Research reportOscillatory fast wave activity in the rat pyriform cortex: relations to olfaction and behavior
Introduction
The pyriform cortex of several mammalian species, waking or anesthetized, generates high amplitude, nearly sinusoidal `fast' wave field potentials primarily within the frequency bands of 15–35 and 35–85 Hz 1, 3, 4, 10, 11, 12, 13, 14, 15, 16. It has been proposed that these fast waves are not exclusively related to pyriform cortex mechanisms involved in olfaction but, rather, can be elicited by a wide array of sensory stimuli and are related to general arousal levels or motivation. 1, 3, 4, 10, 11, 12, 13, 14, 15, 16, 27. Further, it has also been suggested that pyriform cortex fast waves are correlated with motor activity 10, 11, 12, 13, 14, 15, 16.
However, a specific relation between fast waves and olfaction has been shown to exist in other areas of odor-sensitive cortex in the brain. In particular, 15–30 Hz field oscillations have been detected in the dentate gyrus of the rat in response to the odors of several organic solvents (xylene, toluene, diethyl ether, and methyl methacrylate) and synthetic predator odors of the red fox (trimethyl thiazoline) and weasel (2-propylthietane) 17, 18, 35. Other strong odors such as butyric acid, caproic acid, cadaverine, indole, putrescine, and irritants like ammonia are ineffective in generating dentate fast wave activity. Auditory, visual, somatosensory, and gustatory stimuli are also ineffective. Further, dentate fast waves bear no relation to concurrent motor activity. These observations suggest that dentate fast waves may play a role in olfactory mechanisms that have evolved for the recognition and detection of predators. Organic solvents, not ordinarily present in high concentrations in the natural world, may mimic the effect of predator odors.
The specific relation of dentate fast waves to olfaction raises the question of whether the pyriform fast wave is, as well, specifically olfactory or is related to arousal or other behavioral factors as previously suggested. It is conceivable that pyriform fast waves are related to behavior in much the same way as hippocampal rhythmical slow activity (RSA) is related to behavior. Hippocampal RSA in rats is prominent during locomotion, spontaneous head movements or posture changes, and during manipulation of objects (Type 1 behavior) but is ordinarily absent during alert immobility and other more reflexive or automatic behaviors such as chewing, licking, face washing, and shivering (Type 2 behavior) 32, 34. The correlation of RSA with behavior is unrelated to respiration and persists under conditions of apnea (e.g. underwater swimming; [36]). The cingulate cortex also displays rhythmical electrical activity similar to that observed in the hippocampus and this activity is also correlated with Type 1 behavior 2, 24. It is not known whether pyriform cortex activity is also correlated with Type 1 behavior in normal, freely moving rats.
Hippocampal RSA is correlated with the occurrence of Type 1 behavior regardless of whether central muscarinic blockade is present or not. The relation of spontaneous neocortical slow wave activity to behavior is not closely related to Type 1 and 2 behaviors in undrugged rats but exhibits a clear correlation with concurrent behavior after central muscarinic blockade, displaying activation during Type 1 behavior and deactivation during Type 2 behavior [34]. Further, the amplitude and duration of neocortical transcallosal evoked potentials are also correlated with the occurrence of Type 1 behavior 9, 23, 30, 33.
These findings raise the question of whether the correlations between slow wave activity and behavior are similar in all three major divisions of cerebral cortex, the paleocortex (pyriform lobe), archicortex (hippocampal formation and the related transitional cortex of the cingulate gyrus), and neocortex. The relation between pyriform activity and Type 1 behavior has not been previously examined in rats given an antimuscarinic drug.
The aim of the present study is to examine the relation of oscillatory electrical activity in the rat pyriform cortex to olfaction and behavior.
Section snippets
Animals
Experiments were conducted on a group of 30 male, Long Evans rats weighing between 328 and 605 g at experimental onset. The rats were housed individually in wire cages (on a 12:12 h light/dark cycle) and were given free access to Agway rat chow and bottled water. The housing environment was maintained at 20°C. All testing was conducted during the light phase.
Surgery
The rats were anesthetized with sodium pentobarbital (50 mg/kg, i.p.), placed in a stereotaxic device, and bilateral, bipolar electrodes
Histology
Olfactory mucosa electrodes were located in the labyrinth of the ethmoid bone in eight rats. Nasal thermistors were similarly located in the nasal passages of two rats. The deep olfactory bulb electrode sites were located in three implantations in two of the six rats with such electrodes. In all three cases, the electrodes were found in or between the internal granule and the external plexiform layer. In a random sample of fourteen rats, 15 pyriform cortex bipolar electrode pairs were located.
Discussion
The results show that the presentation of a number of odors elicited rhythmical, oscillatory fast activity of about 20 Hz in the olfactory bulb and pyriform cortex of rats. Several observations indicated that these fast waves were exclusively related to olfaction. (i) A wide variety of auditory, visual, gustatory, and somatosensory stimuli failed to generate significant 15–50 Hz activity in the olfactory bulb and pyriform cortex even though they often elicited vigorous behavioral responses
Acknowledgements
We thank Sharon N.D.A. Clarke for her assistance in implanting the intraoral cannulas; Richard Cooley for general technical assistance; L.-W. Stan Leung for help with the Fast Fourier Transform Analysis; and Colin Springett, zookeeper at Storybook Gardens, London, Ont., for the donations of the natural animal faecal samples. This work was supported by an operating grant to C.H.V. and by a student grant to E.M.Z. from the Natural Sciences and Engineering Research Council of Canada.
References (36)
- et al.
Electrical activity of the cingulate cortex. II Cholinergic modulation
Brain Res.
(1987) - et al.
Construction of wire leads and electrodes for use in slow wave recording in small animals
Brain Res. Bull.
(1978) - et al.
Double and triple labelling of neurons with fluorescent substances: the study of collateral pathways in the ascending raphe system
Neurosci. Lett.
(1980) - et al.
Transcallosal evoked potentials: behavior-dependent modulation by muscarinic and serotonergic receptors
Brain Res. Bull.
(1994) Changes in prepyriform evoked potential with food deprivation and consumption
Exp. Neurol.
(1962)The electrical activity of a primary sensory cortex: analysis of EEG waves
Int. Rev. Neurobiol.
(1963)- et al.
Components of weasel and fox odors elicit fast-wave bursts in the dentate gyrus of rats
Behav. Brain Res.
(1994) - et al.
Scopolamine blocks olfaction-induced fast-waves but not olfactory-evoked potentials in the dentate gyrus
Behav. Brain Res.
(1995) - et al.
The importance of lipid-solubility for the central action of cholinolytic drugs
Int. J. Neuropharmacol.
(1965) - et al.
Identification of serotonin and non-serotonin-containing neurons of the midbrain raphe projecting to the entorhinal area and the hippocampal formation. A combined immunohistochemical and fluorescent retrograde tracing study in the rat brain
Neuroscience
(1982)