P. Langhorst

Reticular formation of the lower brainstem. A common system for cardiorespiratory and somatomotor functions: discharge patterns of neighboring neurons influenced by cardiovascular and respiratory afferents☆

Experiments were done in dogs with chloralose-urethane anesthesia. Long-lasting extracellular recordings were made from the medial parts of the reticular formation of the lower brainstem for up to 250 min. The study is based on reactions of 103 neurons. The activities of 2 or 3 neighbouring neurons recorded under identical conditions with one electrode or of neurons recorded with two electrodes at the same time could be changed regularly and synchronously by experimental changes of hemodynamic or ventilatory parameters. Action potentials were separated by amplitude discrimination. Rhythmic pulsatile modulations were proved to be present in 78% of all neurons by post-event-time histograms triggered by the R-wave of the ECG. In the 96 neurons tested 86% changed their activity when arterial pressure was raised by inflating a balloon in the abdominal aorta (79% decreased and 7% increased their activity). In post-event-time histograms triggered by the start of inspiration, 83% of the neurons showed modulations of their activity with respiratory rhythm. Experimental lung inflation decreased the activity in 75% of the tested neurons, while experimental lung deflation activated 47% of the tested neurons. Stimulation of arterial chemoreceptors activated 77% of the tested neurons. It was thus demonstrated that receptors in the cardiovascular and respiratory systems exert an influence on nearly all neurons from which recordings were made in that part of the reticular formation. Arterial baroreceptors and lung stretch receptors revealed a generalized depressing effect on the neuronal activity while chemoreceptors exert a generalized augmenting effect. At different times of recording these neurons did not always react to the same extent to comparable stimulations of afferents.

Phase transitions in the common brainstem and related systems investigated by nonstationary time series analysis.

Neuronal activities of the reticular formation (RF) of the lower brainstem and the nucleus tractus solitarii (NTS, first relay station of baroreceptor afferents) were recorded together in the anesthized dog with related parameters of EEG, respiration and cardiovascular system. The RF neurons are part of the common brainstem system (CBS) which participates in regulation and coordination of cardiovascular, respiratory, somatomotor systems, and vigilance. Multiple time series of these physiological subsystems yield useful information about internal dynamic coordination of the organism. Essential problems are nonlinearity and instationarity of the signals, due to the dynamic complexity of the systems. Several time-resolving methods are presented to describe nonlinear dynamic couplings in the time course, particularly during phase transitions. The methods are applied to the recorded signals representing the complex couplings of the physiological subsystems. Phase transitions in these systems are detected by recurrence plots of the instationary signals. The pointwise transinformation and the pointwise conditional coupling divergence are measures of the mutual interaction of the subsystems in the state space. If the signals show marked rhythms, instantaneous frequencies and their shiftings are demonstrated by time frequency distributions, and instantaneous phase differences show couplings of oscillating subsystems. Transient signal components are reconstructed by wavelet packet time selective transient reconstruction. These methods are useful means for analyzing coupling characteristics of the complex physiological system, and detailed analyses of internal dynamic coordination of subsystems become possible. During phase transitions of the functional organization (a) the rhythms of the central neuronal activities and the peripheral systems are altered, (b) changes in the coupling between CBS neurons and cardiovascular signals, respiration and the EEG, and (c) between NTS neurons (influenced by baroreceptor afferents) and CBS neurons occur, and (d) the processing of baroreceptor input at the NTS neurons changes. The results of this complex analysis, which could not be done formerly in this manner, confirm and complete former investigations on the dynamic organization of the CBS with its changing relations to peripheral and other central nervous subsystems.

Postganglionic sympathetic activity with correlation to heart rhythm and central cortical rhythms.

Summary1.Renal sympathetic nerve activity, ECG and parieto-occipital EEG were recorded in dogs anaesthetized with chloralose. The carotid sinus nerves were cut. Autocovariance functions and power spectra for these variables were computed.2.During cooling of the vagus nerves, the integrated renal sympathetic activity exhibited rhythms which were correlated to the delta-theta rhythm of the EEG. This rhythm was also present with the vagus nerves functionally intact, but a cardiac rhythm was dominant.3.Blood pressure-dependent neurones in the lower brain stem reticular formation have both cardiac and central cortical rhythms. This provides a hint that these neurones might be involved in the sympathetic tone generating network.

Neuronal activity with cardiac rhythm in the nucleus of the solitary tract in cats and dogs. I. Different discharge patterns related to the cardiac cycle

In anaesthetized, spontaneously breathing cats and dogs, extracellular recordings were made of the spontaneous activities of 28 single neurones with cardiac rhythm. It was confirmed by histological examination that the neurones were situated in the mediodorsal portion of the nucleus of the solitary tract. Different discharge patterns in relation to the heart cycle were demonstrated using R-deflection triggered histograms. Most of the neurones discharged with systolic bursts. In the cat, about half the neurones showed two to three activity peaks in the histograms which could occur at any time of the heart cycle. The height of the various peaks sometimes changed in different ways in the course of the respiratory cycle. It can be concluded that different cardiovascular afferents converge to single neurones. In some neurones it could be shown by elimination of the vagus nerves that the pulse-rhythmical discharge pattern was induced mainly by vagal inputs, mainly by glossopharyngeal inputs or by inputs from both nerves. Two-thirds of the neurones discharging with systolic bursts could be enhanced by increasing the arterial blood pressure. In some of these neurones a proportionality between the number of impulses per heart cycle and the mean arterial blood pressure was found.

Reticular formation of the lower brainstem. A common system for cardiorespiratory and somatomotor functions: Discharge patterns of neighboring neurons influenced by somatosensory afferents☆

Extracellular recordings were made from 103 neurons located in the medial parts of the reticular formation of the lower brainstem of chloralose-urethane anesthetized dogs. Activities of 2 or 3 neighbouring neurons under identical conditions could be recorded with one electrode. In 9 recordings it was possible to register simultaneously up to 5 neurons with two electrodes placed in both halves of the medulla. Action potentials of individual neighbouring neurons were identified by amplitude discrimination. The influences of somatosensory afferents from skin, joints and muscles on neuronal discharge patterns were tested. Responses of single neurons were characterized by multisensory afferent spectra including afferents from various parts of the body. The combinations of afferents converging onto neighbouring neurons were similar, whereas neurons in more distant parts of the medulla revealed different combinations of converging afferents. In long-lasting recordings the influence of somatosensory afferents on the discharge behaviour changed from time to time. When the discharge behaviour was mainly determined by somatosensory afferents, neighbouring neurons were shown to be organized in sub-populations. The results led to the conclusion that in this part of the reticular formation different types of functional organization of the neuronal network are possible. The type of functional organization depends on the actual preponderances of different inputs to the neurons.

Dynamic Characteristics of the “Unspecific Brain Stem System”

The reticular formation of the lower brain stem is a morphological substrate for different functional systems.

Reticular formation of the lower brainstem. A common system for cardio-respiratory and somatomotor functions. Cross-correlation analysis of discharge patterns of neighbouring neurones

Temporal relations of discharges of 73 pairs of neurones located in the medial parts of the reticular formation of the lower brainstem were studied by cross correlation analyses in chloralose-urethane anaesthetized dogs. The action potentials of 2 or 3 neighbouring neurones were recorded with one electrode simultaneously. Uncorrelated discharges of neurones and 4 different types of correlated discharges were observed in cross correlation histograms: they were: (1) rhythmic couplings with frequencies between 2 and 5 Hz related to the same rhythm in the EEG; (2) strong, non-rhythmic couplings with short latencies up to 5 ms; (3) a combination of strong and rhythmic couplings, and (4) high-frequency oscillation couplings. Most pairs of neurones showed different types of correlation during the recordings. The different forms of correlated discharge behaviour could be related to different types of functional organization of the neuronal network in the reticular formation.

Central control and interactions affecting sympathetic and parasympathetic activity

Current thinking concerning the central control of the autonomic nervous system and the central interactions affecting sympathetic and parasympathetic activity is presented. Among the questions discussed are the following: are there neurons within the common brain stem system which exert an influence on preganglionic parasympathetic neurons and can they be differentiated from neurons which affect sympathetic preganglionic neuron functions? What interactions occur between sympathetic and parasympathetic tone-mediating neurons? In discussing these problems information is presented as obtained by recording from reticular formation (RF) neurons with discharge patterns similar to efferent parasympathetic activity. The general conclusion reached is that there is a common central control; interactions occur in the brain stem as well as peripherally; depending on the functional situation, these two systems can be organized to act either reciprocally or non-reciprocally.

Neuronal activity with cardiac rhythm in the nucleus of the solitary tract in cats and dogs. II. Activity modulation in relation to the respiratory cycle

In anaesthetized, spontaneously breathing cats and dogs extracellular recordings were made of the spontaneous activities of 28 single neurones with cardiac rhythm. Histological exmaination confirmed that the neurones were situated in the mediodorsal portion of the nucleus of the solitary tract. The neurones, which had already been analysed in respect to their pulse-rhythmical pattern27, were investigated by means of inspiration triggered histograms. The neurones could be grouped according to the respiratory modulations of their activities. Increased activities occurred during (a) the rise of the respiratory blood pressure wave, (b) the respiratory rest period, and (c) the inspiration. Three neurones did not exhibit respiratory modulation. The respiratory modulations of groups a and b were most probably caused by changing inputs from cardiovascular receptors in the course of respiration. It could be shown by adequate stimulation and elimination of the vagus nerves that the neurones of group c were influenced by lung inflation receptors as well as by cardiovascular receptors.

Neuronal activity with relation to cardiac rhythm in the lower brain stem of the dog

Extracellular recordings of reticular neurons in the lower brain stem were performed in anesthetized dogs. Thirty out of 131 neurons showed rhythms of about 2-4 c/sec which were similar to heart or to EEG rhythms. By means of post-event-time histograms, correlations to the EEG delta-theta rhythm could be found in some neurons. These results were published elsewhere. Fixed relations of the neuronal activity to the cardiac rhythm could be verified in 7 neurons. Two neurons showed maxima 70 msec and 120 msec, respectively, after the beginning of the pulse wave. Two neurons showed minima after 110 msec and 130 msec, respectively. Three pulse-rhythmical neurons could not be classified in this way. This rhythmicity was changing or vanishing during the course of registration, but it could be strengthened experimentally by blood-pressure increase. It was shown that these neurons receive inputs from cardiovascular afferents and therefore are blood-pressure dependent neurons. From the finding that pulse-rhythmical modulation is different at different times under the same blood-pressure levels, it is assumed that there are varying strong influences from other systems to these neurons. The fact that these neurons are influenced by cardiovascular afferents does not mean, however, that they are cardiovascular neurons exclusively. It is suggested that blood-pressure reticular neurons may belong to the cardiovascular system as well as to other brain stem systems.