The effect of heterogeneity on decorrelation mechanisms in spiking neural networks: a neuromorphic-hardware study

High-level brain function such as memory, classification or reasoning can be realized by means of recurrent networks of simplified model neurons. Analog neuromorphic hardware constitutes a fast and energy efficient substrate for the implementation of such neural computing architectures in technical applications and neuroscientific research. The functional performance of neural networks is often critically dependent on the level of correlations in the neural activity. In finite networks, correlations are typically inevitable due to shared presynaptic input. Recent theoretical studies have shown that inhibitory feedback, abundant in biological neural networks, can actively suppress these shared-input correlations and thereby enable neurons to fire nearly independently. For networks of spiking neurons, the decorrelating effect of inhibitory feedback has so far been explicitly demonstrated only for homogeneous networks of neurons with linear sub-threshold dynamics. Theory, however, suggests that the effect is a general phenomenon, present in any system with sufficient inhibitory feedback, irrespective of the details of the network structure or the neuronal and synaptic properties. Here, we investigate the effect of network heterogeneity on correlations in sparse, random networks of inhibitory neurons with non-linear, conductance-based synapses. Emulations of these networks on the analog neuromorphic hardware system Spikey allow us to test the efficiency of decorrelation by inhibitory feedback in the presence of hardware-specific heterogeneities. The configurability of the hardware substrate enables us to modulate the extent of heterogeneity in a systematic manner. We selectively study the effects of shared input and recurrent connections on correlations in membrane potentials and spike trains. Our results confirm ...Comment: 20 pages, 10 figures, supplement

Neurons and circuits for odor processing in the piriform cortex

Increased understanding of the early stages of olfaction has lead to a renewed interest in the higher brain regions responsible for forming unified ‘odor images’ from the chemical components detected by the nose. The piriform cortex, which is one of the first cortical destinations of olfactory information in mammals, is a primitive paleocortex that is critical for the synthetic perception of odors. Here we review recent work that examines the cellular neurophysiology of the piriform cortex. Exciting new findings have revealed how the neurons and circuits of the piriform cortex process odor information, demonstrating that, despite its superficial simplicity, the piriform cortex is a remarkably subtle and intricate neural circuit

On-Center/Inhibitory-Surround Decorrelation via Intraglomerular Inhibition in the Olfactory Bulb Glomerular Layer

Classical lateral inhibition, which relies on spatially ordered neural representations of physical stimuli, cannot decorrelate sensory representations in which stimulus properties are represented non-topographically. Recent theoretical and experimental studies indicate that such a non-topographical representation of olfactory stimuli predominates in olfactory bulb, thereby refuting the classical view that olfactory decorrelation is mediated by lateral inhibition comparable to that in the retina. Questions persist, however, regarding how well non-topographical decorrelation models can replicate the inhibitory “surround” that has been observed experimentally (with respect to odor feature-similarity) in olfactory bulb principal neurons, analogous to the spatial inhibitory surround generated by lateral inhibition in retina. Using two contrasting scenarios of stimulus representation – one “retinotopically” organized and one in which receptive fields are unpredictably distributed as they are in olfactory bulb – we here show that intracolumnar inhibitory interactions between local interneurons and principal neurons successfully decorrelate similar sensory representations irrespective of the scenario of representation. In contrast, lateral inhibitory interactions between these same neurons in neighboring columns are only able to effectively decorrelate topographically organized representations. While anatomical substrates superficially consistent with both types of inhibition exist in olfactory bulb, of the two only local intraglomerular inhibition suffices to mediate olfactory decorrelation

Synchronous chaos and broad band gamma rhythm in a minimal multi-layer model of primary visual cortex

Visually induced neuronal activity in V1 displays a marked gamma-band component which is modulated by stimulus properties. It has been argued that synchronized oscillations contribute to these gamma-band activity [... however,] even when oscillations are observed, they undergo temporal decorrelation over very few cycles. This is not easily accounted for in previous network modeling of gamma oscillations. We argue here that interactions between cortical layers can be responsible for this fast decorrelation. We study a model of a V1 hypercolumn, embedding a simplified description of the multi-layered structure of the cortex. When the stimulus contrast is low, the induced activity is only weakly synchronous and the network resonates transiently without developing collective oscillations. When the contrast is high, on the other hand, the induced activity undergoes synchronous oscillations with an irregular spatiotemporal structure expressing a synchronous chaotic state. As a consequence the population activity undergoes fast temporal decorrelation, with concomitant rapid damping of the oscillations in LFPs autocorrelograms and peak broadening in LFPs power spectra. [...] Finally, we argue that the mechanism underlying the emergence of synchronous chaos in our model is in fact very general. It stems from the fact that gamma oscillations induced by local delayed inhibition tend to develop chaos when coupled by sufficiently strong excitation.Comment: 49 pages, 11 figures, 7 table

Pharmacological analysis of ionotropic glutamate and GABA recptor function in neuronal circuits of the zebrafish olfactory bulb

In the olfactory bulb and other brain areas, basic cellular and synaptic properties of individual neurons have been studied extensively in reduced preparations. Nevertheless, it is still poorly understood how intactions between multiple neurons shape spatio-temporal activity patterns and give rise to the computational properties of the the intact circuit. In this thesis, I used pharmacological manipulations of excitatory and inhibitory neurotransmitter receptors to examine the synaptic interactions underlying spontaneous and odor-evoked activity patterns in the intact olfactory bulb of zebrafish. Electrophysiological and one- and two-photon calcium imaging methods were used to record activity from the principal neurons of the OB (mitral cells, MCs), their sensory input, and local interneurons. The combined blockade of AMPA/kainate and NMDA receptors abolished odor-evoked excitation of MCs, indicating that sensory input to the OB is mediated by ionotropic glutamate receptors. Surprisingly, however, the blockade of AMPA/Kainiate receptors alone increased the mean response of MCs and decreased the mean response of interneurons (INs), and the blockade of NMDA receptors caused little or no change in the mean responses of MCs and INs. In addition, antagonists of both glutamate receptor types had diverse effects on the magnitude and time course of individual MC and IN responses and, thus, changed spatio-temporal activity patterns across neuronal populations. The blockade of GABA(A) receptors increased spontaneous and odor evoked firing rates of mitral cells and often induced rhythmic bursting. Moreover, the blockade of, GABA(A) or AMPA/kainate receptors abolished fast oscillatory activity in the local field potential. Blockade of GABA(B) receptors reduced calcium influx in afferent sensory axons and modulated response time courses of mitral cells. These results indicate that (1) IN activity during an odor response depends mainly on AMPA/Kainiate receptor input, (2) interactions between MCs and INs regulate the total OB output activity, (3) AMPA/Kainiate receptors and GABA(A) receptors underly the synchronization of odor-dependent neuronal ensembles and (4) odor-specific patterns of OB output activity are shaped by circuits containing iGlu receptors and GABA receptors. These results provide insights into the mechanisms underlying the processing of odor-encoding activity patterns in the OB.Im olfaktorischen Bulbus (OB) und anderen Hirnarealen wurden grundlegende zelluläre und synaptische Eigenschaften der Einzelneurone ausführlich in reduzierten Präparaten studiert. Trotzdem ist kaum bekannt, wie die Interaktionen mehrerer Nervenzellen untereinander räumlich-zeitlich strukturierte Aktivitätsmuster formen und dadurch die rechnerischen Eigenschaften der intakten Schaltkreise entstehen. In dieser Arbeit nutzte ich pharmakologische Manipulationen der erregenden und hemmenden Neurotransmitter-Rezeptoren, um die synaptischen Interaktionen zu untersuchen, die spontanen und geruchsinduzierten Aktivitätsmustern im intakten OB des Zebrafisch zugrunde liegen. Methoden der Elektrophysiology sowie der konventionellen und Zwei-Photonen-Mikroskopie wurden genutzt, um Aktivität von Ausgangsneuronen des OB (Mitralzellen, MCs), ihrem sensorischen Eingang, und Interneuronen (INs) zu messen. Die gleichzeitige Blockierung von AMPA/Kainate- und NMDA-Rezeptoren verhinderte die geruchsinduzierte Erregung von MCs, was darauf hinweist, dass der sensorische Eingang des OB durch ionotrope Glutamatrezeptoren vermittelt wird. Die Blockierung von AMPA/Kainate Rezeptoren allein jedoch erhöhte überraschender Weise im Mittel die Antwort von MCs und reduzierte im Mittel die Antwort von INs. Die Blockierung von NMDA Rezeptoren allein lösten im Mittel geringe oder keine Veränderung der Antworten von MCs and INs aus. Außerdem hatten die Antagonisten für beide Glutamatrezeptoren unterschiedliche Einflüsse auf Größe und Zeitverlauf individueller MC- und IN- Antworten und veränderten daher das räumlich-zeitliche Aktivitätsmuster innerhalb der Nervenzellpopulation. Die Blockierung von GABA(A)-Rezeptoren erhöhte spontane und geruchsinduzierte Feuerraten in MCs und induzierten oft rhythmische, stoßweise Aktivität. Die Blockierung von GABA(A)- und AMPA/Kainate-Rezeptoren hob überdies geruchsinduzierte Oszillationen im Feldpotenzial auf. Die Blockierung von GABA(B)-Rezeptoren verringerte den Kalziumeinstrom in die Endigungen afferenter sensorischer Axone und modulierte den Zeitverlauf von MC-Antworten. Die Ergebnisse zeigen, dass (1) die Aktivität der Interneurone während der Geruchsantwort hauptsächlich von AMPA/Kainate-Rezeptoren abhängt, (2) die Interaktionen zwischen Mitralzellen und Interneuronen die Gesamtaktivität des Ausgangssingnales des olfaktorischen Bulbus regulieren, (3) AMPA/Kainate-Rezeptoren und GABA(A)-Rezeptoren der Synchronisation geruchsabhängiger Gruppen von Nervenzellen zugrunde liegen und (4) geruchsspezifische Muster im Ausgangssignal des olfaktorischen Bulbus durch Schaltkreise geformt werden, die iGlu Rezeptoren und GABA Rezeptoren enthalten. Diese Ergebnisse ermöglichen Einblick in die Mechanismen die der Verarbeitung geruchskodierender Aktivitätsmuster im olfaktorischen Bulbus unterliegen

The correlation structure of local cortical networks intrinsically results from recurrent dynamics

The co-occurrence of action potentials of pairs of neurons within short time intervals is known since long. Such synchronous events can appear time-locked to the behavior of an animal and also theoretical considerations argue for a functional role of synchrony. Early theoretical work tried to explain correlated activity by neurons transmitting common fluctuations due to shared inputs. This, however, overestimates correlations. Recently the recurrent connectivity of cortical networks was shown responsible for the observed low baseline correlations. Two different explanations were given: One argues that excitatory and inhibitory population activities closely follow the external inputs to the network, so that their effects on a pair of cells mutually cancel. Another explanation relies on negative recurrent feedback to suppress fluctuations in the population activity, equivalent to small correlations. In a biological neuronal network one expects both, external inputs and recurrence, to affect correlated activity. The present work extends the theoretical framework of correlations to include both contributions and explains their qualitative differences. Moreover the study shows that the arguments of fast tracking and recurrent feedback are not equivalent, only the latter correctly predicts the cell-type specific correlations