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Abstract
Anatomic connections between brain areas affect information flow between neuronal circuits and the synchronization of neuronal activity. However, such structural connectivity does not coincide with effective connectivity (or, more precisely, causal connectivity), related to the elusive question “Which areas cause the present activity of which others?”. Effective connectivity is directed and depends flexibly on contexts and tasks. Here we show that dynamic effective connectivity can emerge from transitions in the collective organization of coherent neural activity. Integrating simulation and semi-analytic approaches, we study mesoscale network motifs of interacting cortical areas, modeled as large random networks of spiking neurons or as simple rate units. Through a causal analysis of time-series of model neural activity, we show that different dynamical states generated by a same structural connectivity motif correspond to distinct effective connectivity motifs. Such effective motifs can display a dominant directionality, due to spontaneous symmetry breaking and effective entrainment between local brain rhythms, although all connections in the considered structural motifs are reciprocal. We show then that transitions between effective connectivity configurations (like, for instance, reversal in the direction of inter-areal interactions) can be triggered reliably by brief perturbation inputs, properly timed with respect to an ongoing local oscillation, without the need for plastic synaptic changes. Finally, we analyze how the information encoded in spiking patterns of a local neuronal population is propagated across a fixed structural connectivity motif, demonstrating that changes in the active effective connectivity regulate both the efficiency and the directionality of information transfer. Previous studies stressed the role played by coherent oscillations in establishing efficient communication between distant areas. Going beyond these early proposals, we advance here that dynamic interactions between brain rhythms provide as well the basis for the self-organized control of this “communication-through-coherence”, making thus possible a fast “on-demand” reconfiguration of global information routing modalities.
Highlights
In Arcimboldo’s (1527–1593) paintings, whimsical portraits emerge out of arrangements of flowers and vegetables
Mechanisms for effective connectivity switching We have shown that a simple structural motif of interacting brain areas can give rise to multiple effective motifs with different directionality and strengths of effective connectivity, organized into different families
Such effective motifs correspond to distinct dynamical states of the underlying structural motif
Summary
In Arcimboldo’s (1527–1593) paintings, whimsical portraits emerge out of arrangements of flowers and vegetables. The capacity to detect faces in an Arcimboldo canvas may be lost when lesions impair the connectivity between these areas [2]. It is not conceivable, that, in a healthy subject, shifts between alternate perceptions are obtained by actual ‘‘plugging and unplugging’’ of synapses, as in a manual telephone switchboard. Brain functions –from vision [3] or motor preparation [4] up to memory [5], attention [6,7,8] or awareness [9]– as well as their complex coordination [10] require the control of inter-areal interactions on time-scales faster than synaptic changes [11,12]. How can manifold effective connectivities –corresponding to different patterns of interareal interactions, or brain states [17]– result from a fixed structural connectivity? And how can effective connectivity be controlled without resorting to structural plasticity, leading to a flexible ‘‘on demand’’ selection of function?
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