Short-term synaptic dynamics control the activity phase of neurons in an oscillatory network

Abstract

In oscillatory systems, neuronal activity phase is often independent of network frequency. Such phase maintenance requires adjustment of synaptic input with network frequency, a relationship that we explored using the crab, Cancer borealis, pyloric network. The burst phase of pyloric neurons is relatively constant despite a > two fold variation in network frequency. We used noise input to characterize how input shape influences burst delay of a pyloric neuron, and then used dynamic clamp to examine how burst phase depends on the period, amplitude, duration, and shape of rhythmic synaptic input. Phase constancy across a range of periods required a proportional increase of synaptic duration with period. However, phase maintenance was also promoted by an increase of amplitude and peak phase of synaptic input with period. Mathematical analysis shows how short-term synaptic plasticity can coordinately change amplitude and peak phase to maximize the range of periods over which phase constancy is achieved.

The differential contribution of pacemaker neurons to synaptic transmission in the pyloric network of the Jonah crab, Cancer borealis

“…where g dyn was the maximal synaptic conductance and the reversal potential E dyn was set to Ϫ80 mV. The synaptic conductance waveform w(t) was a predefined waveform, as previously described (Martinez et al 2019). For each value of g dyn , I dyn was applied repetitively with a cycle period of 1 s for at least 30 s, and only the last five cycles were analyzed.…”

“…Most recent studies of the pyloric circuit use the crab Cancer borealis as the experimental species (Blitz 2017;Follmann et al 2017;Haddad and Marder 2018;Haley et al 2018;Lett et al 2017;Li et al 2018;Martinez et al 2019;Otopalik et al 2017; White et al 2017). In C. borealis, however, the neurotransmitters used by the pacemaker AB and PD neurons have not entirely been described, and the relative contribution of the AB and PD synapses to the total pacemaker synaptic output exerted on the follower pyloric neurons remains unquantified.…”

Frequency-Dependent Action of Neuromodulation

“…Although in the LP neuron the transient inward current I MI-T has an even higher maximal conductance value than I MI , it does not elicit oscillatory activity in this neuron. This is probably because, in the absence of inhibitory input, the resting membrane potential of the LP neuron is fairly depolarized (Martinez et al, 2019), leading to the inactivation of I MI-T .…”

“…For example, thalamocortical neurons produce bursting oscillations arising from the T-type calcium current (I CaT ), but only when the baseline membrane potential is hyperpolarized (Amarillo et al, 2014;Steriade and Contreras, 1995). Additionally, responses of bursting neurons critically depend on strength, frequency, short-term plasticity, and temporal trajectory of their synaptic input (Martinez et al, 2019). In many circuits, neurons burst upon rebound from synaptic inhibition (Bucher et al, 2015;Huguenard and McCormick, 2007).…”

“…However, the effect of I MI on follower neurons, which can provide feedback to pacemaker neurons, is less understood. The strength, shape and frequency of inhibition influence the voltage trajectory of the burst response of follower neurons (Harris-Warrick et al, 1995b, 1995aHooper, 1998;Kloppenburg et al, 1999;Martinez et al, 2019). Because this voltage trajectory determines the activation of all voltage-gated ionic currents, it also controls the levels of currents regulated by such modulators.…”