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, 124 (4), 490-9

Olfactory Bulb Habituation to Odor Stimuli

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Olfactory Bulb Habituation to Odor Stimuli

Dipesh Chaudhury et al. Behav Neurosci.

Abstract

Habituation is a simple form of memory, yet its neurobiological mechanisms are only beginning to be understood in mammals. In the olfactory system, the neural correlates of habituation at a fast experimental timescale involving very short intertrial intervals (tens of seconds) have been shown to depend on synaptic adaptation in olfactory cortex. In contrast, behavioral habituation to odorants on a longer timescale with intertrial intervals of several minutes depends on processes in the olfactory bulb, as demonstrated by pharmacological studies. We here show that behavioral habituation to odorants on this longer timescale has a neuronal activity correlate in the olfactory bulb. Spiking responses of mitral cells in the rat olfactory bulb adapt to, and recover from, repeated odorant stimulation with 5-min intertrial intervals with a time course similar to that of behavioral habituation. Moreover, both the behavioral and neuronal effects of odor habituation require functioning N-methyl-d-aspartic acid receptors in the olfactory bulb.

Figures

Figure 1
Figure 1
Schematic depiction of electrophysiological (A) and behavioral (B) experimental protocols. A. Electrophysiological protocol. During electrophysiological recordings, odor responses were first measured (Pre) by presenting a 2-second odor stimulus five times with 120 sec interstimulus intervals (response testing protocol). The adaptation protocol, consisting of four fifty-second presentations of the same odorant separated by five-minute intertrial intervals, was then administered. In separate experiments, stimulus duration and ITIs were varied independently of each other. Five and sixty minutes after the end of the last adaptation trial (Post), the response testing protocol was again delivered. Bi. Behavioral protocol. Rats were presented with a weighing dish containing either mineral oil (MO) or the habituation/test odorant. Bii. After a single presentation of mineral oil alone, the habituation/test odorant was presented for four consecutive trials, separated by five minute intertrial intervals, and then twice more at 30 and 60 minutes’ latency following the last habituation trial.
Figure 2
Figure 2. Individual mitral cell responses to one odor over the course of the recording protocol
Raw recorded data from one mitral cell are shown during pre-tests (five 2-second odor presentations separated by 2-minute ITIs), followed by four 50-second adaptation stimuli with the same odorants separated by 5-minute ITIs (adaptation), followed 5 minutes later by a second series of five 2-second odor stimuli separated by 2-minute ITIs. Gray bars indicate odor stimulation times and durations.
Figure 3
Figure 3
Neural adaptation to repeated odor presentations. A. Average number of spikes evoked by odor presentations during pre- and post- adaptation testing expressed as percentages of the response during pre- adaptation testing. Mitral cells stimulated with the adaptation odorant (Odor adaptation, solid line) over four trials during the adaptation protocol responded significantly less during both 5- but 60-minute post- test than during the pre- adaptation tests. Asterisks indicate a significant decrease as compared to pre-testing. In contrast, mitral cells stimulated with plain mineral oil (Mineral oil adaptation, dashed line) during the adaptation protocol did not change their responses significantly compared to pre- adaptation test responses. B. Post-test responses to odorants expressed as the percentage of the pre-test responses in cells stimulated with 5 repeated stimulations of 2, 10, 20, 30 and 50 second durations and 5 minute ITIs. C. Post-test responses to odorants expressed as the percentage of pre-test responses in cells in cells stimulated with 5 repeated stimulations of 50 seconds separated by 1, 2.5 and 5 minute ITIs. D. Post test responses to test odorants differing by 1, 2, 3 or 4 carbons from the odorant used as the adaptation odorant expressed as percentage of the pre-test response to this odorant. Asterisks indicate a significant reduction in response magnitude as compared to pre-adaption.
Figure 4
Figure 4
Effect of bulbar NMDA receptor blockade on neural adaptation. A. Average responses of mitral cells during pre-adaptation and post-adaptation odor tests in rats infused with MK-801, expressed as percentages of the average pre-adaptation test response. In these rats, responses to odorants post-habituation were not significantly different from those recorded pre-adaptation. B. Percentages of cells responding significantly to odor presentations in pre- adaptation and post- adaptation tests under control and MK-801 conditions. Asterisks indicate a significant decrease in response magnitude as compared to the first trial or pre- adaptation response (p < 0.05).
Figure 5
Figure 5. Average responses of mitral cells during the adaptation protocol in control and MK-801 rats
Ai and Bi. Spontaneous activity, recorded for 4 seconds before each odor presentation, did not change significantly over the course of a recording protocol (Ai: control rats, Bi: MK-801 infused rats). Aii and Bii. Average number of evoked spikes per second during pre-test, adaptation trials and posttests. In control rats, the average number of odor evoked spikes per second significantly decreased after the first two adaptation trials (Aii), whereas in MK-801 infused rats no significant decrease was observed (Bii). Asterisk indicates a significant difference to the first adaptation trial. Aiii and Biii. Time course of mitral cell responses during adaptation trials. The graphs show the average number of odor-evoked spikes normalized by the number evoked during pre-tests recorded in 10-second intervals. No significant change over the course of a 50-second odor presentation was observed in either group of animals, except for the first adaptation trial in control rats.
Figure 6
Figure 6. Behavioral results
A. Average behavioral investigation times in saline and MK801 infused rats over the course of the behavioral experiment. Saline-injected control rats responded significantly less on the fourth habituation trial as compared to the first trial (* indicates a significant difference between responses during the first and fourth trial), whereas MK-801 infused rats did not significantly habituate, as indicated by a non-significant difference between investigation times during the fourth and first trials. B. Blockade of bulbar NMDA receptors does not impair odor detection. The graph shows the average investigation times of saline-infused and MK-801 infused rats presented with the mineral oil carrier during four trials followed by a single odor presentation. All rats responded significantly more to the odor than to the carrier alone, indicating that they detected the odorant.

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