Neural sensitivity to odorants in deprived and normal olfactory bulbs

Abstract

Early olfactory deprivation in rodents is accompanied by an homeostatic regulation of the synaptic connectivity in the olfactory bulb (OB). However, its consequences in the neural sensitivity and discrimination have not been elucidated. We compared the odorant sensitivity and discrimination in early sensory deprived and normal OBs in anesthetized rats. We show that the deprived OB exhibits an increased sensitivity to different odorants when compared to the normal OB. Our results indicate that early olfactory stimulation enhances discriminability of the olfactory stimuli. We found that deprived olfactory bulbs adjusts the overall excitatory and inhibitory mitral cells (MCs) responses to odorants but the receptive fields become wider than in the normal olfactory bulbs. Taken together, these results suggest that an early natural sensory stimulation sharpens the receptor fields resulting in a larger discrimination capability. These results are consistent with previous evidence that a varied experience with odorants modulates the OB's synaptic connections and increases MCs selectivity.

Figure 1. Trial and odorant stimulation protocol.

Each trial ( s) starts with seconds of clean air named prestimulus (PRE) epoch, followed by the odorant stimulation epoch (STIM) starting at seconds. Four different stimuli were applied in sequence and this sequence was repeated times: clean air or control, r-carvone, isoamylacetate and hexanal. The interstimulus time was s.

Figure 2. Example of signal recording and single-unit sorting in the normal OB.

A: the top traces correspond to the filtered signal ( Hz) from electrodes (channel ). The black arrows indicate the spikes corresponding to the neuron in channel and neuron in channel . B: scatter plot of waveform peak-to-peak amplitudes recorded in channel vs. channel . Two clusters clearly emerge, corresponding to the single-unit activity shown in A. C: An example of the spike waveforms of the clusters shown in B.

Figure 3. Percentage of responses estimated by the probability method as a function of the P_r in the absence of odorant stimulation.

The percentage of detected responses, calculated for all MCs including all the trials with clean air, decreased significantly as the value is increased. This criteria was used to decide which value of the probability was selected for a desired maximum of false positive. We choose a maximum of false positive (see dash line) corresponding to a value .

Figure 4. Examples of three different types of MCs responses to odorant stimulation.

The left panels show the spike rasters for three different cells during odorant stimulation. The right panels show the firing rate histograms calculated in ms bins for the same cells. The continuous line represents the mean firing rate during the baseline epoch. The MC on the top shows an excitatory response, the middle MC shows an inhibitory response and the bottom cell does not respond to odorants.

Figure 5. Mean firing rate of MCs in the normal and deprived OB during the baseline epoch.

Mean firing rates were not significantly different in normal and deprived OBs ( and , respectively, K-S test). We show cumulative distribution function of spikes in the normal and deprived OB for visual comparison. The variance (or SD) appears to be smaller in deprived OBs and we perform a K-S test for differences of the SD giving a .

Figure 6. Examples of MC's odorant responses estimated with the probability method for the same cells shown in Fig. 4.

The graphs represent the response probability in a ms moving window in steps of ms in a single trial. The response probability is shown in a logarithmic scale. The detection criteria () is indicated by the continuous line.

Figure 7. MCs responses to odorants in normal and deprived OBs.

We used the lower bound estimation of probability response when . The left panels show the distribution of odorant responses (filled rectangles) for MCs. The numbers , or of the odorants correspond to r-carvone, isoamylacetate and hexanal respectively. The right panel shows the sensitivity of odorants for the normal and deprived OBs.

Figure 8. Mean firing rate ratio between stimulus and baseline epochs for the cells that exhibited an excitatory or inhibitory responses in normal and deprived OB.

Ratios for excitatory ( and ) and inhibitory ( and ) were not significantly different between normal and deprived OB ( and respectively, K-S test). We show for visual comparison, cumulative distribution function of spikes for the cells that exhibited an excitatory (Exc) or inhibitory (Inh) responses in the normal and deprived OB.

Figure 9. Mean firing rate ratio between stimulus and baseline epochs for the unresponsive cells in normal and deprived OB. Ratios for normal OB (1.01±0.16) and deprived OB (1.04±0.27) were not significantly different (P = 0.99, K-S test).

We show cumulative distribution function of spikes in the normal and deprived OB for visual comparison.

Figure 10. Theoretical estimation of odorant capacity vs. discriminability.

The left panels show the probability of overlap calculated for the deprived and normal OBs that exhibits and of responses, respectively. The right panels present the potential storage capacity and the mean overlap probability as a function of the percentage of activated neurons.