Estimating the contribution of assembly activity to cortical dynamics from spike and population measures

The hypothesis that cortical networks employ the coordinated activity of groups of neurons, termed assemblies, to process information is debated. Results from multiple single-unit recordings are not conclusive because of the dramatic undersampling of the system. However, the local field potential (LFP) is a mesoscopic signal reflecting synchronized network activity. This raises the question whether the LFP can be employed to overcome the problem of undersampling. In a recent study in the motor cortex of the awake behaving monkey based on the locking of coincidences to the LFP we determined a lower bound for the fraction of spike coincidences originating from assembly activation. This quantity together with the locking of single spikes leads to a lower bound for the fraction of spikes originating from any assembly activity. Here we derive a statistical method to estimate the fraction of spike synchrony caused by assemblies—not its lower bound—from the spike data alone. A joint spike and LFP surrogate data model demonstrates consistency of results and the sensitivity of the method. Combining spike and LFP signals, we obtain an estimate of the fraction of spikes resulting from assemblies in the experimental data

The Local Field Potential Reflects Surplus Spike Synchrony

The oscillatory nature of the cortical local field potential (LFP) is commonly interpreted as a reflection of synchronized network activity, but its relationship to observed transient coincident firing of neurons on the millisecond time-scale remains unclear. Here we present experimental evidence to reconcile the notions of synchrony at the level of neuronal spiking and at the mesoscopic scale. We demonstrate that only in time intervals of excess spike synchrony, coincident spikes are better entrained to the LFP than predicted by the locking of the individual spikes. This effect is enhanced in periods of large LFP amplitudes. A quantitative model explains the LFP dynamics by the orchestrated spiking activity in neuronal groups that contribute the observed surplus synchrony. From the correlation analysis, we infer that neurons participate in different constellations but contribute only a fraction of their spikes to temporally precise spike configurations, suggesting a dual coding scheme of rate and synchrony. This finding provides direct evidence for the hypothesized relation that precise spike synchrony constitutes a major temporally and spatially organized component of the LFP. Revealing that transient spike synchronization correlates not only with behavior, but with a mesoscopic brain signal corroborates its relevance in cortical processing.Comment: 45 pages, 8 figures, 3 supplemental figure

Coordinated neuronal ensembles in primary auditory cortical columns.

The synchronous activity of groups of neurons is increasingly thought to be important in cortical information processing and transmission. However, most studies of processing in the primary auditory cortex (AI) have viewed neurons as independent filters; little is known about how coordinated AI neuronal activity is expressed throughout cortical columns and how it might enhance the processing of auditory information. To address this, we recorded from populations of neurons in AI cortical columns of anesthetized rats and, using dimensionality reduction techniques, identified multiple coordinated neuronal ensembles (cNEs), which are groups of neurons with reliable synchronous activity. We show that cNEs reflect local network configurations with enhanced information encoding properties that cannot be accounted for by stimulus-driven synchronization alone. Furthermore, similar cNEs were identified in both spontaneous and evoked activity, indicating that columnar cNEs are stable functional constructs that may represent principal units of information processing in AI

Cell assembly dynamics of sparsely-connected inhibitory networks: a simple model for the collective activity of striatal projection neurons

Striatal projection neurons form a sparsely-connected inhibitory network, and this arrangement may be essential for the appropriate temporal organization of behavior. Here we show that a simplified, sparse inhibitory network of Leaky-Integrate-and-Fire neurons can reproduce some key features of striatal population activity, as observed in brain slices [Carrillo-Reid et al., J. Neurophysiology 99 (2008) 1435{1450]. In particular we develop a new metric to determine the conditions under which sparse inhibitory networks form anti-correlated cell assemblies with time-varying activity of individual cells. We found that under these conditions the network displays an input-specific sequence of cell assembly switching, that effectively discriminates similar inputs. Our results support the proposal [Ponzi and Wickens, PLoS Comp Biol 9 (2013) e1002954] that GABAergic connections between striatal projection neurons allow stimulus-selective, temporally-extended sequential activation of cell assemblies. Furthermore, we help to show how altered intrastriatal GABAergic signaling may produce aberrant network-level information processing in disorders such as Parkinson's and Huntington's diseases.Comment: 22 pages, 9 figure

Noise Suppression and Surplus Synchrony by Coincidence Detection

The functional significance of correlations between action potentials of neurons is still a matter of vivid debates. In particular it is presently unclear how much synchrony is caused by afferent synchronized events and how much is intrinsic due to the connectivity structure of cortex. The available analytical approaches based on the diffusion approximation do not allow to model spike synchrony, preventing a thorough analysis. Here we theoretically investigate to what extent common synaptic afferents and synchronized inputs each contribute to closely time-locked spiking activity of pairs of neurons. We employ direct simulation and extend earlier analytical methods based on the diffusion approximation to pulse-coupling, allowing us to introduce precisely timed correlations in the spiking activity of the synaptic afferents. We investigate the transmission of correlated synaptic input currents by pairs of integrate-and-fire model neurons, so that the same input covariance can be realized by common inputs or by spiking synchrony. We identify two distinct regimes: In the limit of low correlation linear perturbation theory accurately determines the correlation transmission coefficient, which is typically smaller than unity, but increases sensitively even for weakly synchronous inputs. In the limit of high afferent correlation, in the presence of synchrony a qualitatively new picture arises. As the non-linear neuronal response becomes dominant, the output correlation becomes higher than the total correlation in the input. This transmission coefficient larger unity is a direct consequence of non-linear neural processing in the presence of noise, elucidating how synchrony-coded signals benefit from these generic properties present in cortical networks

Neuron-level dynamics of oscillatory network structure and markerless tracking of kinematics during grasping

Oscillatory synchrony is proposed to play an important role in flexible sensory-motor transformations. Thereby, it is assumed that changes in the oscillatory network structure at the level of single neurons lead to flexible information processing. Yet, how the oscillatory network structure at the neuron-level changes with different behavior remains elusive. To address this gap, we examined changes in the fronto-parietal oscillatory network structure at the neuron-level, while monkeys performed a flexible sensory-motor grasping task. We found that neurons formed separate subnetworks in the low frequency and beta bands. The beta subnetwork was active during steady states and the low frequency network during active states of the task, suggesting that both frequencies are mutually exclusive at the neuron-level. Furthermore, both frequency subnetworks reconfigured at the neuron-level for different grip and context conditions, which was mostly lost at any scale larger than neurons in the network. Our results, therefore, suggest that the oscillatory network structure at the neuron-level meets the necessary requirements for the coordination of flexible sensory-motor transformations. Supplementarily, tracking hand kinematics is a crucial experimental requirement to analyze neuronal control of grasp movements. To this end, a 3D markerless, gloveless hand tracking system was developed using computer vision and deep learning techniques. 2021-11-3

LFP beta amplitude is predictive of mesoscopic spatio-temporal phase patterns

Beta oscillations observed in motor cortical local field potentials (LFPs) recorded on separate electrodes of a multi-electrode array have been shown to exhibit non-zero phase shifts that organize into a planar wave propagation. Here, we generalize this concept by introducing additional classes of patterns that fully describe the spatial organization of beta oscillations. During a delayed reach-to-grasp task in monkey primary motor and dorsal premotor cortices we distinguish planar, synchronized, random, circular, and radial phase patterns. We observe that specific patterns correlate with the beta amplitude (envelope). In particular, wave propagation accelerates with growing amplitude, and culminates at maximum amplitude in a synchronized pattern. Furthermore, the occurrence probability of a particular pattern is modulated with behavioral epochs: Planar waves and synchronized patterns are more present during movement preparation where beta amplitudes are large, whereas random phase patterns are dominant during movement execution where beta amplitudes are small

Modular deconstruction reveals the dynamical and physical building blocks of a locomotion motor program

The neural substrates of motor programs are only well understood for small, dedicated circuits. Here we investigate how a motor program is constructed within a large network. We imaged populations of neurons in the Aplysia pedal ganglion during execution of a locomotion motor program. We found that the program was built from a very small number of dynamical building blocks, including both neural ensembles and low-dimensional rotational dynamics. These map onto physically discrete regions of the ganglion, so that the motor program has a corresponding modular organization in both dynamical and physical space. Using this dynamic map, we identify the population potentially implementing the rhythmic pattern generator and find that its activity physically traces a looped trajectory, recapitulating its low-dimensional rotational dynamics. Our results suggest that, even in simple invertebrates, neural motor programs are implemented by large, distributed networks containing multiple dynamical systems