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

Locking of correlated neural activity to ongoing oscillations

Population-wide oscillations are ubiquitously observed in mesoscopic signals of cortical activity. In these network states a global oscillatory cycle modulates the propensity of neurons to fire. Synchronous activation of neurons has been hypothesized to be a separate channel of signal processing information in the brain. A salient question is therefore if and how oscillations interact with spike synchrony and in how far these channels can be considered separate. Experiments indeed showed that correlated spiking co-modulates with the static firing rate and is also tightly locked to the phase of beta-oscillations. While the dependence of correlations on the mean rate is well understood in feed-forward networks, it remains unclear why and by which mechanisms correlations tightly lock to an oscillatory cycle. We here demonstrate that such correlated activation of pairs of neurons is qualitatively explained by periodically-driven random networks. We identify the mechanisms by which covariances depend on a driving periodic stimulus. Mean-field theory combined with linear response theory yields closed-form expressions for the cyclostationary mean activities and pairwise zero-time-lag covariances of binary recurrent random networks. Two distinct mechanisms cause time-dependent covariances: the modulation of the susceptibility of single neurons (via the external input and network feedback) and the time-varying variances of single unit activities. For some parameters, the effectively inhibitory recurrent feedback leads to resonant covariances even if mean activities show non-resonant behavior. Our analytical results open the question of time-modulated synchronous activity to a quantitative analysis.Comment: 57 pages, 12 figures, published versio

Subtractive, divisive and non-monotonic gain control in feedforward nets linearized by noise and delays

The control of input-to-output mappings, or gain control, is one of the main strategies used by neural networks for the processing and gating of information. Using a spiking neural network model, we studied the gain control induced by a form of inhibitory feedforward circuitry—also known as “open-loop feedback”—, which has been experimentally observed in a cerebellum-like structure in weakly electric fish. We found, both analytically and numerically, that this network displays three different regimes of gain control: subtractive, divisive, and non-monotonic. Subtractive gain control was obtained when noise is very low in the network. Also, it was possible to change from divisive to non-monotonic gain control by simply modulating the strength of the feedforward inhibition, which may be achieved via long-term synaptic plasticity. The particular case of divisive gain control has been previously observed in vivo in weakly electric fish. These gain control regimes were robust to the presence of temporal delays in the inhibitory feedforward pathway, which were found to linearize the input-to-output mappings (or f-I curves) via a novel variability-increasing mechanism. Our findings highlight the feedforward-induced gain control analyzed here as a highly versatile mechanism of information gating in the brain

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

Feedback optimizes neural coding and perception of natural stimuli

Growing evidence suggests that sensory neurons achieve optimal encoding by matching their tuning properties to the natural stimulus statistics. However, the underlying mechanisms remain unclear. Here we demonstrate that feedback pathways from higher brain areas mediate optimized encoding of naturalistic stimuli via temporal whitening in the weakly electric fish Apteronotus leptorhynchus. While one source of direct feedback uniformly enhances neural responses, a separate source of indirect feedback selectively attenuates responses to low frequencies, thus creating a high-pass neural tuning curve that opposes the decaying spectral power of natural stimuli. Additionally, we recorded from two populations of higher brain neurons responsible for the direct and indirect descending inputs. While one population displayed broadband tuning, the other displayed high-pass tuning and thus performed temporal whitening. Hence, our results demonstrate a novel function for descending input in optimizing neural responses to sensory input through temporal whitening that is likely to be conserved across systems and species

Spatial processing of conspecific signals in weakly electric fish: from sensory image to neural population coding

In this dissertation, I examine how an animal’s nervous system encodes spatially realistic conspecific signals in their environment and how the encoding mechanisms support behavioral sensitivity. I begin by modeling changes in the electrosensory signals exchanged by weakly electric fish in a social context. During this behavior, I estimate how the spatial structure of conspecific stimuli influences sensory responses at the electroreceptive periphery. I then quantify how space is represented in the hindbrain, specifically in the primary sensory area called the electrosensory lateral line lobe. I show that behavioral sensitivity is influenced by the heterogeneous properties of the pyramidal cell population. I further demonstrate that this heterogeneity serves to start segregating spatial and temporal information early in the sensory pathway. Lastly, I characterize the accuracy of spatial coding in this network and predict the role of network elements, such as correlated noise and feedback, in shaping the spatial information. My research provides a comprehensive understanding of spatial coding in the first stages of sensory processing in this system and allows us to better understand how network dynamics shape coding accuracy

Population Coding and Correlated Variability in Electrosensory Pathways

The fact that perception and behavior depend on the simultaneous and coordinated activity of neural populations is well established. Understanding encoding through neuronal population activity is however complicated by the statistical dependencies between the activities of neurons, which can be present in terms of both their mean (signal correlations) and their response variability (noise correlations). Here, we review the state of knowledge regarding population coding and the influence of correlated variability in the electrosensory pathways of the weakly electric fish Apteronotus leptorhynchus. We summarize known population coding strategies at the peripheral level, which are largely unaffected by noise correlations. We then move on to the hindbrain, where existing data from the electrosensory lateral line lobe (ELL) shows the presence of noise correlations. We summarize the current knowledge regarding the mechanistic origins of noise correlations and known mechanisms of stimulus dependent correlation shaping in ELL. We finish by considering future directions for understanding population coding in the electrosensory pathways of weakly electric fish, highlighting the benefits of this model system for understanding the origins and impact of noise correlations on population coding

Formation of Structure in Cortical Networks through Spike Timing-Dependent Plasticity

The connectivity of mammalian brains exhibits structure at a wide variety of spatial scales, from the broad (which brain areas connect to which) to the extremely fine (where synapses form on the morphology of individual neurons). Two striking features of the neuron-to- neuron connectivity are 1) the strong over-representation of multi-synapse connectivity pat- terns compared to simple random-network models and 2) a strong relationship between neurons’ local connectivity and their stimulus preferences, so that local network structure plays a large role in the computations neurons perform. A central question in systems neu- roscience is how such structures emerge. Answers to this question are confounded by the mutual interactions of neuronal activity and neural network structure. Patterns of synaptic connectivity influence neurons’ joint activity, while the synapses between neurons are plastic and strengthen or weaken depending on the activity of the pre- and postsynaptic neurons. In this thesis, I develop a self-consistent framework for the coevolution of network struc- ture and spiking activity. Subsequent chapters leverage this to develop low-dimensional sets of equations that directly describe the plasticity of connectivity patterns in large spiking networks. I examine plasticity during spontaneous activity and then how the structure of external stimuli can shape network structure and subsequent spontaneous plasticity. These studies provide a step towards understanding how the structure of neuronal networks and neurons’ joint activity interact to allow network computations