Prominent facilitation at beta and gamma frequency range revealed with physiological calcium concentration in adult mouse piriform cortex in vitro

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.

Effect of adenosine on short-term synaptic plasticity in mouse piriform cortex in vitro: adenosine acts as a high-pass filter

“…Brain slices were prepared as previously described (Gleizes et al. ). In short: the brains of 2‐ to 4‐month‐old C57BL/6 female mice were extracted after deep anesthetization with isoflurane.…”

“…The in vivo‐like ACSF composition was based on ionic concentrations measured in rodent interstitial and cerebrospinal fluids in vivo (for references see Gleizes et al. ) and consisted in (in mmol/L): NaCl 124, NaHCO 3 26, KCl 3.2, MgSO 4 1, NaH 2 PO 4 0.5, CaCl 2 1.1, and glucose 10. This ACSF was continuously bubbled with a 95% O 2 /5% CO 2 mixture (pH 7.4).…”

“…() and Oswald and Urban (), has been described previously (Gleizes et al. ). Two versions of the model were used in this study: the first stipulates that one single facilitation mechanism can account for the data while the second allows for the presence of either one or two depression mechanisms in addition to facilitation.…”

“…In a previous in vitro study (Gleizes et al. ), we studied STP in the adult mouse olfactory system, at the connection between the olfactory bulb output and layer 1a of the anterior piriform cortex. In the olfactory bulb, odorant stimulation triggers three kinds of oscillations: beta (15 to 35–40 Hz) and gamma (>35–40 Hz) fluctuations that are superimposed onto a slow breathing rhythm (1–10 Hz) (e.g., Adrian ; Chapman et al.…”

“…A phenomenological model fitted to the data suggested that the frequency‐dependence of this enhancement was determined by the interaction between STF and STD mechanisms acting on different time scales (Gleizes et al. ).…”