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di Volo, M.

Publications and source records attributed to di Volo, M..

11 recordsLinked to original sources

Prefrontal mechanisms of goal progress inference and monitoring in macaque monkeys

Primates pursue goals over extended periods and over multiple steps. The ability to track progress and its rate is critical for such pursuit, yet the neural mechanisms of this tracking are unclear. We recorded single-unit activity from macaque midcingulate cortex (MCC) and lateral prefrontal cortex (LPFC) whilst animals worked for immediate rewards and checked a gauge showing progress towards a larger reward. MCC expressed a temporally extended progress rate signal linked to the long timescale neurons in the region. LPFC expressed progress rate only when inferences on that property were required. In MCC, independent feedback-valence information was also preserved, enabling both readout of work success and rate-specific progress updating. An RNN trained under the same constraints showed that progress rate representations emerge spontaneously, and are critical for tracking goal progress. These results demonstrate a frontal mechanism for inferring and predicting goal progress by extracting progress rate information.

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A cortical microcircuit model reveals distinct inhibitory mechanisms of network oscillations and stability

We identify a computational mechanism for network oscillations distinct from classic excitatory-inhibitory networks - CAMINOS (Canonical Microcircuit Network Oscillations) - in which different inhibitory-interneuron classes make distinct causal contributions to network oscillations and stability. A computational network model of the canonical microcircuit consisting of SOM, PV and excitatory neurons reproduced key experimental findings, including: Stochastic gamma oscillations with drive-dependent frequency; precise phase-locking of PV interneurons and delayed firing of SOM interneurons; and the distinct effects of optogenetic perturbations of SOM and PV cells. In CAMINOS, the generation of network oscillations depends on both the precise spike timing of SOM and PV interneurons, with PV cells regulating oscillation frequency and network stability, and delayed SOM firing controlling the oscillation amplitude. The asymmetric PV-SOM connectivity is found to be the key source ingredient to generate these oscillations, that naturally establishes distinct PV and SOM-cell spike timing. The CAMINOS model predicts that increased SOM/PV densities along the cortical hierarchy leads to decreased oscillation frequencies (from gamma to alpha/beta) and increased seizure susceptibility, suggesting a unified circuit model for oscillations across different frequency bands.

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Discrete synaptic events induce global oscillations in balanced neural networks

Neural dynamics is triggered by discrete synaptic inputs of finite amplitude. However, the neural response is usually obtained within the diffusion approximation (DA) representing the synaptic inputs as Gaussian noise. We derive a mean-field formalism encompassing synaptic shot-noise for sparse balanced networks of spiking neurons. For low (high) external drives (synaptic strenghts) irregular global oscillations emerge via continuous and hysteretic transitions, correctly predicted by our approach, but not from the DA. These oscillations display frequencies in biologically relevant bands.

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Hippocampal gamma oscillations form complex ensembles modulated by behavior and learning

The hippocampus and the entorhinal cortex display a rich oscillatory activity, believed to support neural information processing in key cognitive functions1. In the hippocampal region CA1, a "slow gamma" rhythm (30-80 Hz) generated in CA3 would support memory retrieval whereas a "medium gamma" rhythm (60-120 Hz) generated in the entorhinal cortex would support memory encoding2,3. However, descriptions involving discrete gamma sub-bands can only partially account for the haphazard diversity of oscillatory behaviors observed in individual recordings during spatial navigation behavior. Here, we stress that transient gamma oscillatory episodes at any frequency or phase relative to the ongoing theta (4-12 Hz) rhythm can be recorded at any layer within CA1. Eventually, the commonly reported averages are dominated by a minority of very strong power events overshadowing gamma heterogeneity. Nevertheless, we show that such gamma diversity can be naturally explained by a simple mechanistic model, and that behavior-related information (position within a maze) can be decoded from most individual gamma events, despite their low power and erratic-like nature. Our results indicate that behavior specifically shapes ensembles of irregular hippocampal gamma oscillations, in a way which evolves with learning, depends on the hippocampal layer and is hard to reconcile with the hypothesis of rigid, narrowly tuned gamma sub-bands. Beyond randomness, the pervasive gamma diversity may thus reflect complexity at the "fringe-of-synchrony"4 likely functional but invisible to classic average-based analyses.

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Asynchronous and coherent dynamics in balanced excitatory-inhibitory populations

Dynamic excitatory-inhibitory (E-I) balance is a paradigmatic mechanism invoked to explain the irregular low firing activity observed in the cortex. However, we will show that the E-I balance can be at the origin of other regimes observable in the brain. The analysis is performed by combining extensive simulations of sparse E-I networks composed of N spiking neurons with analytical investigations of low dimensional neural mass models. The bifurcation diagrams, derived for the neural mass model, allow to classify the possible asynchronous and coherent behaviours emerging in balanced E-I networks with structural heterogeneity for any finite in-degree K. In the limit N >> K >> 1 both supra and sub-threshold balanced asynchronous regimes can be observed in our system. Due to the heterogeneity the asynchronous states are characterized by the splitting of the neurons in three groups: silent, fluctuation and mean driven. These features are consistent with experimental observations reported for heterogeneous neural circuits. The coherent rhythms observed in our system can range from periodic and quasi-periodic collective oscillations (COs) to coherent chaos. These rhythms are characterized by regular or irregular temporal fluctuations joined to spatial coherence somehow similar to coherent fluctuations observed in the cortex over multiple spatial scales. The COs can emerge due to two different mechanisms. A first mechanism similar to the pyramidal-interneuron gamma (PING) one, usually invoked for the emergence of{gamma} -oscillations. The second mechanism is intimately related to the presence of current fluctuations, which sustain COs characterized by an essentially simultaneous bursting of the two populations. We observe period-doubling cascades involving the PING-like COs finally leading to the appearance of coherent chaos. Fluctuation driven COs are usually observable in our system as quasi-periodic collective motions characterized by two incommensurate frequencies. However, for sufficiently strong current fluctuations we report a novel mechanism of frequency locking among collective rhythms promoted by these intrinsic fluctuations. Our analysis suggest that despite PING-like or fluctuation driven COS are observable for any finite in-degree K, in the limit N >> K >> 1 these solutions finally result in two coexisting balanced regimes: an asynchronous and a fully synchronized one.

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A reduction methodology for fluctuation driven population dynamics

Lorentzian distributions have been largely employed in statistical mechanics to obtain exact results for heterogeneous systems. Analytic continuation of these results is impossible even for slightly deformed Lorentzian distributions, due to the divergence of all the moments (cumulants). We have solved this problem by introducing a pseudo-cumulants expansion. This allows us to develop a reduction methodology for heterogeneous spiking neural networks subject to extrinsinc and endogenous fluctuations, thus obtaining an unified mean-field formulation encompassing quenched and dynamical disorder sources.

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A mean-field approach to the dynamics of networks of complex neurons, from nonlinear Integrate-and-Fire to Hodgkin-Huxley models

We present a mean-field formalism able to predict the collective dynamics of large networks of conductance-based interacting spiking neurons. We apply this formalism to several neuronal models, from the simplest Adaptive Exponential Integrate-and-Fire model to the more complex Hodgkin-Huxley and Morris-Lecar models. We show that the resulting mean-field models are capable of predicting the correct spontaneous activity of both excitatory and inhibitory neurons in asynchronous irregular regimes, typical of cortical dynamics. Moreover, it is possible to quantitatively predict the populations response to external stimuli in the form of external spike trains. This mean-field formalism therefore provides a paradigm to bridge the scale between population dynamics and the microscopic complexity of the individual cells physiology. NEW & NOTEWORTHYPopulation models are a powerful mathematical tool to study the dynamics of neuronal networks and to simulate the brain at macroscopic scales. We present a mean-field model capable of quantitatively predicting the temporal dynamics of a network of complex spiking neuronal models, from Integrate-and-Fire to Hodgkin-Huxley, thus linking population models to neurons electrophysiology. This opens a perspective on generating biologically realistic mean-field models from electrophysiological recordings.

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Coexistence of fast and slow gamma oscillations in one population of inhibitory spiking neurons

Oscillations are a hallmark of neural population activity in various brain regions with a spectrum covering a wide range of frequencies. Within this spectrum gamma oscillations have received particular attention due to their ubiquitous nature and to their correlation with higher brain functions. Recently, it has been reported that gamma oscillations in the hippocampus of behaving rodents are segregated in two distinct frequency bands: slow and fast. These two gamma rhythms correspond to different states of the network, but their origin has been not yet clarified. Here, we show theoretically and numerically that a single inhibitory population can give rise to coexisting slow and fast gamma rhythms corresponding to collective oscillations of a balanced spiking network. The slow and fast gamma rhythms are generated via two different mechanisms: the fast one being driven by the coordinated tonic neural firing and the slow one by endogenous fluctuations due to irregular neural activity. We show that almost instantaneous stimulations can switch the collective gamma oscillations from slow to fast and vice versa. Furthermore, to make a closer contact with the experimental observations, we consider the modulation of the gamma rhythms induced by a slower (theta) rhythm driving the network dynamics. In this context, depending on the strength of the forcing and the noise amplitude, we observe phase-amplitude and phase-phase coupling between the fast and slow gamma oscillations and the theta forcing. Phase-phase coupling reveals on average different theta-phases preferences for the two coexisting gamma rhythms joined to a wide cycle-to-cycle variability.

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A state-dependent mean-field formalism to model different activity states in conductance based networks of spiking neurons

Higher and higher interest has been shown in the recent years to large scale spiking simulations of cerebral neuronal networks, coming both from the presence of high performance computers and increasing details in the experimental observations. In this context it is important to understand how population dynamics are generated by the designed parameters of the networks, that is the question addressed by mean field theories. Despite analytic solutions for the mean field dynamics has already been proposed generally for current based neurons (CUBA), the same for more realistic neural properties, such as conductance based (COBA) network of adaptive exponential neurons (AdEx), a complete analytic model has not been achieved yet. Here, we propose a novel principled approach to map a COBA on a CUBA. Such approach provides a state-dependent approximation capable to reliably predict the firing rate properties of an AdEx neuron with non-instantaneous COBA integration. We also applied our theory to population dynamics, predicting the dynamical properties of the network in very different regimes, such as asynchronous irregular (AI) and synchronous irregular (SI) (slow oscillations, SO). This results show that a state-dependent approximation can be successfully introduced in order to take into account the subtle effects of COBA integration and to deal with a theory capable to correctly predicts the activity in regimes of alternating states like slow oscillations.

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Two types of slow waves in anesthetized and sleeping brains

Sleep slow waves are known to participate in memory consolidation, yet slow waves occurring under anesthesia present no positive effects on memory. Here, we shed light onto this paradox, based on a combination of extracellular recordings in vivo, in vitro, and computational models. We find two types of slow waves, based on analyzing the temporal patterns of successive slow-wave events. The first type is consistently observed in natural slow-wave sleep, while the second is shown to be ubiquitous under anesthesia. Network models of spiking neurons predict that the two slow wave types emerge due to a different gain on inhibitory vs excitatory cells and that different levels of spike-frequency adaptation in excitatory cells can account for dynamical distinctions between the two types. This prediction was tested in vitro by varying adaptation strength using an agonist of acetylcholine receptors, which demonstrated a neuromodulatory switch between the two types of slow waves. Finally, we show that the first type of slow-wave dynamics is more sensitive to external stimuli, which can explain how slow waves in sleep and anesthesia differentially affect memory consolidation, as well as provide a link between slow-wave dynamics and memory diseases.

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Mean-field model for the dynamics of conductance-based networks of excitatory and inhibitory spiking neurons with adaptation

Accurate population models are needed to build very large scale neural models, but their derivation is difficult for realistic networks of neurons, in particular when nonlinear properties are involved such as conductance-based interactions and spike-frequency adaptation. Here, we consider such models based on networks of Adaptive exponential Integrate and fire excitatory and inhibitory neurons. Using a Master Equation formalism, we derive a mean-field model of such networks and compare it to the full network dynamics. The mean-field model is capable to correctly predict the average spontaneous activity levels in asynchronous irregular regimes similar to in vivo activity. It also captures the transient temporal response of the network to complex external inputs. Finally, the mean-field model is also able to quantitatively describe regimes where high and low activity states alternate (UP-DOWN state dynamics), leading to slow oscillations. We conclude that such mean-field models are \"biologically realistic\" in the sense that they can capture both spontaneous and evoked activity, and they naturally appear as candidates to build very large scale models involving multiple brain areas.

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