Research reportWhat is the significance of gamma wave activity in the pyriform cortex?
Introduction
Adrian [1], using anesthetized hedgehogs and cats, described the occurrence of nearly sinusoidal rhythmical electrical potentials of 15–50 Hz in the mammalian olfactory bulb and pyriform cortex. These waves could be elicited by drawing air in through the nasal passages by means of a cannula passed rostrally through the severed trachea. A second endotracheal cannula permitted spontaneous respiration. Subsequent work in unanesthetized rabbits [4] revealed one spectral peak in pyriform activity in the 15–35 Hz range (beta waves) and another peak in the 35–85 Hz range (gamma waves). Bursts of waves at the lower of these two frequencies (about 20 Hz) can be elicited reliably in the pyriform cortex and dentate gyrus in rats by the odors of a variety of organic solvents, chemicals derived from the anal scent glands of rat predators, and certain chemicals derived from plants [7], [22], [36], [39], [40]. A variety of other strongly odorous compounds are completely ineffective.
The functional relations of gamma waves occurring in the pyriform cortex have not been entirely resolved. These waves are phase-reversed above and below the pyriform pyramidal cell layer [13] and cortical pyramidal cells fire in phase with them [10] indicating that the waves are probably generated by synchronized synaptic activity in the pyramidal cells of the pyriform cortex. W.J. Freeman, who has been the principal investigator of pyriform gamma waves in unanesthetized animals, at first concluded that “during anticipation the amplitude of prepyriform electrical activity is in general related to the input to the nervous system, whereas during action it is related to the output of the nervous system” ([13, p. 130). In later papers, Freeman concluded that pyriform gamma waves occur “only in animals in a state of expectancy” ([14, p. 574) and that “the major behavioral correlates were between EEG amplitudes (of gamma waves) and the levels of arousal, motivation and attention” [18], p. 152).
Bursts of pyriform gamma waves appear to be initiated by olfactory input to some extent, although there is also evidence, based on the study of phase delays in gamma waves in different structures, that gamma waves can be centrally generated and proceed in a centrifugal direction [6], [23]. Fig. 3, Fig. 6 in Freeman [13] show gamma wave bursts occurring during expiration (respiration was recorded by a pneumograph) in freely moving cats but in later papers these wave bursts are said to occur during inspiration [5], [18].
A pneumograph has certain limitations as a means of recording input to the olfactory system. It has long been recognized that during quiet breathing air currents may pass ventral to the olfactory receptor area so that olfactory stimulation may be minimal or non-existent [11]. An alternative means of recording the olfactory effects of respiration is suggested by the observation that the olfactory mucosa generates a slow negative wave in response to odorants, presumably as a result of depolarization of olfactory receptors [3], [30]. This slow potential is usually correlated with activity in olfactory nerves and its amplitude is proportional to the rate of air flow [26]. Air flow rate is also a major determinant of olfactory thresholds in normal intact humans [27].
In the experiments reported here, the gamma wave activity of the pyriform cortex in the rat was studied in relation to spontaneous behavior and respiration recorded by means of an electrode placed in the olfactory mucosa.
Section snippets
Animals
Experiments were performed in 14 male hooded rats weighing 395–820 g at the time of surgery. The rats were housed individually in wire cages on a 12:12 h light/dark cycle at about 20°C and had free access to Agway rat chow and bottled water throughout most of the experiments. In six cases, however, rats were given access to food for only about 3 h per day for 2–4 days. Water was available at all times to all the rats. All experiments were conducted during the light period.
Surgery
The rats were
Results
Inspection of the histological and electrophysiological observations confirmed a previous finding [13] that the roughly 40–60 Hz waves recorded monopolarly above and below the pyramidal cell layer display an accurate phase reversal (Fig. 1). Consequently, differential bipolar records taken from such sites have approximately twice the amplitude of the monopolar signal while extraneous potentials, present as in-phase signals, are rejected. Therefore, surface-to-depth bipolar records were taken
Discussion
In freely moving rats, gamma wave bursts occurred in the pyriform cortex in close relation to the respiratory potentials of the olfactory mucosa. Gamma waves had a low amplitude during periods of apnea, a slightly higher amplitude during vigorous sniffing, a still higher amplitude during the rhythmical breathing associated with quiet immobility, walking, grooming or eating and a very high amplitude during very deep breaths occurring during sighing or vocalizing. These observations suggest that,
Acknowledgements
This research was supported by a grant from the Natural Sciences and Engineering Research Council of Canada. I thank Francis Boon for technical assistance, Daniella Chirila for typing the manuscript, and L.-W.S. Leung, and E. Zibrowski for helpful comments on an earlier draft of this paper. The methods used were approved by Animal Use Subcommittee of the University of Western Ontario.
References (40)
Spatial organization of EEGs from olfactory bulb and cortex
Electroenceph. Clin. Neurophysiol.
(1984)- et al.
Frequency analysis of olfactory system EEG in cat, rabbit, and rat
Electroenceph. Clin. Neurophysiol.
(1980) - et al.
Beta-frequency (15–35 Hz) electroencephalogram activities elicited by toluene and electrical stimulation in the behaving rat
Neuroscience
(1998) - et al.
Construction of wire leads and electrodes for use in slow wave recording in small animals
Brain Res. Bull.
(1978) - et al.
Correlations between unit firing and EEG in the rat olfactory system
Brain Res.
(1990) - et al.
Spatial EEG patterns, non-linear dynamics and perception: the neo-Sherringtonian view
Brain Res. Rev.
(1985) - et al.
Components of weasel and fox odors elicit fast wave bursts in the dentate gyrus of rats
Behav. Brain Res.
(1994) Olfactory, vomeronasal and trigeminal receptor response to odorants
Hippocampal activity, olfaction, and sniffing: an olfactory input to the dentate gyrus
Brain Res.
(1992)- et al.
Hippocampal RSA (theta) apnea, bradycardia and effects of atropine during underwater swimming in the rat
Electroenceph. Clin. Neurophysiol.
(1977)