Abstract
Short-term depression is a low-pass filter of synaptic information, reducing synaptic information transfer at high presynaptic firing frequencies. Consequently, during elevated presynaptic firing, little information passes to the postsynaptic neuron. However, many neurons fire at relatively high frequencies all the time. Does depression silence their synapses? We tested this apparent contradiction in the indirect pathway of the basal ganglia. Using numerical modeling and whole-cell recordings from single entopeduncular nucleus (EP) neurons in rat brain slices, we investigated how different firing rates of globus pallidus (GP) neurons affect information transmission to the EP. Whole-cell recordings showed significant variability in steady-state depression, which decreased as stimulation frequency increased. Modeling predicted that this variability would translate into different postsynaptic noise levels during constitutive presynaptic activity. Our simulations further predicted that individual GP-EP synapses mediate gain control. However, when we consider the integration of multiple inputs, the broad range of GP firing rates would enable different modes of information transmission. Finally, we predict that changes in dopamine levels can shift the action of GP neurons from rate coding to gain modulation. Our results thus demonstrate how short-term depression shapes information transmission in the basal ganglia in particular and via GABAergic synapses in general.
Highlights
Short-term depression is a low-pass filter of synaptic information, reducing synaptic information transfer at high presynaptic firing frequencies
The steady-state depression of the globus pallidus (GP)-entopeduncular nucleus (EP) synapse in our model increased exponentially with the presynaptic firing rate, in a similar manner to that found in slices[11,14] (Fig. 1E,F)
We explored the role of short-term depression on information transmission in a constitutively active GABAergic synapse of the basal ganglia’s indirect pathway
Summary
Short-term depression is a low-pass filter of synaptic information, reducing synaptic information transfer at high presynaptic firing frequencies. Whole-cell recordings showed significant variability in steady-state depression, which decreased as stimulation frequency increased Modeling predicted that this variability would translate into different postsynaptic noise levels during constitutive presynaptic activity. Tsodyks and Markram showed that cortical excitatory synapses displaying short-term depression have a limiting frequency above which changes in presynaptic firing only marginally affect the postsynaptic membrane potential[5]. We obtained paired recordings from GP neurons and showed that despite substantial depression, www.nature.com/scientificreports the constitutively active GP-GP inhibitory synapse transmitted information to postsynaptic targets as a result of temporal summation[16]. We used numerical modeling and whole-cell patch-clamp recordings to shed light on the contribution of diverse presynaptic activity on information transmission in the basal ganglia indirect pathway in particular, and via GABAergic synapses in general Why do GP neurons fire at such a wide range? How is information transmission during movement affected by the baseline firing rate of GP neurons? Here, we used numerical modeling and whole-cell patch-clamp recordings to shed light on the contribution of diverse presynaptic activity on information transmission in the basal ganglia indirect pathway in particular, and via GABAergic synapses in general
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