onset where the two mixture conditions actually differ. The prolonged difference between response patterns to synchronous and asynchronous mixtures could facilitate odour segregation in downstream circuits of the olfactory pathway. We present a detailed data-driven model of the bee antennal lobe that reproduces a large data set of experimentally observed physiological odour responses, successfully implements the hypothesised symmetry-breaking mechanism and so demonstrates that this mechanism is consistent with our current knowledge of the olfactory circuits in the bee brain

Input-modulation as an alternative to conventional learning strategies

Animals use various strategies for learning stimulus-reward associations. Computational methods that mimic animal behaviour most commonly interpret learning as a high level phenomenon, in which the pairing of stimulus and reward leads to plastic changes in the final output layers where action selection takes place. Here, we present an alternative input-modulation strategy for forming simple stimulus-response associations based on reward. Our model is motivated by experimental evidence on modulation of early brain regions by reward signalling in the honeybee. The model can successfully discriminate dissimilar odours and generalise across similar odours, like bees do. In the most simplified connectionist description, the new input- modulation learning is shown to be asymptotically equivalent to the standard perceptron

Mechanisms explaining transitions between tonic and phasic firing in neuronal populations as predicted by a low dimensional firing rate model

Several firing patterns experimentally observed in neural populations have been successfully correlated to animal behavior. Population bursting, hereby regarded as a period of high firing rate followed by a period of quiescence, is typically observed in groups of neurons during behavior. Biophysical membrane-potential models of single cell bursting involve at least three equations. Extending such models to study the collective behavior of neural populations involves thousands of equations and can be very expensive computationally. For this reason, low dimensional population models that capture biophysical aspects of networks are needed. \noindent The present paper uses a firing-rate model to study mechanisms that trigger and stop transitions between tonic and phasic population firing. These mechanisms are captured through a two-dimensional system, which can potentially be extended to include interactions between different areas of the nervous system with a small number of equations. The typical behavior of midbrain dopaminergic neurons in the rodent is used as an example to illustrate and interpret our results. \noindent The model presented here can be used as a building block to study interactions between networks of neurons. This theoretical approach may help contextualize and understand the factors involved in regulating burst firing in populations and how it may modulate distinct aspects of behavior.Comment: 25 pages (including references and appendices); 12 figures uploaded as separate file

Gain control network conditions in early sensory coding

Gain control is essential for the proper function of any sensory system. However, the precise mechanisms for achieving effective gain control in the brain are unknown. Based on our understanding of the existence and strength of connections in the insect olfactory system, we analyze the conditions that lead to controlled gain in a randomly connected network of excitatory and inhibitory neurons. We consider two scenarios for the variation of input into the system. In the first case, the intensity of the sensory input controls the input currents to a fixed proportion of neurons of the excitatory and inhibitory populations. In the second case, increasing intensity of the sensory stimulus will both, recruit an increasing number of neurons that receive input and change the input current that they receive. Using a mean field approximation for the network activity we derive relationships between the parameters of the network that ensure that the overall level of activity of the excitatory population remains unchanged for increasing intensity of the external stimulation. We find that, first, the main parameters that regulate network gain are the probabilities of connections from the inhibitory population to the excitatory population and of the connections within the inhibitory population. Second, we show that strict gain control is not achievable in a random network in the second case, when the input recruits an increasing number of neurons. Finally, we confirm that the gain control conditions derived from the mean field approximation are valid in simulations of firing rate models and Hodgkin-Huxley conductance based models

No Need for a Cognitive Map: Decentralized Memory for Insect Navigation

In many animals the ability to navigate over long distances is an important prerequisite for foraging. For example, it is widely accepted that desert ants and honey bees, but also mammals, use path integration for finding the way back to their home site. It is however a matter of a long standing debate whether animals in addition are able to acquire and use so called cognitive maps. Such a ‘map’, a global spatial representation of the foraging area, is generally assumed to allow the animal to find shortcuts between two sites although the direct connection has never been travelled before. Using the artificial neural network approach, here we develop an artificial memory system which is based on path integration and various landmark guidance mechanisms (a bank of individual and independent landmark-defined memory elements). Activation of the individual memory elements depends on a separate motivation network and an, in part, asymmetrical lateral inhibition network. The information concerning the absolute position of the agent is present, but resides in a separate memory that can only be used by the path integration subsystem to control the behaviour, but cannot be used for computational purposes with other memory elements of the system. Thus, in this simulation there is no neural basis of a cognitive map. Nevertheless, an agent controlled by this network is able to accomplish various navigational tasks known from ants and bees and often discussed as being dependent on a cognitive map. For example, map-like behaviour as observed in honey bees arises as an emergent property from a decentralized system. This behaviour thus can be explained without referring to the assumption that a cognitive map, a coherent representation of foraging space, must exist. We hypothesize that the proposed network essentially resides in the mushroom bodies of the insect brain

Elemental and configural olfactory coding by antennal lobe neurons of the honeybee (Apis mellifera)

When smelling an odorant mixture, olfactory systems can be analytical (i.e. extract information about the mixture elements) or synthetic (i.e. creating a configural percept of the mixture). Here, we studied elemental and configural mixture coding in olfactory neurons of the honeybee antennal lobe, local neurons in particular. We conducted intracellular recordings and stimulated with monomolecular odorants and their coherent or incoherent binary mixtures to reproduce a temporally dynamic environment. We found that about half of the neurons responded as ‘elemental neurons’, i.e. responses evoked by mixtures reflected the underlying feature information from one of the components. The other half responded as ‘configural neurons’, i.e. responses to mixtures were clearly different from responses to their single components. Elemental neurons divided in late responders (above 60 ms) and early responder neurons (below 60 ms), whereas responses of configural coding neurons concentrated in-between these divisions. Latencies of neurons with configural responses express a tendency to be faster for coherent stimuli which implies employment in different processing circuits

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