Switches to rhythmic brain activity lead to a plasticity-induced reset in synaptic weights

Abstract

1Neural circuits often alternate between tonic and burst firing - two distinct activity regimes that reflect changes in excitability and neuromodulatory state. While tonic firing produces asynchronous spiking driven by diverse external inputs, collective burst firing consists of rapid clusters of spikes followed by a period of silence, happening synchronously within the network. Synaptic plasticity has typically been studied only in either one of these regimes, leaving unclear how alternating states jointly shape long-term weight dynamics. Here, we use a conductance-based network model endowed with calcium-based or spike-timing-based plasticity rules to examine how synaptic weights evolve across state transitions. During tonic firing, synaptic weights are driven by the statistics of external inputs, producing a broad distribution across the network. In contrast, during collective burst firing, weights converge to a narrow region in weight space: a burst-induced attractor. We derive the location of this attractor analytically in terms of plasticity parameters and activity statistics, and confirm its emergence across diverse plasticity rules. The attractor reflects the synchronization of plasticity-driving signals during bursts, which homogenizes synaptic dynamics and forces convergence toward shared fixed points. We further show that neuromodulation and synaptic tagging can shift or split the burst-induced attractor, stabilizing selected synapses while weakening others. This mechanism reconciles flexibility during tonic-driven learning with stability during burst-driven consolidation. These results identify burst-induced attractors as a robust emergent property of networks combining collective bursting with soft-bound plasticity rules. By showing how they can be analytically predicted and experimentally modulated, our work provides a general computational framework linking state transitions, synaptic plasticity, and memory organization. 2 Author SummaryBrains operate in different activity states, reflecting different behaviors or neuromodulatory states. Neurons can fire isolated spikes in a tonic mode that encodes information about external inputs. They can fire rapid bursts of spikes, generating large synchronized oscillations that dominate population activity. Both tonic and burst firing are linked to learning and memory, yet their distinct contributions to shaping synaptic plasticity remain poorly understood. In this study, we use biophysical network models equipped with well-established plasticity rules to investigate how synaptic weights evolve under tonic and burst firing. We show that during tonic activity, synapses diverge toward a wide variety of values, reflecting the diversity of input statistics. In contrast, when the network enters a collective bursting state, synaptic weights collapse into a narrow region of weight space--a "burst-induced attractor." We derive the attractor mathematically and show that its position depends directly on the plasticity parameters, meaning it can be shifted or split through neuromodulatory and tag-dependent processes. Our results suggest that bursts provide a robust and controllable stage for synaptic consolidation. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=170 SRC="FIGDIR/small/500198v3_ufig1.gif" ALT="Figure 1"> View larger version (34K): org.highwire.dtl.DTLVardef@2ab6aeorg.highwire.dtl.DTLVardef@3f8199org.highwire.dtl.DTLVardef@155900borg.highwire.dtl.DTLVardef@63f520_HPS_FORMAT_FIGEXP M_FIG C_FIG