Elsevier

Neuroscience

Volume 86, Issue 4, 18 June 1998, Pages 1307-1319
Neuroscience

Beta-frequency (15–35 Hz) electroencephalogram activities elicited by toluene and electrical stimulation in the behaving rat

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Abstract

Bursts of beta-frequency (15–35 Hz) electroencephalogram activity occur in the olfactory system during odour sampling, but their mode of propagation within the olfactory system and potential contribution to the mechanisms of learning and memory are unclear. We have elicited large-amplitude beta activity in the rat olfactory system by applying noxious olfactory stimuli (toluene), and have monitored the bursts via chronically-implanted electrodes. Following exposure to toluene, coherent bursts with a peak frequency of 19.8±0.9 Hz were observed in the olfactory bulb, piriform cortex, entorhinal cortex and dentate gyrus. The timing of the bursts and the phases of electroencephalogram cross-spectra indicate that beta bursts propagate in a caudal direction from the olfactory bulb to the entorhinal cortex. The time delays between peaks of bursts in these structures were similar to latency differences for field potentials evoked by olfactory bulb or piriform cortex test-pulses. Peaks of burst cycles in the dentate region, however, were observed just prior to those in the entorhinal cortex. Surprisingly, power in toluene-induced beta-frequency oscillations was not increased following long-term potentiation induced by tetanic stimulation of the olfactory bulb, piriform cortex and entorhinal cortex. The activity of local inhibitory mechanisms may therefore counteract the effects of synaptic enhancements in afferent pathways during beta bursts. Low-frequency electrical stimulation of the piriform cortex was most effective in inducing coherent oscillatory responses in the entorhinal cortex and dentate gyrus at stimulation frequencies between 12 and 16 Hz.

The results show that repetitive polysynaptic volleys at frequencies in the beta band induced by either toluene or electrical stimulation are transmitted readily within the olfactory system. The propagation of neural activity within this frequency range may therefore contribute to the transmission of olfactory signals to the hippocampal formation, particularly for those odours which induce high-amplitude bursts of beta activity.

Section snippets

Surgery

Male Long–Evans hooded rats (320–460 g) from the McMaster University breeding colonies were anaesthetized with 0.9 mg/kg ketamine and 0.05 mg/kg xylazine and were placed in a stereotaxic frame with the skull surface on the horizontal plane. The level of anaesthesia was monitored closely, and 10 to 20% supplemental doses were administered as required. Bipolar, Teflon-coated stainless-steel twisted-wire electrodes (125 μm exposed tips) were implanted in the right piriform cortex (posterior 3.6 mm,

Spontaneous electroencephalogram activity and toluene-induced beta activity

Spontaneous EEG recordings included beta-, gamma- and theta-frequency activities, which varied in power across the four recording sites. Fig. 1 shows the major aspects of spontaneous and toluene-induced EEG activity in both time- and frequency-domains in one of the five animals. Spontaneous beta and gamma activities were observed most strongly in the olfactory bulb and piriform cortex, and were weakly represented in the entorhinal cortex and dentate gyrus. Gamma activity had a mean frequency of

Discussion

Bursts of toluene-induced beta-frequency EEG activity in the olfactory system and hippocampal formation have been found here to be characterized by high-amplitude coherent oscillations that spread in a caudal direction from the olfactory bulb to the entorhinal cortex and dentate gyrus. Electrical stimulation was also applied to the piriform cortex at frequencies between 2 and 35 Hz, and optimal field responses in both the entorhinal cortex and dentate gyrus were found for frequencies of

Conclusions

Noxious odours such as toluene induce high-amplitude bursts of beta-frequency EEG activity which are transmitted from the olfactory bulb to the hippocampal formation via the piriform and entorhinal cortices, and which are highly coherent between these structures. Partial coherence analysis indicates that the spectral characteristics of the bursts are not significantly altered during transmission between the piriform cortex and the hippocampus. Although bursts induced by toluene were increased

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Acknowledgements

This research was supported by grants from the Natural Sciences and Engineering Research Council to R.J.R. and S.H., and by an NSERC post-graduate scholarship to C.A.C.

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