Pier Luigi Parmeggiani

On the Functional Significance of the Hippocampal θ–Rhythm*

Publisher Summary This chapter focuses on the functional significance of the hippocampal θ-rhythm. The appearance of the θ-rhythm in the hippocampogram depends on a moderate level of reticular activation. In this condition the hippocampal output elicits a rhythmic firing of subcortical neurones. Via the anterior thalamic nuclei and the gyrus cinguli a hippocampo-hippocampal circuit is closed, and reactivation of the hippocampus at the same rate is quite possible. This circuit as well as the other thalamo-neocortical circuits of the nuclei lateralis dorsalis and in part medialis dorsalis are not consistently affected by the ascending influences of the activating reticular formation. In conditions of moderate arousal the hippocampal output during the appearance of the θ-rhythm has enough driving power to exert definite control on the bioelectrical activity of subcortical and neocortical structures. It is evident that the preceding considerations cannot be directly extended to higher mammals. The depression or suppression of the hippocampal θ-rhythm does not necessarily mean that the hippocampus has lost or basically changed its functional significance.

Behavioral phenomenology of sleep (somatic and vegetative)

The foregoing analysis of behavioral sleep phenomenology shows that the most significant factual and theoretical aspects of sleep can be logically organized only according to several criteria, it being impossible to choose a singli one as truly paradigmatic. For this reason an ordinal classification of sleep phases was preferred. This fact does not detract from the usefulness of classifications based consistently on 1 criterion at a time (e.g.: synchronized-desynchronized; quiet-active; orthodoxical-paradoxical; NREM-REM; homeostatic-poikilostatic; spindle wave-slow wave-fast wave; external appetitive-internal appetitive-internal consummatory; and so on). In this respect, the bioelectrical classification is surely the best as it allows an analytical subdivision of the evolution of sleep with high resolving power137–139. In particular, the electroencephalographic activity of late phase II (stage 4 in man139 and slow wave11 or deep slow wave140 sleep in the cat) appears to be related to the triggering mechanisms and to the quantitative regulation of the circadian amount of phase III3,5,11,140. However, in extending the field of functional implications of sleep phenomenology other criteria may be more significant. In fact, the somatic and vegetative events of sleep also lend themselves to an analysis according to the behavioral model of ethology6,141–144 and the theory of homeostasis3–5, 145, respectively. As an example, a number of classifying criteria are indicated in the table, where others, particularly neurochemical ones146,147, could be added. At any rate, the difficulty of organizing sleep events into a satisfactory operational scheme is due to the fact that sleep is still an open problem as far as its mechanisms and functional significance are concerned.

Hypothalamic temperature during the sleep cycle at different ambient temperatures

Hypothalamic temperature during complete and incomplete sleep cycles (slow wave sleep followed by fast wave sleep and slow wave sleep followed by arousal, respectively) has been studied in freely moving cats at 20 degrees C and 0 degrees C ambient temperatures. The results show that sleep and thermoregulatory processes interact and, at 0 degrees C ambient temperature, become mutally exclusive. The occurrence of fast wave sleep is related to an opptimum range of hypothalamic temperatures which is specific in each enviromental conditions.

On the functional significance of the circuit of papez

Summary This study was performed with the aim of clarifying the functional properties of the circuit of Papez as a feedback loop regulating hippocampal activity. The circulation in the loop of volleys of impulses elicited by delivering to the hippocampus trains of low-frequency electrical stimuli was studied in the cat by recording unit activity at mammillary, thalamic, cingulate and hippocampal levels. The results show the properties of two feedback loops, one related to the nucleus anterior ventralis and the other to the nucleus anterior medialis. The output of the nucleus anterior ventralis is dependent on the hippocampal output, whereas the output of the nucleus anterior medialis is affected by both hippocampal and extralimbic thalamo-neocortical influences. The intermodulation of septal and feedback volleys at the level of the hippocampal region appears, in physiological conditions, to underlie the regulation of hippocampal bioelectrical activity in general and of theta rhythm in particular. A revelant effect of the output of the anterior thalamic nuclei consists in the depression of unit activity of the gyrus cinguli and area retrosplenialis.

Quantitative analysis of short term deprivation and recovery of desynchronized sleep in cats

A quantitative analysis of desynchronized sleep (DS) deprivation (exposure to low ambient temperature) and recovery was carried out in unrestrained cats. The results show that: (1) the circadian obligate quota of DS is precisely regulated by a control mechanism paying by the 24th h the DS debt induced by up to 14 h of total DS deprivation, if recovery occurs during the rest phase of circadian photoperiodicity (CP); (2) during static rebound DS hourly duration is increased by 40 +/- 4 sec/h of total deprivation (mean and S.E.) and there is a statistically significant increase in the hourly frequency and in the duration of DS episodes, with respect to control values; (3) the hourly obligate and facultative quotas of DS amount to 409 +/- 82 and 229 +/- 140 sec/h (mean and S.D.), respectively. (4) preoptic heating during deprivation at low ambient temperature decreases the DS static rebound during recovery at control ambient temperature by an amount corresponding to the cumulative duration of DS episodes elicited by the preoptic treatment; (5) preoptic temperature decreases the more markedly the shorter the duration of exposure to low ambient temperature and regains control values the sooner the smaller the DS debt incurred during deprivation; (6) DS debt cumulation is a continuous process which develops at a steady rate during day and night, whereas DS debt payment is a discontinuous process (ultradian rhythm of DS) which develops at a variable rate depending on the DS debt and on the phase of CP.

Thermosensitivity of anterior hypothalamic-preoptic neurons during the waking-sleeping cycle: a study in brain functional states

The thermosensitivity of anterior hypothalamic-preoptic neurons was studied in cats during the waking-sleeping cycle. Direct cooling and warming of the anterior hypothalamic-preoptic region was accomplished with water-perfused thermodes. Neuronal thermosensitivity was determined by means of the linear regression analysis of firing rate changes vs anterior hypothalamic-preoptic temperature changes. A total of 117 neurons were classified as thermosensitive during wakefulness and synchronized sleep (20.1% of the studied neurons). Cold-sensitive neurons outnumbered warm-sensitive neurons by 3.7:1. The homeothermic states, wakefulness and synchronized sleep, are characterized by similar frequency distributions of neuronal thermosensitivity, although variable changes in single neuron thermosensitivity are state-dependent. Such changes underlie the quantitative differences in homeothermic regulation between these states. The impairment of thermoregulation during desynchronized sleep is characterized by a different frequency distribution of neuronal thermosensitivity resulting from both a drop in the responsiveness to thermal stimulation of a majority of neurons and a reversal in the sensitivity to cooling and warming of a minority of neurons. In conclusion, only the frequency distribution of thermosensitivity in the neuronal population is indicative of changes in the thermoregulation paradigm across behavioral states.

Absence of thermoregulatory vasomotor responses during fast wave sleep in cats.

The skin temperature of the pinna was recorded in unrestrained cats sleeping at different ambient temperatures. The results show that during fast wave sleep vasomotion is inconsistent with homeothermic regulation as ear skin temperature increases and decreases at low and high ambient temperatures, respectively. The effects of preoptic heating during slow wave and fast wave sleep reveal that a depression of the responsiveness of hypothalamic thermoceptive structures underlies the absence of thermoregulatory vasomotor responses during fast wave sleep.

Transfer of the hippocampal output by the anterior thalamic nuclei

Abstract This study was performed in the cat with the aim of clarifying the transfer properties of the thalamic nuclei anterior ventralis and anterior medialis with respect to volleys of impulses elicited by delivering trains of electrical stimuli of different frequency and intensity to the contralateral hippocampus. The results show that the responses of the nucleus anterior ventralis are only intensity-dependent whereas those of the nucleus anterior medialis depend on both stimulus intensity and frequency. The nucleus anterior ventralis performs an operation of input-output transfer within one of the loops of the Papez circuit. The nucleus anterior medialis is under the influence of both the hippocampus and a thalamoneocortical feedback activated by the output of the nucleus itself. This nucleus, therefore, operates as a gate controlling the integration of archicortical and neocortical activities.

Threshold of respiratory responses to preoptic heating during sleep in freely moving cats.

Abstract The respiratory effects of unilateral preoptic heating were studied during sleep in freely moving cats. Hypothalamic temperature was recorded by means of a thermistor placed about 5 mm posteriorly to the caudal electrode of the heating pair. Environmental temperature was kept at about 24–28 °C to maintain panting threshold low. Preoptic heating, increasing the hypothalamic temperature by 0.047 ± 0.001 °C, elicited thermal polypnoea or panting during slow-wave sleep, whereas during fast-wave sleep it raised hypothalamic temperature by 0.050 ± 0.003 °C above the value of treated slow-wave sleep but did not result in thermal polypnoea or panting. Only stronger heating, applied to the preoptic region until the hypothalamic temperature increase averaged 0.131 ± 0.009 °C above the value of treated slow-wave sleep, elecited thermal polypnoea during fast-wave sleep. The results show that the threshold of respiratory responses to preoptic heating is consistently increased during fast-wave sleep. The implications of this conclusion are discussed in terms of the homeostatic function of the hypothalamus.

Telencephalo-diencephalic aspects of sleep mechanisms

Summary This review is concerned with the functional significance of forebrain structures in sleep. Their fundamental role in its genesis is stressed by presenting sleep phenomenology as a dynamic sequence of interrelated functional events that results from the integrative action of the whole nervous system.