Elsevier

Neuropsychologia

Volume 36, Issue 5, 1 May 1998, Pages 461-468
Neuropsychologia

Hemisphere asymmetry in parasympathetic control of the heart

https://doi.org/10.1016/S0028-3932(97)00129-2Get rights and content

Abstract

Hemisphere asymmetry in the control of parasympathetic outflow to the sino-atrial node of the heart was studied in healthy human subjects using lateralized film presentation for selective sensory stimulation of the hemispheres and power spectral analysis of heart rate variability as a measure of vagal tone. There was a clear and consistent left hemisphere predominance in the control of parasympathetic modulation of cardiac activity which cannot be attributed to differences in emotional processing. Supplementing previous findings of our research group, the present study indicates that control of autonomic cardiac activity at the level of the cerebral cortex seems to be characterized by a division of responsibility between both hemispheres, sympathetic activity being mainly controlled by the right hemisphere and parasympathetic activity being under the left hemisphere’s main control.

Introduction

Recent research has supported the view that brain asymmetry is a universal phenomenon characterizing functioning of the whole nervous system [1]. The two brain sides not only differ in cognitive and emotion-related processing, as has been known since many years, but possibly to an even higher degree in the control of a broad spectrum of autonomic-physiologic functions including cardiac activity [2].

Neuralcontrol of the heart is accomplished by right-sided and left-sided sympathetic and parasympathetic pathways innervating the sinoatrial (SA) node, the atrial myocardium, the atrioventricular (AV) node, and the ventricular myocardium 3, 4. There is ample evidence that efferent innervation of the heart is lateralized in the peripheral part of the autonomic system with right-sided and left-sided autonomic pathways influencing cardiac activity in an asymmetric manner [5]. In accordance with a clearly denser distribution of right-sided sympathetic and parasympathetic fibers to the pacemaker tissues of the SA-node, chronotropic cardiac activity, as manifested by heart rate changes, is predominantly and more efficiently controlled by sympathetic and parasympathetic fibers running on the right side. Atrioventricular conduction (dromotropic activity) and myocardial contractility (inotropic activity), on the contrary, are more efficiently controlled by outflow from left-sided autonomic pathways.

Considering the remarkable lateralization of autonomic cardiac control at the peripheral level, the question arises whether there is an analogous mode or organization at the level of the central nervous system. Since most of the autonomic pathways descending from brain stem areas take an ipsilateral route, it is not surprising to find that brain stem regions immediately involved in autonomic regulation of cardiac activity, such as hypothalamic or medullary areas, seem to be lateralized in the same manner as the peripheral pathways. With respect to sympathetic outflow to the heart, it was found that unilateral stimulation of the right hypothalamus in vagotomized dogs produced a marked acceleration of heart rate with only moderate increase in cardiac contractility, whereas stimulation of the left hypothalamus caused a strong increase in cardiac contractility with only moderate acceleration of heart rate [6]. Similar results were obtained for the dorsal [7]and rostral ventrolateral medulla in cats [8]. With respect to parasympathetic control of dromotropic activity, a three times higher number of retrogradely labeled vagal neurons were found in the left rostral ventrolateral nucleus ambiguus as compared to the right 9, 10.

The above observations led to the common conviction [11]that brain in general is organized according to these principles, the right brain side being responsible for sympathetic and parasympathetic control of chronotropic cardiac activity and the left brain side being responsible for sympathetic and parasympathetic control of dromotropic and inotropic activity.

But there is now increasing evidence that at the level of the cerebral cortex, the situation is not as clear, and asymmetry seems to obey a different logic. Recent research favors the view that sympathetic control of the heart is entirely under right-hemispheric predominance. Whereas this has been expected for chronotropic activity 12, 13, it is somewhat surprising that sympathetic modulation of inotropic activity also seems to be under the primary control of the right hemisphere. This has been demonstrated recently by our research group [14]showing that myocardial contractility in humans is influenced mainly by the right hemisphere.

At present, no reliable conclusions can be drawn with respect to parasympathetic control of the heart. With rare exceptions 15, 16, 17, 18, most studies examining differences in parasympathetic control relied on heart rate deceleration as a measure of parasympathetic innervation. Whereas some clinical studies on patients with unilateral brain damage 19, 20as well as a study on normal subjects [21]seem to point to a closer involvement of the right hemisphere in inducing heart rate deceleration, studies using unilateral cerebral inactivation by amobarbital injection 12, 22, 23or electric stimulation of the left versus right insular cortex [24], favor the view that heart rate deceleration is predominantly under left-hemispheric control. The crucial problem in all these studies is that heart rate deceleration is not an unequivocal measure of parasympathetic activity because heart rate is dually influenced by both sympathetic and parasympathetic activity, and a decrease in heart rate can also be due to reduced sympathetic innervation of the sinoatrial node.

A methodological approach allowing for a selective and independent assessment of vagal control of the heart is power spectral analysis of heart rate variability (HRV) 25, 26, 27. By transforming beat-to-beat fluctuations of heart rate into their frequency components, a power spectrum is obtained that contains two distinct spectral bands. Fluctuations in the high frequency (HF) band, ranging between 0.12–0.40 Hz, are mainly caused by central and peripheral correlates of respiratory activity. Power in this component is nearly exclusively due to parasympathetic activity. This is attributable in large part to differences in low-pass filter properties of the sympathetic and parasympathetic cardioeffector synapses, sympathetic synapses being less able to follow the high frequency oscillations (>0.12 Hz) associated with respiration [28].Empirical support for these physiological observations is also provided by autonomic blockade studies, revealing that power in the HF-component is virtually eliminated by vagal blockade but is largely unaffected by sympathetic blockade 29, 30, 31, 32. Additional information can be derived from analyzing the low frequency (LF) component (0.04–0.12 Hz) and the LF\HF-ratio, although interpretation of this component is not as straightforward as interpretation of the HF-component [33]. Whereas some authors claim that the LF-component primarily reflects sympathetic activity the majority of research workers favors the view that it is jointly influenced by parasympathetic and sympathetic outflow. Strong vagal contributions to the LF-band are reflected by a marked reduction of LF-power during vagal blockade 30, 31, 32. Sympathetic influences are revealed by reducing or increasing LF-power by either blocking or stimulating sympathetic outflow 27, 34, 35. They become especially marked if LF-power is expressed in normalized units [26]. Due to the fact that the LF-band includes sympathetic influences, whereas the HF-band reflects only vagal tone, the LF\HF-ratio is considered by most authors as an estimate of sympathovagal balance.

As far as we know, no studies have been done in healthy subjects to compare the roles of the right and left hemispheres in parasympathetic control of the heart using a selective and unequivocal measure of parasympathetic activity, as described above. Therefore, in the present study we used power spectral analysis of HRV to examine hemisphere differences in parasympathetic control of chronotropic cardiac activity in a group of healthy human subjects.

Forty-five right-handed subjects (34 females, 11 males), aged 20–30 years, participated in the study. None of the subjects had been in ambulatory or stationary treatment because of cardiovascular or brain diseases and none had serious complications in the cardiovascular or central nervous system as assessed by a disease questionnaire.

The ECG was recorded by means of a bipolar chest lead. Respiration was monitored by a strain-gauge placed around the chest at the height of the xyphoid process. All signals were amplified on a ZAK-Mediport polygraph interfaced to a microcomputer. Respiratory rate was processed by a respiration scoring program and expressed as breath per minute. The ECG signals were digitized at 1 kHz by a 8-bit A\D converter. A peak detection algorithm determined the temporal position of the R-waves to an accuracy of 0.1 ms. Errors in R-wave detection were edited manually. The presence of ectopic beats and artifacts was checked on the screen, although no abnormalities were found in any subject. R-R intervals were then calculated as the time interval between two consecutive R-waves. Afterwards, R-R interval data were resampled at 1 Hz to obtain equidistant time series values.

Fourier transforms were used to calculate spectral power. A record length of 308 sample points (approximately 5 min), corresponding to the length of film presentation, was selected for power spectrum analysis. Prior to computing Fourier transforms, time series data were linearly detrended and filtered using a Hanning window. Estimates of spectral power were adjusted to compensate for attenuation produced by the filter. The following measures of HRV were obtained: total power (TP, 0.04–0.50 Hz), absolute values of power in the HF- and LF-range, normalized units of power in the HF- and LF-range (nHF, nLF), and the LF\HF-ratio of power.

In order to study whether the cerebral hemispheres differ in the way they are modulating parasympathetic innervation of the heart, they were selectively stimulated by presenting short movies under lateralized viewing conditions alternately to the left or right visual half field (VHF) while simultaneously recording HRV. The theoretical and methodological foundations of lateralized film presentations as a method of studying cerebral asymmetries in the control of autonomic-physiologic activity have been extensively discussed elsewhere [36]. In short, stimuli which are perceived in the periphery of the visual field are projected via the optic tracts of both eyes only to the visual areas of the opposite hemisphere. Therefore, presenting a film to the left visual half field (L-VHF) implicates that it is processed by the visual areas of the right hemisphere, whereas presenting it to the right visual half field (R-VHF) means that it is processed by the visual areas of the left hemisphere. There are several indications that neural activity evoked by unilateral visual stimulation remains largely lateralized, with cortical activation being higher in the directly stimulated hemisphere even after neural processing has spread beyond the inferotemporal visual areas enabling stimulus correlates to be conveyed to the other hemisphere.

In order to warrant that a film can only be perceived in one preselected VHF irrespective of the subject’s eye movements, we have developed a technique preventing foveal fixation of the visual stimuli while allowing free ocular scanning. The technique has been successfully applied to the study of brain asymmetry in the control of various physiologic, endocrine and emotional response parameters and has been described in detail elsewhere 2, 37, 38, 39, 40. It is based on the following principle. While subjects are watching a short movie on a video screen, eye movements are monitored by an infrared oculometer. To prevent artifacts in eye movement recording, head movements are eliminated by a system of low pressure pads which are adapted to the head. By means of a video board an electronic mask, an empty grey area, is generated and superimposed on parts of the video display. The mask is yoked to the subject’s horizontal eye movements by the voltage output of the oculometer. It moves in a horizontal direction in close correspondence with the subject’s gaze position and always fades out that part of the screen that is centrally represented in the fovea and, additionally, either the right or left VHF. Unilateral activation of the visually stimulated hemisphere is further strengthened by asking subjects to continuously judge the emotional arousal evoked by the film’s contents by means of a manual-motor rating technique served by the contralateral hand.

Subjects were shown two different film strips by means of the aforementioned technique. Each film lasted approximately five minutes and was presented without sound. The first film (Film A) contained depressing, appalling, piteous, and deeply moving scenes from Steven Spielberg’s movie ‘‘Schindler’s List’’ showing the pogrom in Germany. The second movie (Film B) was a scenic film containing non-arousing and peaceful pictures. Both films were selected on the basis of a pilot study [2]examining the film’s effects under central viewing conditions. Presentation of Film A resulted in a clearly higher increase of HF-power compared to a baseline condition than presentation of Film B. Therefore, in the present study, Film A was chosen in the expectation that parasympathetic activity should be more markedly stimulated by this film than by Film B.fn2 Since a strong activation of a specific response parameter is usually a prerequisite to detect hemisphere differences, we expected that hemisphere differences in parasympathetic control of the heart should primarily result from presentation of Film A. Film B, being lower in parasympathetic arousal in the pilot study, served as a control film to answer the question whether intensity of parasympathetic arousal evoked by a filmic stimulus is critical for hemisphere differences to become manifest. Moreover, it should be mentioned that both films clearly differed in their affective contents as assessed in the pilot study, too. Whereas Film A aroused strongly negative emotional responses in the subjects, Film B was experienced as emotionally neutral. Therefore, Film B served the further purpose to decide whether hemisphere differences in parasympathetic control of the heart are secondary to affective stimulation or independent from subjective emotional responses. If hemisphere differences should be observed both for Films A and B, this would indicate that sensory stimulation of the hemispheres with neutral filmic materials is sufficient to activate the hemispheres to such a degree that differences in parasympathetic control mechanisms become evident.

The experiment was carried out in a darkened, electrically, and acoustically shielded room at our neuropsychological laboratory, having a constant temperature and humidity. Control of stimulus presentation and data recording were carried out from an adjoining room. Immediately before the onset of film presentation the oculometer was calibrated and the congruence between mask position and gaze direction was checked. Subsequent to film presentation, the congruence between mask position and gaze direction was checked again to examine whether accuracy of mask positioning had changed during the film period. Moreover, prior to each period of film, presentation baseline values of HRV were assessed. As could be expected for a within subjects design, no baseline differences were obtained for any experimental variable and response measure. Therefore, baseline values were not considered for statistical analysis.

Each subject was shown both films twice, once in his right and once in his left VHF. Between the first and the second presentation of the films, there was a break of 30 min. To control the order of succession, half the subjects were presented with both films first in their left and then in their right VHF, whereas for the other subjects, the order of presentation was reversed. HRV was processed over the whole five-minutes periods of film presentation. Three-factor ANOVAs with the variables ‘‘VHF’’, ‘‘film’’, and ‘‘order’’ and repeated measures on the first two factors, were calculated for each measure of HRV assessed during film presentation. In addition, three-factor ANCOVAs with the covariates ‘‘respiration rate (breath\min)’’ and ‘‘subjective arousal’’ were calculated to control for possible differences in respiration and amount of subjective emotional excitement.

Mean values and standard deviations for the results of power spectral analysis of HRV are illustrated in Table 1. Except for a VHF×Order-interaction effect for LF-power [F(1,43) = 6.60, P = 0.0138] no significant main or interaction effects were found for the variable order of succession. This indicates that starting film presentation with either the left or right VHF has no influence on measured responses.

With respect to the variable film, significant main effects favoring Film B were obtained for the LF range, both when expressed in absolute power values [F (1,43) = 12.30, P = 0.0011] or in normalized units [F (1,43) = 12.69, P = 0.0009]. Total power, too, is significantly higher for Film B [F (1,43) = 5.20, P = 0.0275], being mainly due to differences in the LF-range. With respect to the HF-range significantly higher nHF-power values [F (1,43) = 9.62, P = 0.0030] and a significantly lower L\H-ratio were obtained for Film A. Both differences had been expected because of the results of the pilot study and indicate a higher parasympathetic activation during our experimental Film A.

Clear-cut differences are found for the effects of left- versus right-lateralized film presentation on HRV. Mean values for the HF-range, being of crucial importance for the aims of the present study, are depicted in Fig. 1. There is a significant main effect for HF-power expressed in absolute values with clearly higher power values for film presentation in the right VHF [F (1,43) = 6.66, P = 0.0133]. Normalizing HF-power with respect to total power, too, results in clearly higher nHF-power values with right-sided film presentation, although the VHF-main effect just fails to reach significance [F (1,43) = 3.79, P = 0.0580]. Calculating the LF\HF-ratio, which is another commonly accepted means to account for differences in total power, a highly significant main effect with a lower ratio for right-sided film presentation is obtained [F (1,43) = 7.53, P = 0.0088], supporting the other findings of higher parasympathetic activity during sensory stimulation of the right VHF. With respect to the LF-range, no significant differences are found for absolute LF-power. Yet, a significant main effect is obtained for normalized LF-power [F (1,43) = 4.13, P = 0.0481] with higher values for left-sided film presentation, thus pointing to a probably higher sympathetic influence during stimulation of the left VHF. No significant VHF×Films interaction effects were obtained for any spectral measures.

Since respiration rate is able to influence HRV [43], respiration was also recorded. Respiration rate did not differ between right- and left-sided film presentation [F (1,41) = 0.25, n.s.], but there was a highly significant film-related difference [F (1,41) = 32.92, P = 0.0001]. Mean values were as follows: Film A: L-VHF = 19.31, R-VHF = 19.44; FIlm B: L-VHF = 17.81, R-VHF = 17.89. Therefore, three-factor ANCOVAs with ‘‘respiration rate’’ as a covariate, were calculated, too. Except for the VHF-related main effect for nLF-power and the film-related main effect for LF-power, which disappeared, no other effects were noticeably changed. Therefore, we think that especially the VHF-effects on HF-power are uninfluenced by differences in respiration rate.

It should also be mentioned that none of the main effects reported for the three-factor ANOVAs were significantly changed by ANCOVAs using intensity of subjective arousal as measured by the aforementioned manual-motor rating technique as a covariate to control for possible differences in subjective emotional experiencing.

Summarizing our main findings, the present study suggests that parasympathetic control of the heart is differently influenced by the two hemispheres, at least with respect to chronotropic cardiac activity. Selective sensory stimulation of the left hemisphere results in a clearly higher amount of efferent vagal activity reaching the sinus node than right-hemispheric stimulation. Higher vagal tone during left-hemispheric stimulation is reflected both by measures of absolute power in the HF-range as well as by measures making allowance for differences in total power, such as the LF\HF-ratio and, with some reservation, normalized HF-power. This implicates that the left cerebral hemisphere plays a predominant role in the control of parasympathetic modulation of cardiac activity. Supplementing a prior study of our research group [14], we also found some indications justifying the assumption that during right-hemispheric stimulation the sympathovagal balance is displaced towards the sympathetic branch of the autonomic nervous system. This is mainly supported by the observed differences in nLF-power and in the LF\HF-ratio.

How can the obtained differences in hemispheric control of parasympathetic activity be explained? Since we have used filmic stimuli involving affective contents to accomplish lateralized activation of the hemispheres, we cannot exclude the possibility that the observed differences are, at least, partially due to emotion-related asymmetry favoring processing in one or other hemisphere (see Introduction). If this proves correct, we should expect a significant VHF film-interaction effect with higher differences for the emotionally arousing Film A. Moreover, due to the negative emotional valence of Film A, differences should favor the right hemisphere, being predominantly involved in the processing of negative affect [44]. But, although parasympathetic activity (nHF-power, LF\HF-ratio) had been stimulated significantly stronger by Film A, as had been expected, hemisphere differences were equally high for both films, markedly favoring the left against the right hemisphere. Therefore, we think that the obtained differences in hemispheric control of parasympathetic activity are not due to emotion-related asymmetry. Furthermore, our results demonstrate that sensory stimulation per se, using neutral stimuli, is sufficient to prove hemisphere differences in the control of autonomic activity.

These conclusions are also supported by the findings that none of the obtained differences were significantly changed by using height of subjective arousal during film presentation as a covariate to control for differences in subjective emotional experiencing. Moreover, they are in accord with related findings of previous studies demonstrating unrelatedness between phenomena of emotional and autonomic asymmetry 2, 37, 40.

How are the obtained results related to findings reported in the literature? As has been maintained at the outset, studies using heart rate deceleration as an index of parasympathetic activity cannot be interpreted unequivocally, due to the dual autonomic influence on this measure. Nevertheless, it should be mentioned that especially those studies using sophisticated techniques such as cortical stimulation [24]or hemispheric inactivation [12]to examine lateralized influences on heart rate changes, also suggest a stronger left hemisphere influence on parasympathetic modulation or heart rate. Until now, no studies have been done in healthy subjects using measures of HF-power to examine hemisphere differences in the control of vagal tone. But, there are some clinical studies with conflicting results that have examined the effects of unilateral brain lesions on HRV. In one study [17], a trend was found towards a decrease in nHF-power in seven patients with left insular lesions compared to normal controls, but no comparison had been performed with right insular lesions. No differences between the effects of right-hemispheric and left-hemispheric infarctions on HF-power had been found in a second study [18], although HRV was generally depressed in patients compared to healthy subjects. In two further studies 15, 16, right-hemispheric infarction had either been associated with lower HF-power or with reduced respiratory sinus arrhythmia (RSA), but one study [16]included patients with brain stem lesions, whereas in the other study the HF-band seems to have been defined very narrowly—both matters impeding an unequivocal interpretation of results. In addition, general problems intimately associated with studies on brain damaged patients, are the confounding influences of medication and preexisting heart diseases on HRV, as well as the theoretical uncertainty to decide whether reduced HF-power following unilateral stroke is due to a suppressive effect of stroke on brain areas regulating parasympathetic activity, or to the regularly observed increase in sympathetic activity, reflexively attenuating cardiac vagal effects due to the release of neuropeptide Y from sympathetic nerve endings [3]. Therefore, these studies are not very helpful in supporting or rejecting conclusions drawn from the present study.

Comparing our results with established findings on lateralized parasympathetic control of the heart at the levels of peripheral pathways and medullary regions 3, 5, 10,it becomes obvious that asymmetries observed at the level of the cerebral hemispheres are characterized by different principles than asymmetries reported for lower parts of the neural control system. Control at the level of the peripheral pathways, being immediately involved in the regulation of specific aspects of cardiac activity, is organized according to whether chronotropic or inotropic and dromotropic heart activity is to be influenced. Right-sided structures are mainly responsible for both sympathetic and parasympathetic control of chronotropic activity, whereas left-sided structures mainly control inotropic and dromotropic aspects. On the contrary, the present study shows that at the level of the cerebral hemispheres, modulation of chronotropic parasympathetic activity is under the primary control of the left hemisphere. Whether left-hemispheric predominance of parasympathetic control also extends to other aspects of cardiac activity, is undecided at the moment. But, because heart block and death in asystolic arrest have been observed following left-hemispheric insular cortex stimulation [45], it seems not unlikely that parasympathetic regulation of the heart is entirely under the left hemisphere’s predominant control. This would be in line with recent findings on hemispheric control of sympathetic activity, indicating that the whole spectrum of sympathetic activity including chronotropic and inotropic regulation of the heart as well as effects related to other physiologic systems is under the primary control of the right hemisphere 14, 46, 47.

Therefore, we feel in line with the reasoning of other authors [33]in assuming that control of autonomic activity at the level of the cerebral cortex is most adequately characterized by a division of responsibility between both hemispheres, sympathetic activity being mainly controlled by the right hemisphere and parasympathetic activity being under the left hemisphere’s main control.

From a neuroanatomic perspective, the proposed model of autonomic control would imply a specific pattern of efferent pathways connecting cortical areas involved in autonomic modulation of cardiac activity with postganglionic fibers innervating the heart. Whereas pathways connecting brain stem areas with heart ganglia should predominantly take an ipsilateral route, it should be assumed that cortical areas project bilaterally to brain stem areas involved in autonomic control of the heart. Although knowledge about the precise course of the involved left-sided and right-sided pathways in humans is sparse at present [11], experimental findings from animal studies seem to support our assumption. In general, there is little doubt that descending fibers between higher and lower brain stem areas as well as between brain stem areas and cardiac ganglia take predominantly though not exclusively an ipsilateral route 9, 10, 48, 49. Contrary to this, there are some indications that cortical areas such as the medial frontal and insular cortex which are intimately involved in autonomic modulation of cardiac activity have substantial bilateral projections to brain stem areas being of immediate importance for efferent modulation of sympathetic and parasympathetic outflow 50, 51, 52. Although these findings are in line with the proposed model of cardiac control, it should be kept in mind that our conclusions can only be of a preliminary nature as long as the empirical results of the present study are not confirmed independently by other research groups.

Section snippets

Acknowledgements

Supported by the Maximilian-Bickhoff Foundation. We thank B. Mühle, U. Scherer, B. Schulda, M. Schwarzkopf, U. Weidenhof and R. A. Wittling for assistance and technical advice.

References (52)

  • W Wittling

    Neuropsychologia

    (1990)
  • L.N Shapoval et al.

    Journal of the Autonomic Nervous System

    (1991)
  • V.J Massari et al.

    BrainResearch

    (1995)
  • P.J Gatti et al.

    Journal of the Autonomic Nervous System

    (1996)
  • W Wittling et al.

    Brain

    (1990)
  • W Wittling et al.

    Cortex

    (1993)
  • W Wittling et al.

    Neuropsychologia

    (1993)
  • K Hugdahl

    Current Opinion in Neurobiology

    (1996)
  • S.M Oppenheimer et al.

    Brain Research

    (1991)
  • C.B Saper et al.

    Brain Research

    (1976)
  • M.T Shipley

    Brain Research

    (1982)
  • M.T Shipley et al.

    Brain Research

    (1982)
  • R.R Terreberry et al.

    Brain Research

    (1983)
  • Davidson, R. J. and Hugdahl, K., (Eds). Brain Asymmetry. MIT-Press, Cambridge, MA,...
  • Levy, M. N. and Warner, M. R., Parasympathetic effects of cardiac function. In Neurocardiology, ed. J. A. Armour and J....
  • Randall, W. C., Sympathetic control of the heart. In Neural Regulation of the Heart, ed. W. C. Randall. Oxford...
  • Levy, M. N. and Martin, P. J., Neural control of the heart. In Handbook of Physiology, Sect. 2: The Cardiovascular...
  • H.S Fang et al.

    American Journal of Physiology

    (1962)
  • C.Y Chai et al.

    American Journal of Physiology

    (1962)
  • Lane, R. D. and Jennings, J. R., Hemispheric asymmetry, autonomic asymmetry, and the problem of sudden cardiac death....
  • E.Y Zamrini et al.

    Neurology

    (1990)
  • Hugdahl, K., Classical conditioning and implicit learning: The right hemisphere hypothesis. In Brain Asymmetry, ed. R....
  • Wittling, W., Block, A., Schweiger, E. and Genzel, S., Hemisphere asymmetry in autonomic control of the human...
  • S.A Barron et al.

    Stroke

    (1994)
  • H.K Naver et al.

    Stroke

    (1996)
  • S.M Oppenheimer et al.

    ClinicalAutonomic Research

    (1996)
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