Decorrelation of neural-network activity by inhibitory feedback

Correlations in spike-train ensembles can seriously impair the encoding of information by their spatio-temporal structure. An inevitable source of correlation in finite neural networks is common presynaptic input to pairs of neurons. Recent theoretical and experimental studies demonstrate that spike correlations in recurrent neural networks are considerably smaller than expected based on the amount of shared presynaptic input. By means of a linear network model and simulations of networks of leaky integrate-and-fire neurons, we show that shared-input correlations are efficiently suppressed by inhibitory feedback. To elucidate the effect of feedback, we compare the responses of the intact recurrent network and systems where the statistics of the feedback channel is perturbed. The suppression of spike-train correlations and population-rate fluctuations by inhibitory feedback can be observed both in purely inhibitory and in excitatory-inhibitory networks. The effect is fully understood by a linear theory and becomes already apparent at the macroscopic level of the population averaged activity. At the microscopic level, shared-input correlations are suppressed by spike-train correlations: In purely inhibitory networks, they are canceled by negative spike-train correlations. In excitatory-inhibitory networks, spike-train correlations are typically positive. Here, the suppression of input correlations is not a result of the mere existence of correlations between excitatory (E) and inhibitory (I) neurons, but a consequence of a particular structure of correlations among the three possible pairings (EE, EI, II)

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

Tilt Aftereffects in a Self-Organizing Model of the Primary Visual Cortex

RF-LISSOM, a self-organizing model of laterally connected orientation maps in the primary visual cortex, was used to study the psychological phenomenon known as the tilt aftereffect. The same self-organizing processes that are responsible for the long-term development of the map are shown to result in tilt aftereffects over short time scales in the adult. The model permits simultaneous observation of large numbers of neurons and connections, making it possible to relate high-level phenomena to low-level events, which is difficult to do experimentally. The results give detailed computational support for the long-standing conjecture that the direct tilt aftereffect arises from adaptive lateral interactions between feature detectors. They also make a new prediction that the indirect effect results from the normalization of synaptic efficacies during this process. The model thus provides a unified computational explanation of self-organization and both the direct and indirect tilt aftereffect in the primary visual cortex

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

Decorrelation of Odor Representations via Spike Timing-Dependent Plasticity

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 timing-dependent 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

Functional consequences of inhibitory plasticity: homeostasis, the excitation-inhibition balance and beyond

Computational neuroscience has a long-standing tradition of investigating the consequences of excitatory synaptic plasticity. In contrast, the functions of inhibitory plasticity are still largely nebulous, particularly given the bewildering diversity of interneurons in the brain. Here, we review recent computational advances that provide first suggestions for the functional roles of inhibitory plasticity, such as a maintenance of the excitation-inhibition balance, a stabilization of recurrent network dynamics and a decorrelation of sensory responses. The field is still in its infancy, but given the existing body of theory for excitatory plasticity, it is likely to mature quickly and deliver important insights into the self-organization of inhibitory circuits in the brain

The Spatial Structure of Stimuli Shapes the Timescale of Correlations in Population Spiking Activity

Throughout the central nervous system, the timescale over which pairs of neural spike trains are correlated is shaped by stimulus structure and behavioral context. Such shaping is thought to underlie important changes in the neural code, but the neural circuitry responsible is largely unknown. In this study, we investigate a stimulus-induced shaping of pairwise spike train correlations in the electrosensory system of weakly electric fish. Simultaneous single unit recordings of principal electrosensory cells show that an increase in the spatial extent of stimuli increases correlations at short (~10 ms) timescales while simultaneously reducing correlations at long (~100 ms) timescales. A spiking network model of the first two stages of electrosensory processing replicates this correlation shaping, under the assumptions that spatially broad stimuli both saturate feedforward afferent input and recruit an open-loop inhibitory feedback pathway. Our model predictions are experimentally verified using both the natural heterogeneity of the electrosensory system and pharmacological blockade of descending feedback projections. For weak stimuli, linear response analysis of the spiking network shows that the reduction of long timescale correlation for spatially broad stimuli is similar to correlation cancellation mechanisms previously suggested to be operative in mammalian cortex. The mechanism for correlation shaping supports population-level filtering of irrelevant distractor stimuli, thereby enhancing the population response to relevant prey and conspecific communication inputs. © 2012 Litwin-Kumar et al

Intrinsic adaptation in autonomous recurrent neural networks

A massively recurrent neural network responds on one side to input stimuli and is autonomously active, on the other side, in the absence of sensory inputs. Stimuli and information processing depends crucially on the qualia of the autonomous-state dynamics of the ongoing neural activity. This default neural activity may be dynamically structured in time and space, showing regular, synchronized, bursting or chaotic activity patterns. We study the influence of non-synaptic plasticity on the default dynamical state of recurrent neural networks. The non-synaptic adaption considered acts on intrinsic neural parameters, such as the threshold and the gain, and is driven by the optimization of the information entropy. We observe, in the presence of the intrinsic adaptation processes, three distinct and globally attracting dynamical regimes, a regular synchronized, an overall chaotic and an intermittent bursting regime. The intermittent bursting regime is characterized by intervals of regular flows, which are quite insensitive to external stimuli, interseeded by chaotic bursts which respond sensitively to input signals. We discuss these finding in the context of self-organized information processing and critical brain dynamics.Comment: 24 pages, 8 figure

Sparse synaptic connectivity is required for decorrelation and pattern separation in feedforward networks

Pattern separation is a fundamental function of the brain. The divergent feedforward networks thought to underlie this computation are widespread, yet exhibit remarkably similar sparse synaptic connectivity. Marr-Albus theory postulates that such networks separate overlapping activity patterns by mapping them onto larger numbers of sparsely active neurons. But spatial correlations in synaptic input and those introduced by network connectivity are likely to compromise performance. To investigate the structural and functional determinants of pattern separation we built models of the cerebellar input layer with spatially correlated input patterns, and systematically varied their synaptic connectivity. Performance was quantified by the learning speed of a classifier trained on either the input or output patterns. Our results show that sparse synaptic connectivity is essential for separating spatially correlated input patterns over a wide range of network activity, and that expansion and correlations, rather than sparse activity, are the major determinants of pattern separation