Impact of Cortical Network Activity on Short-term Synaptic Depression

Abstract

Repetitive stimulation of synaptic connections in the cerebral cortex often induces short-term synaptic depression (STD), a property directly related to the probability of transmitter release and critical for the computational properties of the network. In order to explore how spontaneous activity in the network affects this property, we first studied STD in cortical slices that were either silent or that displayed spontaneous rhythmic slow oscillations resembling those recorded during slow wave sleep in vivo. STD was considerably reduced by the occurrence of spontaneous rhythmic activity in the cortical network. Once the rhythmic activity started, depression decreased over time in parallel with the duration and intensity of the ongoing activity until a plateau was reached. Thalamocortical and intracortical synaptic potentials studied in vivo also showed stronger depression in a silent than in an active cortical network, and the depression values in the active cortical network in vivo were indistinguishable from those found in active slices in vitro. We suggest that this phenomenon is due to the different steady states of the synapses in active and in silent networks.

The Impact of an LGNd Impulse on the Awake Visual Cortex: Synaptic Dynamics and the Sustained/Transient Distinction

“…Moreover, they found that this depression saturated rapidly and that increases in thalamic activity beyond background levels generated only a mild increased depression. Our results are in general agreement with the finding of a chronic, rapidly saturating depression at the geniculocortical synapse (see also Reig et al, 2006). In contrast to previous work, however, our results are based on the analysis of single LGNd afferents, not summed activity of many electrically driven LGNd afferents.…”

Factors Controlling the Input–Output Relationship of Spherical Bushy Cells in the Gerbil Cochlear Nucleus

“…We address tonic depression as a final candidate. Most cells are silent in slices, but in vivo their spontaneous activity may induce tonic short-term synaptic depression (Boudreau and Ferster, 2005;Reig et al, 2006;Hermann et al, 2007;Wang et al, 2010). In slices, a fast recovery phase has been observed, which depends on calcium buildup within the endbulb (Wang and Manis, 2008;Yang and Xu-Friedman, 2008).…”

State Changes Rapidly Modulate Cortical Neuronal Responsiveness

“…Network responsiveness after the cessation of an Up state may be reduced through use-dependent depression of recurrent cortical connections (Crochet et al, 2004;Crochet and Petersen, 2006;Reig et al, 2006), the buildup of a slow afterhyperpolarization (Sanchez-Vives and McCormick, 2000;McCormick et al, 2003;Shu et al, 2003a), reduction in synaptic potentials through activity-dependent decreases in extracellular [Ca 2ϩ ] (Crochet and Petersen, 2006), or the slow activation or inactivation of a voltage-dependent inhibitory conductance (Bal and McCormick, 1996;Compte et al, 2003). The disproportionately increased excitability of fast-spiking inhibitory interneurons during the Up state may also result in reduced recurrent network activity, by enhancing the inhibitory contribution to whisker-evoked responses and consequently reducing the ability of excitatory inputs to initiate action potentials.…”

“…Increased corticothalamic feedback during the Up state may also shift the thalamus out of the burst firing mode, resulting in a decrease in the number or frequency of spikes initiated in thalamocortical neurons by the whisker movement (McCormick and von Krosigk, 1992;Weyand et al, 2001) [see, however, Haslinger et al, (2006)]. Finally, tonic activity during the Up state may reduce responses to brief whisker stimuli through synaptic depression at the thalamocortical synapse (Gil et al, 1997;Beierlein and Connors, 2002;CastroAlamancos and Oldford, 2002;Hirata and Castro-Alamancos, 2006;Reig et al, 2006).…”