Abstract
Neuronal activity is characterized by a diversity of oscillatory phenomena that are associated with multiple behavioral and cognitive processes, yet the functional consequences of these oscillations are not fully understood. Our aim was to determine whether and how these different oscillatory activities affect short-term synaptic plasticity (STP), using the olfactory system as a model. In response to odorant stimuli, the olfactory bulb displays a slow breathing rhythm as well as beta and gamma oscillations. Since the firing of olfactory bulb projecting neurons is phase-locked with beta and gamma oscillations, structures downstream from the olfactory bulb should be driven preferentially at these frequencies. We examined STP exhibited by olfactory bulb inputs in slices of adult mouse piriform cortex maintained in vitro in an in vivo-like ACSF (calcium concentration: 1.1 mM). We replaced the presynaptic neuronal firing rate by repeated electrical stimulation (frequency between 3.125 and 100 Hz) applied to the lateral olfactory tract. Our results revealed a considerable enhancement of postsynaptic response amplitude for stimulation frequencies in the beta and gamma range. A phenomenological model of STP fitted to the data suggests that the experimental results can be explained by the interplay between three mechanisms: a short-term facilitation mechanism (time constant ≈160 msec), and two short-term depression mechanisms (recovery time constants <20 msec and ≈140 msec). Increasing calcium concentration (2.2 mM) resulted in an increase in the time constant of facilitation and in a strengthening of the slowest depression mechanism. As a result, response enhancement was reduced and its peak shifted toward the low beta and alpha ranges while depression became predominant in the gamma band. Using environmental conditions corresponding to those that prevail in vivo, our study shows that STP in the lateral olfactory tract to layer Ia synapse allows amplification of olfactory bulb inputs at beta and gamma frequencies.
Highlights
EEG and intracerebral LFP recordings have disclosed a variety of oscillatory phenomena in the brain
Response enhancement was maximal in the beta range and was strong in the gamma range. These results suggest that short-term plasticity in layer Ia of the piriform cortex allows amplification of synaptic responses at frequencies corresponding to odor-induced beta and gamma oscillations in the olfactory bulb
The synaptic plasticity (STP) model fitted to the data indicated that this enhancement was essentially achieved through the interaction of 3 mechanisms: a facilitation mechanism with a recovery time constant of 157 msec on average, that resulted in a progressive increase in response amplitude when stimulation frequency was > about 2 Hz, a fast depression mechanism with a recovery time constant of 19 msec that curtailed facilitation
Summary
EEG and intracerebral LFP recordings have disclosed a variety of oscillatory phenomena in the brain. Theta waves (typically 6–12 Hz in awake rodents) have been mostly studied in the hippocampus where they occur during a variety of behaviors as well as during REM sleep [4, 5]. Alpha waves (8–12 Hz), most prominent in visual cortex, are associated with rest [6] and may be involved in awareness and attention [7]. With frequencies larger than 25–35 Hz, are typically observed during the processing of sensory stimuli in visual [13,14,15,16], somesthetic [17, 18] and auditory cortices [19, 20] as well as during various cognitive tasks involving awareness, attention and memory (reviewed in: [21, 22])
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