The utility of monitoring oscillations in the heart rate pattern as a window to the brain is discussed as an index of general central nervous system status. Quantification of the amplitude of respiratory sinus arrhythmia provides an accurate index of cardiac vagal tone. A number of studies have demonstrated the validity of this measure; the relationship between flight performance and vagal tone has also been studied. In general, the vagal tone index appears to monitor global states of the central nervous system and may be useful in screening the general state of pilots

Porges, Stephen W.

English

NASA Technical Reports Server

N88-23373
VAGAL TONE AS AN INDEX OF MENTAL STATE
Stephen W. Porges
University of Maryland
College Park, Maryland
-z3
1'
Overview.
Since autonomic processes such as heart rate are neurally mediated,
it has been proposed that monitoring these variables will provide
sensitive indicators of central nervous system status. Thus, many
researchers have proposed that the neurally mediated oscillations in the
heart rate pattern reflect a variety of mental states, including stress,
emotion, consciousness or alertness, and attention. This paper
will focus on the utility of monitoring oscillations in the heart rate
pattern as a "window to the brain" and an index of general central nervous
system status.
Heart rate in a healthy alert adult is not steady. The pattern of
heart rate reflects the continuous feedback between the central nervous
system and the peripheral autonomic receptors. The feedback produces
phasic increases and decreases in neural efferent output via the vagus to
the heart (ref. I). In most situations like other measures of homeostatic
function, the greater the range of the phasic increases and decreases, the
"healthier" the individual. For example, with the aging process or with
severe stress, there is an attenuation of the range of homeostatic
function. Paralleling this process is a reduction in heart rate
variability (ref. 2).
Thus, the efficiency of neural control may be manifested in rhythmic
_||UAVA_UQ_ _AA_physiological variability and may portray the status of th_ _
the individual's capacity and range to behave. In other terms, the
greater the "organized" rhythmic physiological variability, the greater
the range of behavior. Individuals with attenuated physiological
variability, would then exhibit a lack of behavioral flexibility in
response to environmental demands.
Although average heart rate seems to be a relative accurate index of
metabolic activity, the topography of the heart rate pattern provides
additional information regarding the continuous neural feedback between
the cardiovascular system and the higher central nervous system
structures. The spectral decomposition of the heart rate pattern
identifies reliable oscillations at the respiratory frequency, at
approximately .1Hz hypothesized to reflect blood pressure feedback (e.g.,
Traube-Hering-Mayer wave,ref. 3), and at slower frequencies presumed to
reflect thermoregulatory processes.
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57
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Heart rate variability is a complex and often ambiguous construct.
It has numerous mediators. The same level of heart rate variability can
be mediated by a variety of combinations of neural and extra-neural
influences. Therefore, our research has focused on respiratory sinus
arrhythmia, the one oscillation in the heart rate pattern for which the
physiological mechanisms are known.
It is possible to provide empirical evidence that the amplitude of
respiratory sinus arrhythmia accurately maps into the efferent influence
of the vagus nerve on the heart. It has been proposed that respiration,
either by a central mechanism or via a peripheral feedback loop to
medullary areas, phasically inhibits, or "gates" the source nuclei of the
vagal cardio-inhibitory fibers (ref. 3). Maximal inhibition of vagal
efferent output occurs during the mid to late inspiratory phase and
maximal vagal efferent output occurs during the expiratory phase.
Recent research on neural pathways of vagal cardio-inhibltory neurons
has demonstrated that the vagal cardio-lnhibltory neurons show a
resplratory-related pattern of discharge with the primary efferent action
on the heart occurring during expiration (ref. 4). Data from
electrophysiological studies have been so consistent that functional
properties including bradycardia to neural stimulation, pulse rhythm, and
firing primarily during expiration have been used to determine when a
neuron is a vagal cardio-inhibitory neuron (ref. 5).
Given the above characteristics of vagal cardio-inhibitory neurons, a
strong argument may be made that quantification of the amplitude of
respiratory sinus arrhythmia provides an accurate index of cardiac vagal
tone. Since the vagal cardio-inhibitory neurons, by definition, slow the
heart rate and exhibit a respiratory frequency, the impact on heart rate
should be slowing during the expiratory phase of respiration. The greater
the vagal efferent output to the heart, the greater the slowing of heart
rate during expiration. Thus, respiratory sinus arrhythmia is a
peripheral manifestation of the influence of the vagal cardio-inhibitory
neurons on the heart (i.e., cardiac vagal tone).
Physiological model.
Vagal tone is quantified by measuring the spontaneous rhythmic heart
rate changes associated with respiratory activity. Functionally, the
sensory information is transmitted to the respiratory control area of the
medulla from the stretch receptors in the lungs - monitoring inhalation
and exhalation - as well as information from the chemoreceptors in the
cardiovascular system reflecting blood gas composition levels of oxygen
and carbon dioxide. This information "tunes" the medullary respiratory
drive frequency.
The respiratory center influences the output of the vagus as it
conveys neural information to the heart. The vagal efferents are
modulated by the respiratory center, producing an attenuation of vagal
efferent influences to the heart during inspiration, and a reinstatement
of vagal efferent influences to the heart during expiration. Thus, the
58
phenomenon is known as respiratory sinus arrhythmia. The amplitude of
respiratory sinus arrhythmia is not constant, but reflects higher brain
influences which directly inhibit or stimulate the cells of origin of the
vagus. Changes in the amplitude of respiratory sinus arrhythmia can be
observed in studies of sustained attention, stress, anesthesia, sleep
state, and in response to pharmacological treatments which depress the
central nervous system. During many of these conditions, the respiratory
parameters remain relatively constant.
The Vagal Tone Measure.
Assessment of vagal tone necessitates accurate quantification of the
amplitude of respiratory sinus arrhythmia. _ the component of heart
rate variance associated with respiratory sinus arrhythmia can be both
"physiologically" and "empirically" related to vagal influences to the
heart. The most sensitive measures of vagal tone must be based upon these
constraints. We havedeveloped a time series approach which accurately
extracts from the complex heart rate pattern the amplitude of respiratory
sinus arrhythmia. This measure has been labeled V to emphasize it is a
measure of vagal tone.
This procedure solves many of the problems associated with employing
time series statistics to study physiological processes. These problems
include non-stationarity, aperiodic influences, and the fact that even
when physiological processes are periodic, such as breathing and
respiratory sinus arrhythmia, they are not perfect sine waves. The method
includes a series of mathematically derived steps designed to enhance the
study of periodic processes. Information associated with sampling rate,
heart rate, and breathing rate need to be known and are incorporated in
the algorithms (ref. 6). The methods are based upon knowledge of
physiology and statistics. Misunderstanding of the method, either from a
statistical or physiological dimension, may result in an inappropriate
application and uninterpretable data.
Other estimates of vagal influence, such as measures of total heart
rate variability or mean successive differences, often reflect interesting
relationships with health status and behavior. However, these measures
are less sensitive to manipulations of vagal control and are less
consistent in demonstrating relationships with situational and
physiological variables. Moreover, these measures are confounded by both
physiological constraints (e.g., non-vagal influences) and statistical
abberations (e.g., the sampling rate and the average heart rate influence
the components of heart rate variability assessed with measures of heart
rate variability that incorporate a successive difference approach). In
many situations all measures of heart rate variability may be highly
correlated, however, it can be demonstrated that the vagal tone measure is
more sensitive to processes that can be physiologically linked to changes
in parasympathetic tone.
These findings do not negate the importance of observations that
global measures of heart rate variability are frequently related to mental
states and clinical status. Rather, these points argue that global
measures of heart rate variability are "composite" measures which can be
59
obtained through a variety of combinations of component influences on
heart rate variability (such as movement, blood pressure feedback,
respiratory sinus arrhythmia, and thermoregulatory influences).
Therefore, it is impossible to make a strong statement regarding the
specific physiological mechanisms mediating these relationships.
Validation studies.
To validate the vagal tone measure, a number of studies have
demonstrated its sensitivity to manipulations of cardiac vagal tone (ref.
1). Our research has demonstrated that stimulation of the aortic
depressor nerve in the rabbit increased the amplitude of respiratory sinus
arrhythmia (ref. 7). Stimulation of the aortic depressor nerve produces a
baroreceptor reflex characterized by increased vagal inhibitory action on
the heart. Vagal blockade with atropine removed the effect. Propranolol,
a beta-adrenergic blocker, did not alter the magnitude of the evoked
increase in the amplitude of respiratory sinus arrhythmia. The amplitude
of respiratory sinus arrhythmia was evaluated during manipulations of the
baroreceptor reflex in anesthetized cats (ref. 8). Hypertension, induced
by infusion of nitroprusside, was used to inhibit cardiac vagal tone. The
manipulations effectively produced state changes in blood pressure and
reflexively influenced the cardio-inhibitory influence on the heart (i.e.,
vagal tone). Hypertension produced an increase in the amplitude of
respiratory sinus arrhythmia. Hypotension produced a decrease in the
amplitude of respiratory sinus arrhythmia. Specific autonomic
contributions were assessed with administration of practolol (a beta-
adrenergic blocker) and atropine.
Although the above studies were conducted in anesthetized
preparations, we also have conducted research with alert and moving
preparations. In a study with rats, phenylephrine increased, atropine
abolished, and saline had no effect on the amplitude of respiratory sinus
arrhythmia (ref. 9). In a study with alert adults, four treatment levels
of atropine and a placebo control were administered (ref. 10, ref. 11).
The data demonstrated that the vagal blockade was monotonically related to
the amplitude of respiratory sinus arrhythmia. Moreover, respiratory
sinus arrhythmia was more sensitive to vagal blockade than heart rate (the
change in heart rate in response to atropine is often used a criterion
measure of vagal tone).
Sustained attention.
In a number of studies (ref. 12, ref. 13, ref. 14), heart rate
variability was evaluated during a variety of attention demanding tasks.
These studies demonstrated that independent of the direction of the heart
rate change during the tasks, heart rate variability was consistently
suppressed during sustained attention. Moreover, individuals with higher
baselevel heart rate variability exhibited greater suppression of heart
rate variability and performed better on reaction time tasks. These
studies used a measure of overall heart rate variability and were
conducted before the statistical procedures were developed to extract the
amplitude of respiratory sinus arrhythmia.
6O
Recently we have conducted research on the vagal tone measure
during sustained attention. In this study physiological and
performance measures were evaluated on 30 male and female students with a
mean age of 20.2 years. The tasks were mental arithmetic and a tracking
presented via an Atari Videoarcade system. Both tasks contained timers
that were visibly displayed and that counted down while the subject tried
to accumulate as many laps (in the tracking task) or points (in the
arithmetic task).
For the tracking task, the subject was asked to race a video
representation of a car around a track to make as many laps as possible in
60 sec. The task contained an element of uncontrollabillty. The task was
designed so that there was a tradeoff between speed and accuracy. If the
car went too fast for a certain period of time, the car would veer off
course into the progress-impeding borders. The task required being able
to control the speed while skillfully guiding the car to avoid the time-
consuming border areas. Subjects were told that psychomotor skill was
being assessed and that they would receive five cents for every completed
lap. Subjects were glvena practice session. The 60-second task was
followed by a 60-second rest period referred in the figures as the "off-
task" period. Each subject received three trials of an on-task/off-task
sequence.
In the arithmetic task, five numbers between I and 9 were presented
on the video screen for five seconds. A timer, displayed in the center of
the screen, counted down while the subject tried to add the numbers
together. Subjects responded by pressing a button. Subjects were
rewarded for performance. Similar to the "race," the "sum" task was
presented in three one-minute trials of an on-task/off-task sequence.
Collapsed across tasks heart period was shorter (faster heart rate)
on task (748 msec) than off-task (850 msec); heart period variability was
lower on-task (7.8) than off-task (8.4); respiratory frequency was faster
on task (.33 hz) than off-task (.25 Hz); Vagal tone was lower on-task
(7.4) than off-task (8.9); and the .i Hz wave had lower amplitude on-task
(7.3) than off-task (7.7).
A quantitative method of assessing the relative sensitivity of the
above dependent variables to attention demands is to calculate eta or
omega squared for the on-task/off-task effect. This procedure assesses
the percentage of variance of the dependent variable mediated by the
tasks. If the physiological variable is sensitive to the attention
demands, it will be reflected in a greater percentage of the sums of
squares associated with task relative to the total sums of squares in the
analysis of variance table. The vagal tone index was the most sensitive
of the physiological variables with an eta of .24 (i.e., 24X of the
variance of vagal tone was mediated by the attention demanding tasks).
The amplitude of the .I Hz wave (i.e., Traube-Herlng-Mayer wave), which
has been reputed to be sensitive to sustained attention had the lowest eta
and accounted for only 8_ of the variance.
61
Flight performance and vagal tone.
The study by Dellinger, Taylor, and Porges (1987) (ref. I0) provides
data on the relationship between changes in vagal tone and flight performance
decrement. The injection of atropine resulted in significant performance
decrements beginning at I hour post-lnjection and only minimal recovery by
post-lnjection. In contrast, the decrement in vagal tone was almost
instantaneous. The early physiological symptoms that occur prior to the
performance decrements potentially could be used in blo-cybernetlc system
to allow the pilot to land safely.
Thus, although there is a parallel under the high doses of atropine
(2.0 mg/75 kg, 4.0 mg/75 kg) between vagal tone and pilot performance, the
time courses of the two classes of variables differ. The vagal tone measure
reflects the immediate influence on the physiology although performance
does not deteriorate for at least one hour, thus reflecting the pilot's
ability to compensate.
Summary.
Other influences on central nervous system such as anesthesia, head
trauma and sleep have been investigated. For example, inhalant anesthesia
which blocks central nervous system monitoring of peripheral sensory
information virtually eliminates vagal tone. The vagal tone monitored
following head trauma in the intensive care unit predicts neurological
outcome. Other studies have demonstrated that vagal tone shifts as a
function of sleep state. In general the vagal tone index appears to
monitor global states of the central nervous system and may be useful in
screening the general state of pilots.
62
References.
le
.
e
e
.
.
e
e
.
Porges, S.W., McCabe, P., & Yongue, B.: Resplratory-Heart Rate
Interactions: Psychophysiological Implications for Pathophysiology
and Behavior. In Perspectives in Cardiovascular PsvchoohvsioloRT,
J. Cacloppo & R. Petty (eds.), 1982, pp. 223-264.
Porges, S.W.: Spontaneous Oscillations in Heart Rate: Potential
Index of Stress. In Animal Stress, P.G. Moberg (ed.), 1985, pp. 97-
111.
Hatch, J. P., Klatt, K., Porges, S. W., Schroeder-Sasheway, L., and
Suplk, J. D.: The Relation Between Rhythmic Cardiovascular
Variability and Relativity to Orthostatic, Cognitive, and Cold
Pressor Stress. Psychophyslology, vol. 23 (I), 1986, pp. 48-56.
Lopes, O.V., & Palmer, J.F.: Proposed Respiratory Gating Mechanism
for Cardiac Slowing. Nature, vol. 264, 1976, pp. 454-456.
Gilbey, M.P., Jordan, D., Richter, D. W., & Spyder, K.M.: The
Inspiratory Control of Vagal Cardio-lnhibltory Neurons in the Cat.
American Journal Physiology, 1983, vol. 343, pp. 57-58.
Jordon, D., Khalid, M.E.M., Schneiderman, N., & Spyer, K.M.: The
Location and Properties of Preganglionlc Vagal Cardlomotor Neurones
in the Rabbit. Pfugers Archly-European Journal of Phyalology, vol.
395, 1982, pp. 244-250.
Porges, S. W.: Method and Apparatus for Evaluating Rhythmic
Oscillations in Aperiodic Physiological Response Systems.
Number: 4,510,944. April 16, 1985.
Patent
McCabe, P.M., Yongue, B.G., Porges, S.W., & Ackles, P.K.: Changes in
Heart Period, Heart Period Variability and a Spectral Analysis
Estimate of Respiratory Sinus Arrhythmla During Aortic Nerve
Stimulation in Rabbits. PsYchoDhyslolo_, vol. 22, 1984, pp. 195-
203.
McCabe, P.M., Yongue, B.G., Porges, S.W., & Ackles, P.K.: Changes in
Heart Period, Heart Period Variability and a Spectral Analysis
Estimate of Respiratory Sinus Arrhythmla in Response to
Pharmacological Manipulations of the Baroreceptor Reflex in Cats.
PsychoDhyslolo_v, vol. 21, 1985, pp. 149-148.
63
I0. Yongue, B.G., McCabe, P.M., Porges, S.W., Riviera, M., Kelley, S.L., &
Ackles, P.K.: The Effects of Pharmacological Manipulations that
Influence Vagal Control of the Heart on Heart Period, Heart-Period
Variability, and Respiration in Rats. PsychoDhysioloffy, vol. 19,
1982, pp. 426-432.
II. De]linger, J.A., Taylor, H.L., & Porges, S.W.: Atropine Sulfate
Effects on Aviator Performance and on Respiratory-Heart Period
Interactions. Aviation and Space Environment Medicine, vol. 54,
1987, pp. 1242-1253.
12. Porges, S.W.: Respiratory Sinus Arrhythmla: Physiological Basis,
Quantitative Method, and Clinical Implications. In
Cardioresplratory and Cardlosomatlc Psychophyslolo_v. P.
Grossman, K. Janssen, & D. Valtl, (eds.), 1986, pp. 101-115.
13. Porges, S.W., & Raskln, D.C.: Respiratory and Heart Rate Components
of Attention. Journal of Experimental Psychology, vol. 81, 1969,
pp. 487-503.
14. Porges, S.W.: Heart Rate Variability and Deceleration as Indexes of
Reaction Time. Journal of Experimental PsYcholoffv, vol. 92, 1972,
pp. 103-110.
15. Walter, G.F., & Porges, S.W.: Heart Rate and Respiratory Responses as
a Function of Task Difficulty: The Use of Discrimlnant Analysis in
the Selection of Psychologically Sensitive Physiology Responses.
PsychoDhysloloi_y, vol. 13, 1976, pp. 563_571.
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Vagal tone as an index of mental state

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