Single-unit activity in piriform cortex during slow-wave state is shaped by recent odor experience

Abstract

Memory and its underlying neural plasticity play important roles in sensory discrimination and cortical pattern recognition in olfaction. Given the reported function of slow-wave sleep states in neocortical and hippocampal memory consolidation, we hypothesized that activity during slow-wave states within the piriform cortex may be shaped by recent olfactory experience. Rats were anesthetized with urethane and allowed to spontaneously shift between slow-wave and fast-wave states as recorded in local field potentials within the anterior piriform cortex. Single-unit activity of piriform cortical layer II/III neurons was recorded simultaneously. The results suggest that piriform cortical activity during slow-wave states is shaped by recent (several minutes) odor experience. The temporal structure of single-unit activity during slow waves was modified if the animal had been stimulated with an odor within the receptive field of that cell. If no odor had been delivered, the activity of the cell during slow-wave activity was stable across the two periods. The results demonstrate that piriform cortical activity during slow-wave state is shaped by recent odor experience, which could contribute to odor memory consolidation.

Figure 1.

A, LFP recordings in aPCX revealed spontaneous shifts between SWA and FWA as reported previously (Murakami et al., 2005). The top shows a pseudocolor plot of the LFP fast Fourier transform analysis filtered to emphasize the large delta frequency (1–4 Hz) activity during SWA. B, During SWA, single units fired in-phase with the slow waves as shown in a PSWTH, although different cells had peak activity at different phases of the wave. C, Single-unit odor responses were reduced during SWA compared with FWA. The raster plot and LFPs show that, as an animal cycles through FWA and SWA, odor response magnitude similarly cycles. There was a gradual habituation across repeated FWA states. For direct comparison, responses to the first six stimuli in each state are shown side by side. D, Single-unit and LFP activity were decoupled from respiration during SWA compared with FWA. Histograms show respiratory events as a function of single-unit spiking (at arrowheads). LFPs are mean waveforms triggered on single-unit spikes (at arrowheads). Overdrawn waveform of single unit used for analysis in D in shown at bottom.

Figure 2.

A, Basic experimental design. Spontaneous cortical activity was monitored during SWA (no odor was delivered during SWA). Then, during the next FWA period, odor pulses were delivered to drive cortical activity or no odor in the control condition. Finally, spontaneous activity was again monitored during the subsequent SWA period for comparison with prestimulation SWA activity. B, Single-unit entrainment to slow waves (LFP slow-wave trace at top) was stable over consecutive SWA episodes in control cells. Graph shows mean spike counts across all control units relative to slow-wave peak. C, However, if repeated odor stimulation occurred during the FWA episode intervening between two SWA periods, then single-unit entrainment to slow waves during the post-odor SWA episode was modified. There was a significant decrease in mean firing rate before odor compared with before odor near the peak of the slow wave (*p < 0.05, odor-exposed different from control). D, This change in mean slow-wave-associated unit activity may be attributable to experience-induced shifts in single-unit entrainment. In this example, the PSWTH shifted from early in the slow-wave pre-odor stimulation to later in the wave post-odor stimulation.

Figure 3.

Top, There was no significant change in mean slow-wave morphology in either control or odor-stimulated animals between pre- and post-odor time points. Bottom, However, variability in the leading edge of the slow wave was significantly enhanced by previous odor stimulation. This variability in slow-wave morphology was associated with a significant shift of peak single-unit activity during the slow wave after odor stimulation compared with single units in controls.