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Modulation of network-to-network connectivity via spike-timing-dependent noninvasive brain stimulation.

ABSTRACT: Human cognitive abilities and behavior are linked to functional coupling of many brain regions organized in distinct networks. Gaining insights on the role those networks' dynamics play in cognition and pathology requires their selective, reliable, and reversible manipulation. Here we document the possibility to manipulate the interplay between two brain networks in a controlled manner, by means of a Transcranial Magnetic Stimulation (TMS) protocol inducing spike timing dependent plasticity (STDP). Pairs of TMS pulses at specific inter-stimulus intervals, repeatedly delivered over two negatively correlated nodes of the default mode network (DMN) and the task-positive network (TPN) defined on the basis of individual functional magnetic resonance imaging (fMRI) data, induced a modulation of network-to-network connectivity, even reversing correlation from negative to slightly positive in 30% of cases. Results also suggest a baseline-dependent effect, with a greater connectivity modulation observed in participants with weaker between-networks connectivity strength right before TMS. Finally, modulation of task-evoked fMRI activity patterns during a sustained attention task was also observed after stimulation, with a faster or slower switch between rest and task blocks according to the timing of TMS pulses. The present findings promote paired associative TMS as a promising technique for controlled manipulation of fMRI connectivity dynamics in humans, as well as the causal investigation of brain-behavior relations.

SUBMITTER: Santarnecchi E

PROVIDER: S-EPMC6866459 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Modulation of network-to-network connectivity via spike-timing-dependent noninvasive brain stimulation.

Santarnecchi Emiliano E Momi Davide D Sprugnoli Giulia G Neri Francesco F Pascual-Leone Alvaro A Rossi Alessandro A Rossi Simone S

Human brain mapping 20180816 12

Human cognitive abilities and behavior are linked to functional coupling of many brain regions organized in distinct networks. Gaining insights on the role those networks' dynamics play in cognition and pathology requires their selective, reliable, and reversible manipulation. Here we document the possibility to manipulate the interplay between two brain networks in a controlled manner, by means of a Transcranial Magnetic Stimulation (TMS) protocol inducing spike timing dependent plasticity (STD ...[more]

PMID: 30113111

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Project description:Classic in vitro studies have described spike-timing-dependent plasticity (STDP) at a synapse: the connection from neuron A to neuron B is strengthened (or weakened) when A fires before (or after) B within an optimal time window. Accordingly, more recent in vivo works have demonstrated behavioral effects consistent with an STDP mechanism; however, many relied on single-unit recordings. The ability to modify cortical connections becomes useful in the context of injury, when connectivity and associated behavior are compromised. To avoid the need for long-term, stable isolation of single units, one could control timed activation of two cortical sites with paired electrical stimulation. We tested the hypothesis that STDP could be induced via prolonged paired stimulation as quantified by cortical evoked potentials (EPs) in the sensorimotor cortex of awake, behaving monkeys. Paired simulation between two interconnected sites produced robust effects in EPs consistent with STDP, but only at 2/15 tested pairs. The stimulation protocol often produced increases in global network excitability or depression of the conditioned pair. Together, these results suggest that paired stimulation in vivo is a viable method to induce STDP between cortical populations, but that factors beyond activation timing must be considered to produce conditioning effects.SIGNIFICANCE STATEMENT Plasticity of neural connections is important for development, learning, memory, and recovery from injury. Cellular mechanisms underlying spike-timing-dependent plasticity have been studied extensively in vitro Recent in vivo work has demonstrated results consistent with the previously defined cellular mechanisms; however, the output measure in these studies was typically an indirect assessment of plasticity at the neural level. Here, we show direct plasticity in recordings of neuronal populations in awake, behaving nonhuman primates induced by paired electrical stimulation. In contrast to in vitro studies, we found that plastic effects were only produced between specific cortical areas. These findings suggest that similar mechanisms drive plasticity in vitro and in vivo, but that cortical architecture may contribute significantly to site-dependent effects.

Project description:Neuronal oscillatory activity has been reported in relation to a wide range of cognitive processes including the encoding of external stimuli, attention, and learning. Although the specific role of these oscillations has yet to be determined, it is clear that neuronal oscillations are abundant in the central nervous system. This raises the question of the origin of these oscillations: are the mechanisms for generating these oscillations genetically hard-wired or can they be acquired via a learning process? Here, we study the conditions under which oscillatory activity emerges through a process of spike timing dependent plasticity (STDP) in a feed-forward architecture. First, we analyze the effect of oscillations on STDP-driven synaptic dynamics of a single synapse, and study how the parameters that characterize the STDP rule and the oscillations affect the resultant synaptic weight. Next, we analyze STDP-driven synaptic dynamics of a pre-synaptic population of neurons onto a single post-synaptic cell. The pre-synaptic neural population is assumed to be oscillating at the same frequency, albeit with different phases, such that the net activity of the pre-synaptic population is constant in time. Thus, in the homogeneous case in which all synapses are equal, the post-synaptic neuron receives constant input and hence does not oscillate. To investigate the transition to oscillatory activity, we develop a mean-field Fokker-Planck approximation of the synaptic dynamics. We analyze the conditions causing the homogeneous solution to lose its stability. The findings show that oscillatory activity appears through a mechanism of spontaneous symmetry breaking. However, in the general case the homogeneous solution is unstable, and the synaptic dynamics does not converge to a different fixed point, but rather to a limit cycle. We show how the temporal structure of the STDP rule determines the stability of the homogeneous solution and the drift velocity of the limit cycle.

Dataset Information

Modulation of network-to-network connectivity via spike-timing-dependent noninvasive brain stimulation.

Publications

Modulation of network-to-network connectivity via spike-timing-dependent noninvasive brain stimulation.

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