Adaptation at Synaptic Connections to Layer 2/3 Pyramidal Cells in Rat Visual Cortex

Abstract

Neocortical synapses express differential dynamic properties. When activated at high frequencies, the amplitudes of the subsequent postsynaptic responses may increase or decrease, depending on the stimulation frequency and on the properties of that particular synapse. Changes in the synaptic dynamics can dramatically affect the communication between nerve cells. Motivated by this question, we studied dynamic properties at synapses to layer 2/3 pyramidal cells with intracellular recordings in slices of rat visual cortex. Synaptic responses were evoked by trains of test stimuli, which consisted of 10 pulses at different frequencies (5–40 Hz). Test stimulation was applied either without any adaptation (control) or 2 s after an adaptation stimulus, which consisted of 4 s stimulation of these same synapses at 10, 25, or 40 Hz. The synaptic parameters were then assessed from fitting the data with a model of synaptic dynamics. Our estimates of the synaptic parameters in control, without adaptation are broadly consistent with previous studies. Adaptation led to pronounced changes of synaptic transmission. After adaptation, the amplitude of the response to the first pulse in the test train decreased for several seconds and then recovered back to the control level with a time constant of 2–18 s. Analysis of the data with extended models, which include interaction between different pools of synaptic vesicles, suggests that the decrease of the response amplitude was due to a synergistic action of two factors, decrease of the release probability and depletion of the available transmitter. After a weak (10 Hz) adaptation, the decrease of the response amplitude was accompanied by and correlated with the decrease of the release probability. After a strong adaptation (25 or 40 Hz), the depletion of synaptic resources was the main cause for the reduced response amplitude. Adaptation also led to pronounced changes of the time constants of facilitation and recovery, however, these changes were not uniform in all synapses, and on the population level, the only consistent and significant effect was an acceleration of the recovery after a strong adaptation. Taken together, our results suggest, that apart from decreasing the amplitude of postsynaptic responses, adaptation may produce synapse-specific effects, which could result in a kind of re-distribution of activity within neural networks.