Cardiac perception and cardiac control

The evidence regarding specific cardiac perception and discrimination, and its relationship to voluntary cardiac control, is critically reviewed. Studies are considered in three sections, depending on the method used to assess cardiac perception: questionnaire assessment, discrimination procedures, and heartbeat tracking. The heartbeat tracking procedure would appear to suffer least from interpretative difficulties. Recommendations are made regarding the style of analysis used to assess heartbeat perception in such tracking tasks.     

Estimation of the involvement of subconsciousness in heartbeat perception in healthy volunteers

The results of analysis of heartbeat parameters and characteristics of its self-monitoring by 25 healthy volunteers have been used as the basis for original estimation of the involvement of subconsciousness in heartbeat perception. The first objective index for such estimation is proposed. It is calculated as the individual fragmentation coefficient of heartbeat perception. The discreteness of heartbeat perception is related to changes in the degree (weight) of involvement of subconsciousness in the perception of cardiac signals. A conclusion is drawn on the relationship between the efficiency of perception of one’s own heartbeat and the degree of involvement of subconsciousness in this process. The practical implication of the study is the possibility of using a similar approach to estimating the weight of unconscious processes in perception of stimuli of different types, including those used in psychodiagnostic studies.     

Interoception across modalities: on the relationship between cardiac awareness and the sensitivity for gastric functions

The individual sensitivity for ones internal bodily signals ("interoceptive awareness") has been shown to be of relevance for a broad range of cognitive and affective functions. Interoceptive awareness has been primarily assessed via measuring the sensitivity for ones cardiac signals ("cardiac awareness") which can be non-invasively measured by heartbeat perception tasks. It is an open question whether cardiac awareness is related to the sensitivity for other bodily, visceral functions. This study investigated the relationship between cardiac awareness and the sensitivity for gastric functions in healthy female persons by using non-invasive methods. Heartbeat perception as a measure for cardiac awareness was assessed by a heartbeat tracking task and gastric sensitivity was assessed by a water load test. Gastric myoelectrical activity was measured by electrogastrography (EGG) and subjective feelings of fullness, valence, arousal and nausea were assessed. The results show that cardiac awareness was inversely correlated with ingested water volume and with normogastric activity after water load. However, persons with good and poor cardiac awareness did not differ in their subjective ratings of fullness, nausea and affective feelings after drinking. This suggests that good heartbeat perceivers ingested less water because they subjectively felt more intense signals of fullness during this lower amount of water intake compared to poor heartbeat perceivers who ingested more water until feeling the same signs of fullness. These findings demonstrate that cardiac awareness is related to greater sensitivity for gastric functions, suggesting that there is a general sensitivity for interoceptive processes across the gastric and cardiac modality.     

Visceral perception versus visceral detection: Disentangling methods and assumptions

A within-subject experiment compared three paradigms commonly used in visceral perception: self-report, heartbeat tracking, and signal detection. Eighteen undergraduates estimated heart rate using each technique while engaging in a number of separate tasks conducted a week apart. Although all three techniques significantly tapped accuracy of heart rate perception, only the self-report and signal detection methods were reliable over time. Most important, there was no relationship involving any of the methods in measuring accuracy. The findings suggest some fundamental differences in the assumptions and perceptual properties of the various paradigms. A distinction is made between visceral perception and detection. Perception implies the subject's use of both internal physiological and external environmental information in the perception of visceral state. Detection connotes the subject's use of only physiological information — to the exclusion of all other factors. The relevance of these approaches for biofeedback and real-world symptom perception is discussed.     

Visceral perception versus visceral detection: disentangling methods and assumptions

A within-subject experiment compared three paradigms commonly used in visceral perception: self-report, heartbeat tracking, and signal detection. Eighteen undergraduates estimated heart rate using each technique while engaging in a number of separate tasks conducted a week apart. Although all three techniques significantly tapped accuracy of heart rate perception, only the self-report and signal detection methods were reliable over time. Most important, there was no relationship involving any of the methods in measuring accuracy. The findings suggest some fundamental differences in the assumptions and perceptual properties of the various paradigms. A distinction is made between visceral perception and detection. Perception implies the subject's use of both internal physiological and external environmental information in the perception of visceral state. Detection connotes the subject's use of only physiological information--to the exclusion of all other factors. The relevance of these approaches for biofeedback and real-world symptom perception is discussed.     

Noninvasive technique for measurement of heartbeat regularity in zebrafish (Danio rerio) embryos

Background  

Zebrafish (Danio rerio), due to its optical accessibility and similarity to human, has emerged as model organism for cardiac research. Although various methods have been developed to assess cardiac functions in zebrafish embryos, there lacks a method to assess heartbeat regularity in blood vessels. Heartbeat regularity is an important parameter for cardiac function and is associated with cardiotoxicity in human being. Using stereomicroscope and digital video camera, we have developed a simple, noninvasive method to measure the heart rate and heartbeat regularity in peripheral blood vessels. Anesthetized embryos were mounted laterally in agarose on a slide and the caudal blood circulation of zebrafish embryo was video-recorded under stereomicroscope and the data was analyzed by custom-made software. The heart rate was determined by digital motion analysis and power spectral analysis through extraction of frequency characteristics of the cardiac rhythm. The heartbeat regularity, defined as the rhythmicity index, was determined by short-time Fourier Transform analysis.     

Biogenic amines evoke heartbeat reversal in larvae of the sweet potato hornworm,Agrius convolvuli

The sweet potato hornworm, Agrius convolvuli, possesses a pair of anterior cardiac nerves innervating the dorsal vessel. The anterior cardiac nerves branch off the visceral nerve that arises posteriorly from the frontal ganglion. Heartbeat reversal from anterograde heartbeat to posterograde heartbeat is triggered by the anterior cardiac nerves. Application of octopamine (OA) during the anterograde heartbeat phase reverses the anterograde heartbeat to the posterograde heartbeat, while application of OA during the phase of posterograde heartbeat accelerates heartbeat. The heartbeat reversal from anterograde heartbeat to posterograde heartbeat evoked by stimuli applied to the visceral nerve is blocked by application of the octopaminergic antagonists, phentolamine and chlorpromazine. The results suggest that OA may be a neurotransmitter for the anterior cardiac nerve. The alary muscle of the second segment receives excitatory innervation from the posterior cardiac nerve and from the nerve which extends from the second abdominal ganglion. Activation of the alary muscle results in acceleration of posterograde heartbeat. Other neurotransmitters, besides OA, may take part in the resultant acceleration.     

Realtion of heart rate control to heartbeat perception

The relation of heartbeat perception to voluntary control of heart rate (HR) and to learning of enhanced HR control during feedback was studied in three experiments. In Experiment I heartbeat perception was unrelated to voluntary control of HR but was negatively correlated with HR learning. Experiments II and III showed that heartbeat perception was unrelated to either initial voluntary control or learning and suggested that sampling error accounted for the negative correlation in Experiment I. Experiment I also demonstrated that learned increases in HR are retained for at least 10 weeks following feedback training. Autonomic Perception Questionnaire scores were not predictive of voluntary HR control or learning.     

Relation of heart rate control to heartbeat perception

The relation of heartbeat perception to voluntary control of heart rate (HR) and to learning of enhanced HR control during feedback was studied in three experiments. In Experiment I heartbeat perception was unrelated to voluntary control of HR but was negatively correlated with HR learning. Experiments II and III showed that heartbeat perception was unrelated to either initial voluntary control or learning and suggested that sampling error accounted for the negative correlation in Experiment I. Experiment I also demonstrated that learned increases in HR are retained for at least 10 weeks following feedback training. Autonomic Perception Questionnaire scores were not predictive of voluntary HR control or learning.     

Heartbeat patterns during the postembryonic development of Drosophila melanogaster

Pulsations of the dorsal vessel were recorded in vivo during the whole postembryonic development of D. melanogaster, by means of a newly invented, pulse-light opto-cardiographic method. The young larvae of the 1st and 2nd instars submerged in the feeding medium exhibited extremely high rates of heartbeat, 7Hz at room temperature. These values are among the highest rates of heartbeat ever recorded in the animal kingdom. The fully grown larvae of the 3rd instar showed approximately half of the maximum heartbeat rate (3.5-4Hz), which became stabilized after pupariation to 2.5-2.7Hz.The larval heartbeat was always uni-directional, in the forward-oriented or anterograde direction and it was almost continuous. The slowly disintegrating, old larval heart used to beat at the constant frequency of 2.5-2.7Hz until complete cessation of all cardiac functions in 1-day-old puparium. In spite of the persisting constant heartbeat frequency, the transformation process of the larval heart was associated with successively decreasing amplitude of the systolic contractions and with the prolongation of the resting periods. The newly formed heart of the pupal-adult structure exhibited a qualitatively new pattern of heartbeat activity, which was manifested by periodic reversal of the heartbeat with the faster anterograde and slower retrograde phases. The frequencies of both of these reciprocal cardiac pulsations gradually increased during the advanced pharate adult period, reaching the values of 4-5Hz at the time of adult eclosion. Adult males and females also exhibited a perfect pattern of heartbeat reversal, with still very high rates of the anterograde heartbeat, in the range of 5-6Hz. In addition to the cardiac functions, we have recorded several kinds of extracardiac pulsations, which often interfered severely with the recordings of the heartbeat. There were strong, irregular extracardiac pulsations of a neurogenic nature (somatic muscles, oral armature) and relatively slow extracardiac pulsations of a myogenic nature (intestinal peristaltics, 0.2-0.3Hz). The extracardiac and cardiac pulsations were independent, their functions were not correlated. A possibility of creating new challenges in combination of molecular biology with the functional physiology of the heart have been discussed.     

Cardioregulatory nerves in the spider Eurypelma marxi Simon

The objective of this study was to locate nerves arising from the CNS that have a cardioregulatory function in the tarantula, Eurypelma marxi Simon. Ramifications of the paired abdominal nerve VIIIb merge with the cardiac ganglion within the first heart segment. Electrical stimulation of the branches of nerve VIIIb that connect with the cardiac ganglion produce changes in heartbeat rate and amplitude. Nerve cutting experiments indicate that no other cardioregulatory nerves are present. Both increases and decreases in heart activity can be produced upon electrical stimulation of nerve VIIIb on each side of the heart. Only one action potential associated with the response of each type could be recorded in each member of the nerve pair. Therefore, we conclude that there are two inhibitory and two acceleratory neurons that arise in the central nervous system to modulate heartbeat activity. The inhibitory effect becomes maximal at a stimulation frequency of 20-30 Hz and the accelerator effect at 30-40 Hz. The aftereffect of acceleratory nerve activity exceeds that of inhibitory nerve activity. When the inhibitor and accelerator are activated simultaneously, the inhibitor dominates. The regulatory nerves interact with neurons in the cardiac ganglion. During inhibition, the number of externally recorded spikes in each ganglionic burst is decreased. The rate and magnitude of the heartbeat are decreased concomitantly. Stimulation of the accelerator enhances electrical activity in the cardiac ganglion at the same time that the heartbeat rate and amplitude are increased.     

Cardiac reflexes and their neural pathways in lepidopterous insects

Previously described salines for lepidoptera did not maintain a constant heart rate for a very long. We have been successful in maintaining a normal heartbeat for many hours in a newly designed saline. This saline was also suitable for maintaining normal neuromuscular junctional potentials. The cardiac reflexes studied in larvae of Bombyx and Agrius were five types of cardiac responses induced by mechanical stimuli to sensillar setae. The cardiac responses were caused by electrical stimulation of nerves in the reflex pathways. The antidromic heartbeat was triggered even in larvae before the 5th instar by stimulation of axons in the visceral nerve arising from the frontal ganglion and terminating at the aorta, while spontaneous heartbeat reversal started to occur in wandering larvae. Other axons in the visceral nerve terminate at the rear end of the heart. Electrical stimuli to the nerves caused cardiac inhibition of the orthodromic heartbeat. Nerves extending from the visceral nerve to the alary muscles of the 2nd abdominal segment contain axons to increase the tone of the muscles. Nerves extending from the 7th abdominal ganglion to the most posterior alary muscles also contain axons to increase the tone of the muscles, and were responsible for acceleration of the antidromic and orthodromic heartbeat, respectively.     

Chaotic Signatures of Heart Rate Variability and Its Power Spectrum in Health,Aging and Heart Failure

A paradox regarding the classic power spectral analysis of heart rate variability (HRV) is whether the characteristic high- (HF) and low-frequency (LF) spectral peaks represent stochastic or chaotic phenomena. Resolution of this fundamental issue is key to unraveling the mechanisms of HRV, which is critical to its proper use as a noninvasive marker for cardiac mortality risk assessment and stratification in congestive heart failure (CHF) and other cardiac dysfunctions. However, conventional techniques of nonlinear time series analysis generally lack sufficient sensitivity, specificity and robustness to discriminate chaos from random noise, much less quantify the chaos level. Here, we apply a ‘litmus test’ for heartbeat chaos based on a novel noise titration assay which affords a robust, specific, time-resolved and quantitative measure of the relative chaos level. Noise titration of running short-segment Holter tachograms from healthy subjects revealed circadian-dependent (or sleep/wake-dependent) heartbeat chaos that was linked to the HF component (respiratory sinus arrhythmia). The relative ‘HF chaos’ levels were similar in young and elderly subjects despite proportional age-related decreases in HF and LF power. In contrast, the near-regular heartbeat in CHF patients was primarily nonchaotic except punctuated by undetected ectopic beats and other abnormal beats, causing transient chaos. Such profound circadian-, age- and CHF-dependent changes in the chaotic and spectral characteristics of HRV were accompanied by little changes in approximate entropy, a measure of signal irregularity. The salient chaotic signatures of HRV in these subject groups reveal distinct autonomic, cardiac, respiratory and circadian/sleep-wake mechanisms that distinguish health and aging from CHF.     

Cortical mechanisms of sensory learning and object recognition

Learning about the world through our senses constrains our ability to recognise our surroundings. Experience shapes perception. What is the neural basis for object recognition and how are learning-induced changes in recognition manifested in neural populations? We consider first the location of neurons that appear to be critical for object recognition, before describing what is known about their function. Two complementary processes of object recognition are considered: discrimination among diagnostic object features and generalization across non-diagnostic features. Neural plasticity appears to underlie the development of discrimination and generalization for a given set of features, though tracking these changes directly over the course of learning has remained an elusive task.     

Statistical coding and decoding of heartbeat intervals

The heart integrates neuroregulatory messages into specific bands of frequency, such that the overall amplitude spectrum of the cardiac output reflects the variations of the autonomic nervous system. This modulatory mechanism seems to be well adjusted to the unpredictability of the cardiac demand, maintaining a proper cardiac regulation. A longstanding theory holds that biological organisms facing an ever-changing environment are likely to evolve adaptive mechanisms to extract essential features in order to adjust their behavior. The key question, however, has been to understand how the neural circuitry self-organizes these feature detectors to select behaviorally relevant information. Previous studies in computational perception suggest that a neural population enhances information that is important for survival by minimizing the statistical redundancy of the stimuli. Herein we investigate whether the cardiac system makes use of a redundancy reduction strategy to regulate the cardiac rhythm. Based on a network of neural filters optimized to code heartbeat intervals, we learn a population code that maximizes the information across the neural ensemble. The emerging population code displays filter tuning proprieties whose characteristics explain diverse aspects of the autonomic cardiac regulation, such as the compromise between fast and slow cardiac responses. We show that the filters yield responses that are quantitatively similar to observed heart rate responses during direct sympathetic or parasympathetic nerve stimulation. Our findings suggest that the heart decodes autonomic stimuli according to information theory principles analogous to how perceptual cues are encoded by sensory systems.     

Body Conscious? Interoceptive Awareness,Measured by Heartbeat Perception,Is Negatively Correlated with Self-Objectification

Background

‘Self-objectification’ is the tendency to experience one''s body principally as an object, to be evaluated for its appearance rather than for its effectiveness. Within objectification theory, it has been proposed that self-objectification accounts for the poorer interoceptive awareness observed in women, as measured by heartbeat perception. Our study is, we believe, the first specifically to test this relationship.

Methodology/Principal Findings

Using a well-validated and reliable heartbeat perception task, we measured interoceptive awareness in women and compared this with their scores on the Self-Objectification Questionnaire, the Self-Consciousness Scale and the Body Consciousness Questionnaire. Interoceptive awareness was negatively correlated with self-objectification. Interoceptive awareness, public body consciousness and private body consciousness together explained 31% of the variance in self-objectification. However, private body consciousness was not significantly correlated with interoceptive awareness, which may explain the many nonsignificant results in self-objectification studies that have used private body consciousness as a measure of body awareness.

Conclusions/Significance

We propose interoceptive awareness, assessed by heartbeat perception, as a measure of body awareness in self-objectification studies. Our findings have implications for those clinical conditions, in women, which are characterised by self-objectification and low interoceptive awareness, such as eating disorders.     

Excitatory neural control of posterograde heartbeat by the frontal ganglion in the last instar larva of a lepidopteran, Bombyx mori

The frontal ganglion of the silkworm (Bombyx mori) gives rise to a visceral nerve, branches of which include a pair of anterior cardiac nerves and a pair of the posterior cardiac nerves. Forward-fill of the visceral nerve with dextran labeled with tetramethyl rhodamine shows the anterior cardiac nerves innervate the anterior region of the dorsal vessel. Back-fill of the anterior cardiac nerves with Co²⁺ and Ni²⁺ ions and the fluorescent dye reveals that the cell bodies of two motor neurons are located in the frontal ganglion. Injection of 5, 6-carboxyfluorescein into the cell body of an identified motor neuron shows that the neuron gives rise to an axon running to the visceral nerve. Unitary excitatory junctional potentials (EJPs) were recorded from a myocardial cell at the anterior end of the heart. They responded in a one-to-one manner to electrical stimuli applied to the visceral nerve, or to impulses generated by a depolarizing current injected into the cell body. EJPs induced by stimuli at higher than 0.5 Hz showed facilitation while those induced at higher than 2 Hz showed summation. Individual EJPs without summation, or a train of EJPs with summation, caused acceleration in the phase of posterograde heartbeat and heart reversal from anterograde heartbeat to posterograde heartbeat. It is likely that the innervation of the anterior region of the dorsal vessel by the motor neurons, through the anterior cardiac nerves is responsible for the control of heartbeat in Lepidoptera, at least in part.     

Dual effects of dopamine on the adult heart of the isopod crustacean Ligia exotica

In the adult heart of the isopod crustacean Ligia exotica, the cardiac ganglion acts as the primary pacemaker with the myocardium having a latent pacemaker property. We show several lines of evidence that dopamine modulates the heartbeat of adult L. exotica affecting both pacemaker sites in the heart. Dopamine caused positive chronotropic (frequency increase) and inotropic (amplitude increase) effects on the heartbeat in a concentration dependent manner. The time courses of these effects were considerably different and the inotropic effect appeared later and lasted longer than the chronotropic effect. Dopamine rapidly increased the frequency of the bursting activity in the cardiac ganglion neurons and each impulse burst of the cardiac ganglion was always followed by a heartbeat. Moreover, dopamine slowly increased the amplitude and duration of the action potential plateau (plateau potential) of the myocardium. When the myocardial pacemaker activity was induced by application of tetrodotoxin, which suppresses cardiac ganglion activity, dopamine slowly increased the amplitude and duration of the myocardial plateau potential while decreasing its frequency. These results suggest that dopamine modulates the heartbeat in adult L. exotica producing a dual effect on the two pacemaker sites in the heart, the cardiac ganglion and myocardium.     

Active regulation of respiration and circulation in pupae of the codling moth (Cydia pomonella)

Regulation of autonomic physiological functions has been investigated by means of multisensor electronic methods, including electrocardiographic recording of heartbeat, strain-gauge recording of extracardiac hemocoelic pulsations (EHPs), anemometric recording of air passage through spiracles and respirographic recording of O(2) consumption and CO(2) output. Pupae of Cydia exhibit continuous respiration without remarkable bursts of CO(2). The dorsal vessel of these pupae exhibited regular heartbeat reversals characterized by shorter intervals of faster (forward oriented or anterograde) pulsations and longer intervals of slower (backward oriented or retrograde) peristaltic waves. The periodically repeated EHPs were present during the whole pupal interecdysial period. The internal physiological mechanisms regulating the cardiac (heartbeat) and extracardiac (EHP) pulsations were completely independent for most of the pupal instar. Simultaneous multisensor analysis revealed that the anterograde heartbeat of the dorsal vessel had similar but not identical frequency with EHPs. During advanced pharate adult development, frequency of cardiac and extracardiac pulsation periods profoundly increased until almost uninterrupted pulsation activity towards adult eclosion. At this time, the cardiac and extracardiac pulsations occasionally performed in concert, which enhanced considerably the efficacy of hemolymph circulation in pharate adults with high metabolic rates. The fastest hemolymph flow through the main body cavity was always associated with EHPs and with anterograde heartbeat. Simple physical diffusion of O(2) and CO(2) through spiracles (diffusion theory of insect respiration) does not play a significant role in pupal respiration. Instead, several kinds of regulated, mechanical ventilations of the tracheal system, including EHPs are responsible for effective tracheal ventilation.     

Mechanical aspects of heartbeat reversal in pupae of Manduca sexta

Pulsations of the dorsal vessel were investigated with new optocardiographic techniques based on the transmission and reflection of pulse-light through optic fibers. This noninvasive technique enabled simultaneous, in vivo multisensor recordings of the heartbeat without touching the pupal integument. There was a very regular heartbeat reversal with 3 distinctive phases: (a) a backward-oriented (retrograde) cardiac pulsation; (b) a forward-oriented (anterograde) pulsation with faster frequency; and (c) shorter or longer periods of temporary cardiac standstill that usually occurred after the termination of the anterograde phase. Occasionally, there were localized series of systolic cardiac contractions during the retrograde phase. Simultaneous recordings from the base and the tail of the abdomen revealed a reciprocal, "mirror image-like", quantitative relationship. The most intensive anterograde hemolymph flow occurred at the base while the most intensive retrograde flow occurred at the tail of the abdomen. The bi-directional switchovers of heartbeat (reversal) were occasionally associated with modifications during each of the unidirectional cardiac phases. Anterograde peristalsis showed a 2-fold higher frequency of pulsation in the thoracic aorta in comparison with the posterior parts of the heart. Thus, in addition to the "odd" peristaltic waves originating at the tail, there were intercallated "even" peristaltic waves originating in the middle of the abdomen. Both of them propagated hemolymph through the thoracic aorta into the head; the first waves took the hemolymph in from the distal end, while the second sucked it from the middle of the abdomen. The use of multiple optocardiographic sensors also enabled detection of cardiac pulsations on the opposite, ventral side of the body, within the ventral perineural sinus. The ventral side of the head showed only the presence of an anterograde pulse, whereas the ventral side of the tail exhibited a strong reciprocal retrograde phase and a very weak anterograde phase. These results explain why the existence of a periodic heartbeat reversal should be essential for circulatory functions at both extremities of the cylindrical insect body. In diapausing pupae, regular cycles of heartbeat reversal were substituted by prolonged periods of anterograde pulsation during the entire duration of bursts of CO2 release (average duration of the burst was 18-20 min, periodicity 5 to 18 h). The physiological nature of such feed-back correlation between heartbeat and metabolic CO2 production is not yet clear, because the anterograde heartbeat could be also induced by a number of nonspecific factors unrelated to CO2 (mechanical irritation, injury, injections, elevated temperature). During the postdiapause, developing pharate-adult stage, the correlation between CO2 and anterograde heartbeat completely disappeared. It has been concluded that regulation of insect heartbeat represents a highly coordinated, myogenic stereotype with inherent rhythmicity, which can be modified by a number of external and internal factors.