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Identifying heart-brain interactions during internally and externally operative attention using conditional entropy

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Abstract

Heart and brain interactions mediate human cognition. This investigation identifies heart-brain interactions during internally operative attention (AI) and externally operative attention (AE). AI attention involves short term memory, whereas AE attention deals with automatic and transient response to objects in the external world. A modified Posner’s spatial orienting task used to differentiate AI and AE attention. Heart and brain rhythms recorded in fourteen healthy participants. Functional coupling from heart-to-brain (Cheart→brain) and brain-to-heart (Cbrain→heart) time series derived using an information domain approach based on conditional entropy. The experimental results showed that low-frequency power of heart rate variability (HRV-LF) and sympathovagal balance (LF/HF ratio) during AE significantly increased compared with that for AI. Furthermore, the information flow from heart-to-brain increased and decreased form brain-to-heart during AE as compared to AI. Also, opposite trend in relationship noted between coupling index (Ci→j) and HRV-LF during AI and AE attention. The conditional entropy technique enabled simultaneous analysis of heart-brain rhythms to identify heart-brain interactions during AI and AE attention.

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... Recently proposed methods for brain-heart interaction analysis exploit signal processing techniques to uncover these interactions, including inferences on causality and directionality between cortical and cardiac oscillations [7] . State-of-the-art methods of brain-heart interaction include the analysis of heartbeat-contingent responses [8] , convergent cross-mapping [9] , coupling through symbolic representations [10] , time-delay stability [11] , granger causality [12] , transfer entropy [13] , among others. Synthetic Data Generation (SDG) modeling is a framework that aims to gather the bidirectional interactions of EEG and sympathetic-vagal activity [ 4 , 5 ]. ...
... Therefore, by resolving the system of Eqs. (13) and (14) , and are computed as follows: ...
... ., , , , , or ) , during the previous time window ( − 1 ) . Eqs. (12) and (13) present the final computation of the brain-to-sympathetic and brain-to-vagal interplay coefficients C F →CSI and C F →− CVI , respectively. ...
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Recent studies suggest that the interaction between the brain and heart plays a key role in cognitive processes, and measuring these interactions is crucial for understanding the interaction between the central and autonomic nervous systems. However, studying this bidirectional interplay presents methodological challenges, and there is still much room for exploration. This paper presents a new computational method called the Poincaré Sympathetic-Vagal Synthetic Data Generation Model (PSV-SDG) for estimating brain-heart interactions. The PSV-SDG combines EEG and cardiac sympathetic-vagal dynamics to provide time-varying and bidirectional estimators of mutual interplay. The method is grounded in the Poincaré plot, a heart rate variability method to estimate sympathetic-vagal activity that can account for potential non-linearities. This algorithm offers a new approach and computational tool for functional assessment of the interplay between EEG and cardiac sympathetic-vagal activity. The method is implemented in MATLAB under an open-source license.• A new brain-heart interaction modeling approach is proposed.• The modeling is based on coupled synthetic data generators of EEG and heart rate series.• Sympathetic and vagal activities are gathered from Poincaré plot geometry.
... Stress also modulates heartbeat nonlinear dynamics (20,62). Changes in attention have been referred to as a source of autonomic variability (63). Furthermore, some studies have suggested that high-frequency fluctuations in heartbeat dynamics are associated with memory retrieval, reaction time, and action execution (59,64,65), suggesting a dynamic interaction between sympathetic and parasympathetic activities under stress elicitation. ...
... The functional brain-heart interplay under stress elicitation has been shown in heartbeat-evoked potentials correlating with stress-induced changes in cardiac output (22) and correlates of functional connectivity with heart rate variability (31). The role of cardiac inputs in the neurophysiology of stress is also supported by the experimental evidence showing an increased information flow from the heart to the brain during increased attention (63) and disrupted abilities on detecting cardiac and respiratory signals from oneself under anxiety (91,92). ...
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Dynamical information exchange between central and autonomic nervous systems, as referred to functional brain-heart interplay, occurs during emotional and physical arousal. It is well documented that physical and mental stress lead to sympathetic activation. Nevertheless, the role of autonomic inputs in nervous-system-wise communication under mental stress is yet unknown. In this study, we estimated the causal and bidirectional neural modulations between EEG oscillations and peripheral sympathetic and parasympathetic activities using a recently proposed computational framework for a functional brain-heart interplay assessment, namely the sympathovagal synthetic data generation model. Mental stress was elicited in 37 healthy volunteers by increasing their cognitive demands throughout three tasks associated with increased stress levels. Stress elicitation induced an increased variability in sympathovagal markers, as well as increased variability in the directional brain-heart interplay. The observed heart-to-brain interplay was primarily from sympathetic activity targeting a wide range of EEG oscillations, whereas variability in the efferent direction seemed mainly related to EEG oscillations in the gamma band. These findings extend current knowledge on stress physiology, which mainly referred to top-down neural dynamics. Our results suggest that mental stress may not cause an increase in sympathetic activity exclusively as it initiates a dynamic fluctuation within brain-body networks including bidirectional interactions at a brain-heart level. We conclude that directional brain-heart interplay measurements may provide suitable biomarkers for a quantitative stress assessment and bodily feedback may modulate the perceived stress caused by increased cognitive demand.
... More recently, stress showed changes in heart-rate's non-linear dynamics [48], indicating more complex dynamics, beyond an increase or decrease of autonomic nervous system activities. These autonomic variations have been reported as well to be associated with fluctuations in attention [49]. High frequency activity is associated with memory retrieval, as it correlated with performance and reaction times [50,51]. ...
... It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted September 10, 2022. ; https://doi.org/10.1101/2022.09.09.507362 doi: bioRxiv preprint the neurophysiology of stress is also supported by the experimental evidence showing an increased information flow from heart-to-brain during increased attention [49] and disrupted abilities on detecting cardiac and respiratory signals from oneself under anxiety [65,66]. ...
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Previous endeavors have revealed how the dynamical information exchange between central and autonomous nervous systems, as measured from brain–heart interplay, can explain emotional arousal and physical stress. In this study, we test our recently proposed computational framework for a functional brain–heart interplay assessment; the Sympatho-Vagal Synthetic Data Generation Model. The model estimates the causal and bidirectional neural modulations between EEG oscillations and sympathetic/parasympathetic activity. Here, mental stress is elicited by increasing the cognitive demand and quantified on 37 human volunteers. The increase on mental stress induced an increased variability on heart–to–brain functional interplay, primarily from sympathetic activity on EEG oscillations in the delta and beta bands. Existing theoretical and experimental evidence has shown that stress involves top-down neural dynamics in the brain. Therefore, our results show that mental stress involves dynamic and bidirectional neural interactions at a brain–body level as well, where bodily feedback shapes the perceived stress caused by an increased cognitive demand. We conclude that brain–heart interplay estimators are suitable biomarkers for stress measurements. Highlights We tested a model to assess brain–heart interplay under mental stress elicitation. The model revealed that stress levels are reflected in heart–to–brain variability. Interplay from sympathetic to delta and beta waves are the best markers for stress.
... The early-stage detection of cardiac arrhythmia is of prime importance [1]. But during the acquisition of ECG data, different types of noise gets involved, which hide its important characteristics that mislead its analysis and introduces the non-linearity [38,39]. Analysis of this nonlinear signal requires automated analysis as provided by computer-aided diagnosis (CAD). ...
... In this paper, 12 real-time recordings (RT DB) were also used to establish the performance of the proposed methodology in a practical scenario. The use of two databases in this paper is in line with other studies in the existing literature that made use of variety of databases for validating their work [39,[72][73][74][75]. ...
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... A normalized version of the TE, estimated via non-uniform embedding [116] between the time series of HRV and EEG complexity, was employed as well by Yu and colleagues [118], who revealed the existence of unidirectional effects of the cardiac period length on the irregularity of the brain waves in the resting and mental stress states. A similar approach was employed to distinguish between physiological changes induced by internally-driven attention, linked with short-term memory assessment, and externallydriven attention, associated with automatic and transient responses to external stimuli; the findings revealed that heartto-brain information flow increased, while the brain-to-heart flow decreased, during externally-driven attention compared to internally-driven attention [119]. ...
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The exploration of brain-heart interactions within various paradigms, including affective computing, human-computer interfaces, and sensorimotor evaluation, stands as a significant milestone in biomarker development and neuroscientific research. A range of techniques, spanning from molecular to behavioral approaches, has been proposed to measure these interactions. Different frameworks use signal processing techniques, from the estimation of brain responses to individual heartbeats to higher-order dynamics linking cardiac inputs to changes in brain organization. This review provides an overview to the most notable signal processing strategies currently used for measuring and modeling brain-heart interactions. It discusses their usability and highlights the main challenges that need to be addressed for future methodological developments. Current methodologies have deepened our understanding of the impact of neural disruptions on brain-heart interactions, solidifying it as a biomarker for evaluation of the physiological state of the nervous system and holding immense potential for disease stratification. The vast outlook of these methods becomes apparent specially in neurological and psychiatric disorders. As we tackle new methodological challenges, gaining a more profound understanding of how these interactions operate, we anticipate further insights into the role of peripheral neurons and the environmental input from the rest of the body in shaping brain functioning.
... State-of-the-art methods of brain-heart interaction include the analysis of heartbeat-contingent responses [8], convergent cross-mapping [9], coupling through symbolic representations [10], timedelay stability [11], granger causality [12], transfer entropy [13], among others. Synthetic Data Generation (SDG) modeling is a framework that aims to gather the bidirectional interactions of EEG and sympathetic-vagal activity [4,5]. ...
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Recent studies on brain-heart interaction suggest a functional involvement of such interaction in cognitive processes. Proposals on brain-heart interaction analysis aim at understanding the information exchange between two dynamic systems. Because of methodological challenges, studying the functional value of the bidirectional interplay between central and autonomous nervous systems still has space for further exploration. Here, I introduce a new computational method to estimate brain-heart interactions, the Poincaré Sympathetic-Vagal Synthetic Data Generation Model (PSV-SDG). The PSV-SDG combines EEG and cardiac sympathetic-vagal dynamics to gather time-varying and bidirectional estimators of mutual interplay. The method is grounded on the Poincaré plot, an acknowledged heart rate variability method to estimate sympathetic-vagal activity, accounting for potential non-linearities. The proposed algorithm represents a new method and computational tool for the functional assessment of the interplay between EEG and cardiac sympathetic-vagal activity. The proposed method is implemented in MATLAB under an open-source license.
... For the next step, the sample size should be increased in order to acquire more robust data for statistical analysis. Even though, the sample size is small, it is reasonably enough to do the analysis for the physiological measurements [19,[44][45][46][47]. Also, in the future, more consideration regarding timing could be investigated. ...
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Previous studies have shown that EEG activity in the gamma range can be modulated by attention. Here, we compared this activity for voluntary and involuntary spatial attention in a spatial-cueing paradigm with faces as targets. The stimuli and trial timing were kept constant across attention conditions with only the predictive value of the cue changing. Gamma-band response was linked to voluntary shifts of attention, but not to the involuntary capture of attention. The presence of increased gamma responses for the voluntary allocation of attention, and its absence in cases of involuntary capture suggests that the neural mechanisms governing these two types of attention are different. Moreover, these data allow a description of the temporal dynamics contributing to the dissociation between voluntary and involuntary attention. The distribution of this correlate of voluntary attention is consistent with a top-down process involving contralateral anterior and posterior regions.
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This study employed a paired stimulus paradigm to compare phasic changes in heart rate among children (age categories 6-8, 9-10, and 11-12) and adults (age categories 18-19 and 20-22) with attention-deficit/hyperactivity disorder (ADHD) and age-matched controls. A sample of 95 participants (19 ADHD-diagnosed children, 34 controls, 20 ADHD-diagnosed adults, and 22 controls) solved a planning task, the Tower of London, through 4 levels of difficulty. It was hypothesized that groups with ADHD would show greater heart rate acceleration and less final deceleration than would controls, and that these heart rate responses would change with age and difficulty level as well. Though heart rate differences were found among age categories and difficulty levels, none were found between participants with ADHD and controls. The lack of ADHD differences are not consistent with the behavioral evidence that planning by itself is one of the marked executive function deficits in ADHD. Because ADHD differences were not evident, the effects either were not present or were smaller than that of difficulty level and age. Possible explanations for this lack of difference and future directions are discussed.
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This work assessed the influence of the autoregressive model order (ARMO) on the spectral analysis of the heart rate variability (HRV). A sample of 68 R-R series obtained from digital ECG records of young healthy adults in the supine position was used. Normalized spectral indexes for each ARMO were compared by Friedman test followed by the Dunn's procedure and statistical significance was set at P<0.05. The results showed that the AR method using orders from 9 to 25 produces normalized spectral parameters statistically similar and, hence, the algorithms commonly employed to estimate optimum order are not mandatory in this case.
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The complexity of the short-term cardiovascular control prompts for the introduction of multivariate (MV) nonlinear time series analysis methods to assess directional interactions reflecting the underlying regulatory mechanisms. This study introduces a new approach for the detection of nonlinear Granger causality in MV time series, based on embedding the series by a sequential, non-uniform procedure, and on estimating the information flow from one series to another by means of the corrected conditional entropy. The approach is validated on short realizations of linear stochastic and nonlinear deterministic processes, and then evaluated on heart period, systolic arterial pressure and respiration variability series measured from healthy humans in the resting supine position and in the upright position after head-up tilt.
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Recent studies applying functional magnetic resonance imaging have focused on the description of cerebral substrates of changes in cardiac function during diverse autonomic maneuvers or stressful cognitive tasks. These studies might be limited by the indistinguishable neuronal activity due to cognitive processes, which are known to influence autonomic function, and the 'baseline' activity in the central autonomic network. We therefore investigated 26 healthy volunteers in the magnetic resonance scanner to simultaneously obtain functional brain images and RR intervals (intervals between ventricular depolarizations) of the high-resolution electrocardiogram. The mean RR interval length within each functional scan was computed, which was finally convolved with the canonical hemodynamic response function to obtain a regressor for the functional time series. The resulting individual contrast image indicated a positive covariation of the blood oxygen level-dependent signal and RR interval length in the ventromedial prefrontal cortex (vmPFC). Furthermore, a reduced mean cross-approximate entropy value was shown for the interaction between the vmPFC and individual RR intervals. This suggests reduced asynchrony between the heart rate and vmPFC activity in contrast to other brain areas. Our findings confirm data obtained in animals describing the vmPFC as an important forebrain structure of the central autonomic network and an influence of the vmPFC in the cortical generation of efferent vagal activity. This finding needs to be investigated in diseases with known suppression of efferent vagal modulation.
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In the present paper, we describe a model of neurovisceral integration in which a set of neural structures involved in cognitive, affective, and autonomic regulation are related to heart rate variability (HRV) and cognitive performance. We detail the pathways involved in the neural regulation of the cardiovascular system and provide pharmacological and neuroimaging data in support of the neural structures linking the central nervous system to HRV in humans. We review a number of studies from our group showing that individual differences in HRV are related to performance on tasks associated with executive function and prefrontal cortical activity. These studies include comparisons of executive- and nonexecutive-function tasks in healthy participants, in both threatening and nonthreatening conditions. In addition, we show that manipulating resting HRV levels is associated with changes in performance on executive-function tasks. We also examine the relationship between HRV and cognitive performance in ecologically valid situations using a police shooting simulation and a naval navigation simulation. Finally, we review our studies in anxiety patients, as well as studies examining psychopathy. These findings in total suggest an important relationship among cognitive performance, HRV, and prefrontal neural function that has important implications for both physical and mental health. Future studies are needed to determine exactly which executive functions are associated with individual differences in HRV in a wider range of situations and populations.
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The cerebral cortex had massive bidirectional connections to autonomic nervous system and mental performance can induce change of autonomic activity, but which regions are related to autonomic function is not clear. The study was to analyze the scalp positions which may affect cardiac autonomic nervous activity during a mental arithmetic (MA) task. Forty-three healthy male subjects were voluntarily participated in the study. Sympathetic and parasympathetic activities were estimated with heart rate variability. Scalp potential was determined by the wavelet packet parameters and approximate entropy (ApEn) of Electroencephalogram (EEG). The results showed that heart rate and the normalized low frequency power component were significantly increased (p<0.01) and the high frequency power component was decreased (p<0.01). Meanwhile relative wavelet packet energy in alpha band of EEG at P3, P4, Pz, O1, O2 and Oz electrodes were decreased and the beta band of EEG at the same electrodes were increased significantly (p<0.01). ApEn was significantly increased in MA (p<0.01). Moreover, changes of brain activity were earlier than the changes of autonomic activity and significantly correlations existed between heart rate variability and wavelet packet energy (p<0.05). In addition, a significant positive correlation between HR change and the laterality ratio score of alpha band in P3 v P4 (p<0.05) were observed. It is noted that cerebral conscious activity enhanced with the decrease of parasympathetic activity and increase of sympathetic activity, and the right post-central areas dominated sympathetic activity during stress-inducing mental tasks.
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The neural regulation of circulatory function is mainly effected through the interplay of the sympathetic and vagal outflows. This interaction can be explored by assessing cardiovascular rhythmicity with appropriate spectral methodologies. Spectral analysis of cardiovascular signal variability, and in particular of RR period (heart rate variability, HRV), is a widely used procedure to investigate autonomic cardiovascular control and/or target function impairment. The oscillatory pattern which characterizes the spectral profile of heart rate and arterial pressure short-term variability consists of two major components, at low (LF, 0.04-0.15Hz) and high (HF, synchronous with respiratory rate) frequency, respectively, related to vasomotor and respiratory activity. With this procedure the state of sympathovagal balance modulating sinus node pacemaker activity can be quantified in a variety of physiological and pathophysiological conditions. Changes in sympathovagal balance can be often detected in basal conditions, however a reduced responsiveness to an excitatory stimulus is the most common feature that characterizes numerous pathophysiological states. Moreover the attenuation of an oscillatory pattern or its impaired responsiveness to a given stimulus can also reflect an altered target function and thus can furnish interesting prognostic markers. The dynamic assessment of these autonomic changes may provide crucial diagnostic, therapeutic and prognostic information, not only in relation to cardiovascular, but also non-cardiovascular disease. As linear methodologies fail to provide significant information in conditions of extremely reduced variability (e.g. strenuous exercise, heart failure) and in presence of rapid and transients changes or coactivation of the two branches of autonomic nervous system, the development of new non-linear approaches seems to provide a new perspective in investigating neural control of cardiovascular system.
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In recent years, several attempts have been made to characterize the nature of the cognitive deficits shown by patients with Parkinson's disease. It has been suggested variously that they have difficulty in switching cognitive set, in performing effortful (or controlled) as opposed to automatic tasks, or that their impairment is found in tasks which maximize the amount of 'self-directed task specific planning'. It is proposed that this latter distinction may be reformulated in terms of the degree of internal versus external attentional control which is required by the task. An experiment is described which attempted to manipulate this parameter. A version of the Stroop colour-word test was used, in which the words 'red' and 'green' were presented in the complementary coloured 'ink'. Subjects responded either to the colour of the ink in which the word was written or the colour named by the word. The relevant attribute changed at intervals during the course of the experiment. In one condition, the relevant stimulus attribute was cued before each trial. In another condition, subjects had to remember which attribute was currently relevant. Results revealed that patients with Parkinson's disease were impaired mainly on the second version of the task which required internal attentional control. The results are discussed in relation to the models of Working Memory (Baddeley, 1986), and attentional control (Norman and Shallice, 1980). Exploration of these models leads to the formulation of a theory in which the crucial determinant of cognitive impairment in Parkinson's disease is reduced resources in the Supervisory Attentional System. Provided the demands of the task are within the patient's available attentional resources the patient may not show any deficit. If, however, the attentional demands exceed available resources, as in tasks which depend upon internal cues, then deficits will be observed.
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In the present paper we present the outlines of a model that integrates autonomic, attentional, and affective systems into a functional and structural network that may help to guide us in our understanding of emotion regulation and dysregulation. We will emphasize the relationship between attentional regulation and affective processes and propose a group of underlying physiological systems that serve to integrate these functions in the service of self-regulation and adaptability of the organism. We will attempt to place this network in the context of dynamical systems models which involve feedback and feedforward circuits with special attention to negative feedback mechanisms, inhibitory processes, and their role in response selection. From a systems perspective, inhibitory processes can be viewed as negative feedback circuits that allow for the interruption of ongoing behavior and the re-deployment of resources to other tasks. When these negative feedback mechanisms are compromised, positive feedback loops may develop as a result (of dis-inhibition). From this perspective, the relative sympathetic activation seen in anxiety disorders may represent dis-inhibition due to faulty inhibitory mechanisms.
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Techniques to determine changing system complexity from data are evaluated. Convergence of a frequently used correlation dimension algorithm to a finite value does not necessarily imply an underlying deterministic model or chaos. Analysis of a recently developed family of formulas and statistics, approximate entropy (ApEn), suggests that ApEn can classify complex systems, given at least 1000 data values in diverse settings that include both deterministic chaotic and stochastic processes. The capability to discern changing complexity from such a relatively small amount of data holds promise for applications of ApEn in a variety of contexts.
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The aim of the present study was to investigate the effect of vagal tone on performance during executive and non-executive tasks, using a working memory and a sustained attention test. Reactivity to cognitive tasks was also investigated using heart rate (HR) and heart rate variability (HRV). Fifty-three male sailors from the Royal Norwegian Navy participated in this study. Inter-beat-intervals were recorded continuously for 5 min of baseline, followed by randomized presentation of a working memory test (WMT) based on Baddeley and Hitch's research (1974) and a continuous performance test (CPT). The session ended with a 5-min recovery period. High HRV and low HRV groups were formed based on a median split of the root mean squared successive differences during baseline. The results showed that the high HRV group showed more correct responses than the low HRV group on the WMT. Furthermore, the high HRV group showed faster mean reaction time (mRT), more correct responses and less error, than the low HRV group on the CPT. Follow-up analysis revealed that this was evident only for components of the CPT where executive functions were involved. The analyses of reactivity showed a suppression of HRV and an increase in HR during presentation of cognitive tasks compared to recovery. This was evident for both groups. The present results indicated that high HRV was associated with better performance on tasks involving executive function.
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Sensory processing is affected by both endogenous and exogenous mechanisms of attention, although how these mechanisms interact in the brain has remained unclear. In the present study, we recorded event-related potentials (ERPs) to investigate how multiple stages of information processing in the brain are affected when endogenous and exogenous mechanisms are concurrently engaged. We found that the earliest stage of cortical visual processing, the striate-cortex-generated C1, was immune to attentional modulation, even when endogenous and exogenous attention converged on a common location. The earliest stage of processing to be affected in this experiment was the late phase of the extrastriate-cortex-generated P1 component, which was dominated by exogenous attention. Processing at this stage was enhanced by exogenous attention, regardless of where endogenous attention had been oriented. Endogenous attention, however, dominated a later, higher-order stage of processing indexed by an enhancement of the P300 that was unaffected by exogenous attention. Critically, between these early and late stages, an interaction was found wherein endogenous and exogenous attention produced distinct, and overlapping, effects on information processing. At the same time that exogenous attention was producing an extended enhancement of the late-P1, endogenous attention was enhancing the occipital-parietal N1 component. These results provide neurophysiological support for theories suggesting that endogenous and exogenous mechanisms represent two attention systems that can affect information processing in the brain in distinct ways. Furthermore, these data provide new evidence regarding the precise stages of neural processing that are, and are not, affected when endogenous and exogenous attentions interact.
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Do voluntary (endogenous) and involuntary (exogenous) attention have the same perceptual consequences? Here we used fMRI to examine activity in the fusiform face area (FFA--a region in ventral visual cortex responsive to faces) and frontal-parietal areas (dorsal regions involved in spatial attention) under voluntary and involuntary spatial cueing conditions. The trial and stimulus parameters were identical for both cueing conditions. However, the cue predicted the location of an upcoming target face in the voluntary condition but was nonpredictive in the involuntary condition. The predictable cue condition led to increased activity in the FFA compared to the nonpredictable cue condition. These results show that voluntary attention leads to more activity in areas of the brain associated with face processing than involuntary attention, and they are consistent with differential behavioral effects of attention on recognition-related processes.
Article
We propose that voluntary and involuntary attention affect different mechanisms and have different consequences for performance measured in reaction time. Voluntary attention enhances the perceptual representation whereas involuntary attention affects the tendency to respond to stimuli in one location or another. In a spatial-cueing paradigm, we manipulated perceptual difficulty and compared voluntary and involuntary attention. For the voluntary-attention condition, the spatial cue was predictive of the target location, whereas in the involuntary-attention condition it was not. Increasing perceptual difficulty increased the attention effect with voluntary attention, but decreased it with involuntary attention. Thus voluntary and involuntary attention have different consequences when perceptual difficulty is manipulated and hence are probably caused by different mechanisms.