Fluctuations In Population Activity Research Articles

Biased Orientation and Color Tuning of the Human Visual Gamma Rhythm.

Narrowband γ oscillations (NBG: ∼20-60 Hz) in visual cortex reflect rhythmic fluctuations in population activity generated by underlying circuits tuned for stimulus location, orientation, and color. A variety of theories posit a specific role for NBG in encoding and communicating this information within visual cortex. However, recent findings suggest a more nuanced role for NBG, given its dependence on certain stimulus feature configurations, such as coherent-oriented edges and specific hues. Motivated by these factors, we sought to quantify the independent and joint tuning properties of NBG to oriented and color stimuli using intracranial recordings from the human visual cortex (male and female). NBG was shown to display a cardinal orientation bias (horizontal) and also an end- and mid-spectral color bias (red/blue and green). When jointly probed, the cardinal bias for orientation was attenuated and an end-spectral preference for red and blue predominated. This loss of mid-spectral tuning occurred even for recording sites showing large responses to uniform green stimuli. Our results demonstrate the close, yet complex, link between the population dynamics driving NBG oscillations and known feature selectivity biases for orientation and color within visual cortex. Such a bias in stimulus tuning imposes new constraints on the functional significance of the visual γ rhythm. More generally, these biases in population electrophysiology will need to be considered in experiments using orientation or color features to examine the role of visual cortex in other domains, such as working memory and decision-making.SIGNIFICANCE STATEMENT Oscillations in electrophysiological activity occur in visual cortex in response to stimuli that strongly drive the orientation or color selectivity of visual neurons. The significance of this induced "γ rhythm" to brain function remains unclear. Answering this question requires understanding how and why some stimuli can reliably generate oscillatory γ activity while others do not. We examined how different orientations and colors independently and jointly modulate γ oscillations in the human brain. Our data show that γ oscillations are greatest for certain orientations and colors that reflect known response biases in visual cortex. Such findings complicate the functional significance of γ oscillations but open new avenues for linking circuits to population dynamics in visual cortex.

Cortical State Fluctuations during Sensory Decision Making

SummaryIn many behavioral tasks, cortex enters a desynchronized state where low-frequency fluctuations in population activity are suppressed. The precise behavioral correlates of desynchronization and its global organization are unclear. One hypothesis holds that desynchronization enhances stimulus coding in the relevant sensory cortex. Another hypothesis holds that desynchronization reflects global arousal, such as task engagement. Here, we trained mice on tasks where task engagement could be distinguished from sensory accuracy. Using widefield calcium imaging, we found that performance-related desynchronization was global and correlated better with engagement than with accuracy. Consistent with this link between desynchronization and engagement, rewards had a long-lasting desynchronizing effect. To determine whether engagement-related state changes depended on the relevant sensory modality, we trained mice on visual and auditory tasks and found that in both cases desynchronization was global, including regions such as somatomotor cortex. We conclude that variations in low-frequency fluctuations are predominately global and related to task engagement.

Frequency-separated principal component analysis of cortical population activity.

A hallmark of neocortical activity is the presence of low-dimensional fluctuations in firing rate that are coordinated across neurons. However, the impact of these fluctuations on sensory processing remains unclear. Here, we examined fluctuations in populations of orientation-selective neurons from anesthetized macaque primary visual cortex (V1) during stimulus viewing as well as spontaneous activity. We introduce a novel approach termed frequency-separated principal component analysis (FS-PCA) to characterize these fluctuations. This method unveiled a distribution of components with a broad range of frequencies whose eigenvalues and variance followed an approximate power law. During stimulus viewing, subpopulations of V1 neurons correlated either positively or negatively with low-dimensional fluctuations. These two subpopulations displayed distinct activation properties and noise correlations in response to sensory input. Together, results suggest that slow, low-dimensional fluctuations in V1 population activity shape the response of individual neurons to oriented stimuli and may impact the transmission of sensory information to downstream regions of the primary visual system.NEW & NOTEWORTHY A method termed frequency-separated principal component analysis (FS-PCA) is introduced for analyzing populations of simultaneously recorded neurons. This framework extends standard principal component analysis by extracting components of activity delimited to specific frequency bands. FS-PCA revealed that circuits of the primary visual cortex generate a broad range of components dominated by low-frequency activity. Furthermore, low-dimensional fluctuations in population activity modulated the response of individual neurons to sensory input.

Dynamic states of population activity in prefrontal cortical networks of freely-moving macaque

Neural responses in the cerebral cortex change dramatically between the ‘synchronized’ state during sleep and ‘desynchronized’ state during wakefulness. Our understanding of cortical state emerges largely from experiments performed in sensory areas of head-fixed or tethered rodents due to technical limitations of recording from larger freely-moving animals for several hours. Here, we report a system integrating wireless electrophysiology, wireless eye tracking, and real-time video analysis to examine the dynamics of population activity in a high-level, executive area – dorsolateral prefrontal cortex (dlPFC) of unrestrained monkey. This technology allows us to identify cortical substates during quiet and active wakefulness, and transitions in population activity during rest. We further show that narrow-spiking neurons exhibit stronger synchronized fluctuations in population activity than broad-spiking neurons regardless of state. Our results show that cortical state is controlled by behavioral demands and arousal by asymmetrically modulating the slow response fluctuations of local excitatory and inhibitory cell populations.

Unstructured network topology begets order-based representation by privileged neurons

How spiking activity reverberates through neuronal networks, how evoked and spontaneous activity interacts and blends, and how the combined activities represent external stimulation are pivotal questions in neuroscience. We simulated minimal models of unstructured spiking networks in silico, asking whether and how gentle external stimulation might be subsequently reflected in spontaneous activity fluctuations. Consistent with earlier findings in silico and in vitro, we observe a privileged subpopulation of ‘pioneer neurons’ that, by their firing order, reliably encode previous external stimulation. We also confirm that pioneer neurons are ‘sensitive’ in that they are recruited by small fluctuations of population activity. We show that order-based representations rely on a ‘chain’ of pioneer neurons with different degrees of sensitivity and thus constitute an emergent property of collective dynamics. The forming of such representations is greatly favoured by a broadly heterogeneous connection topology—a broad ‘middle class’ in degree of connectedness. In conclusion, we offer a minimal model for the representational role of pioneer neurons, as observed experimentally in vitro. In addition, we show that broadly heterogeneous connectivity enhances the representational capacity of unstructured networks.

A Markov model for the temporal dynamics of balanced random networks of finite size.

The balanced state of recurrent networks of excitatory and inhibitory spiking neurons is characterized by fluctuations of population activity about an attractive fixed point. Numerical simulations show that these dynamics are essentially nonlinear, and the intrinsic noise (self-generated fluctuations) in networks of finite size is state-dependent. Therefore, stochastic differential equations with additive noise of fixed amplitude cannot provide an adequate description of the stochastic dynamics. The noise model should, rather, result from a self-consistent description of the network dynamics. Here, we consider a two-state Markovian neuron model, where spikes correspond to transitions from the active state to the refractory state. Excitatory and inhibitory input to this neuron affects the transition rates between the two states. The corresponding nonlinear dependencies can be identified directly from numerical simulations of networks of leaky integrate-and-fire neurons, discretized at a time resolution in the sub-millisecond range. Deterministic mean-field equations, and a noise component that depends on the dynamic state of the network, are obtained from this model. The resulting stochastic model reflects the behavior observed in numerical simulations quite well, irrespective of the size of the network. In particular, a strong temporal correlation between the two populations, a hallmark of the balanced state in random recurrent networks, are well represented by our model. Numerical simulations of such networks show that a log-normal distribution of short-term spike counts is a property of balanced random networks with fixed in-degree that has not been considered before, and our model shares this statistical property. Furthermore, the reconstruction of the flow from simulated time series suggests that the mean-field dynamics of finite-size networks are essentially of Wilson-Cowan type. We expect that this novel nonlinear stochastic model of the interaction between neuronal populations also opens new doors to analyze the joint dynamics of multiple interacting networks.

Effect of network structure on spike train correlations in networks of integrate-and-fire neurons

Balanced networks of excitatory and inhibitory neurons are a popular paradigm to describe the ground state of cortical activity. Although such networks can assume a state of asynchronous and irregular activity with low firing rates and low pairwise correlations, recurrent connectivity inevitably induces correlations between spike trains [1]. To elucidate the influence of network topology on correlations, we have recently employed the framework of linearly interacting point processes [2] as an analytically tractable model for network dynamics [3]. A power series of the connectivity matrix can be used to disentangle the different contributions to pairwise correlations from direct and indirect interactions between neurons. In the present study we show that this framework can be applied to approximate dynamics of networks of integrate-and-fire neurons, if the reset after each spike is formally described as self-inhibition. The reset then effectively decreases overall correlations. We study ring networks, where we are able to derive analytical expressions for the distance dependence of correlations and fluctuations in population activity. Rates and correlations in simulated networks are predicted accurately, provided that spike train correlations are reasonably small and the linear impulse response of single neurons is known.

Cellular and network mechanisms of cholinergically-induced transition between gamma and sharp wave – ripple network states in the hippocampus

In different behavioral states cortical networks show distinct dynamics, which may implement distinct computations. Switching between network states may be brought about by subcortical modulatory inputs, which affect both single cell and synaptic properties, but the actual mechanisms are currently unknown. Hippocampal activity in awake rodents is characterized by the behavior-associated alteration of theta-modulated gamma activity, associated with exploration, and sharp wave – ripple (SPW-R) activity, associated with alert stillness. We take advantage of the recent development of an in vitro slice preparation where these activity patterns either emerge spontaneously or can be induced by the application of neuromodulatory substances, to investigate, via the combination of electrophysiological and modeling tools, the link between changes in neuronal characteristics and the resulting switches in emergent network behavior. By improving the preparation and maintenance conditions of in vitro slices, we managed to record activity patterns identical to in vivo described SPW-Rs and gamma activity from the CA3 area. Under baseline conditions the slices spontaneously generated SPW-Rs with characteristics similar to those observed in vivo. Mimicking the increased cholinergic tone during the theta-gamma state in vivo by the application of the cholinergic agonist carbachol (3-5uM, CCH), the SPW-R activity can be quickly (1-2 minutes) and reversibly converted into gamma activity. In the SPW-R state, activity levels were generally low, but activity in the network could transiently build up to an intensely activated, highly synchronous state. In the gamma state, activity levels were sustained at a high level, and synchrony increased rhythmically in each cycle, but never reached levels seen during SPW-Rs. In order to explain these qualitative changes in network behavior, we hypothesize that two network parameters change concurrently during the SPW-R to gamma transition, caused by the increasing cholinergic tone: 1) a cellular parameter: the excitability of principal neurons increases (this is responsible for the increased frequency of network activation), while 2) a network parameter: the strength of synaptic connections decreases (this limits the spread of activity in the network before inhibition terminates it). We measured the effects of CCH on the excitability of single pyramidal cells and perisomatic interneurons, and determined how CCH changes the efficacy of transmission between these cell types in CA3. We confirmed that CCH increased cellular excitability (mainly in pyramidal cells), and found that CCH substantially decreased the efficacy of synaptic transmission in all connections examined, but it especially strongly attenuated excitatory synaptic transmission. Finally, we developed a large-scale model of the CA3 area of a hippocampal slice, consisting of integrate-and-fire models of pyramidal cells and interneurons. Single cell and synaptic properties were determined experimentally in both network states. Our model confirmed that the measured cellular and synaptic changes are sufficient to explain the observed switching between the two types of network dynamics, and also suggested possible mechanisms for the initiation and termination of sharp wave events. it suggested that the initiation of sharp waves relies on random fluctuations of population activity, while the termination of sharp waves probably requires some novel form of slow negative feedback.