Elsevier

Cognition

Volume 196, March 2020, 104149
Cognition

Brief article
Active sampling in visual search is coupled to the cardiac cycle

https://doi.org/10.1016/j.cognition.2019.104149Get rights and content

Abstract

Recent research has demonstrated that perception and reasoning vary according to the phase of internal bodily signals such as heartbeat. This has been shown by locking the presentation of sensory events to distinct phases of the cardiac cycle. However, task-relevant information is not usually encountered in such a phase-locked manner nor passively accessed, but rather actively sampled at one's own pace. Moreover, if the phase of the cardiac cycle is an important modulator of perception and cognition, as previously proposed, then the way in which we actively sample the world should be similarly modulated by the phase of the cardiac cycle. Here we tested this by coregistration of eye movements and heartbeat signals while participants freely compared differences between two visual arrays. Across three different analyses, we found a significant coupling of saccades, subsequent fixations, and blinks with the cardiac cycle. More eye movements were generated during the systolic phase of the cardiac cycle, which has been reported as the period of maximal effect of the baroreceptors' activity upon cognition. Conversely, more fixations were found during the diastole phase (quiescent baroreceptors). Lastly, more blinks were generated in the later period of the cardiac cycle. These results suggest that interoceptive and exteroceptive processing do adjust to each other; in our case, by sampling the outer environment during quiescent periods of the inner organism.

Introduction

Interoception refers to the set of physiological and cognitive processes that are involved in determining the physiological condition of the body (Craig, 2002). It can be distinguished from the domains of exteroception (processing of the environment) and proprioception (the position of the body in space) as a distinct sensory domain. Recently, research studying interoception has markedly increased (Khalsa et al., 2018; Khalsa & Lapidus, 2016). There are at least two motivations for this renewed interest: establishing the extent to which interoception contributes to cognition in the neurotypical brain and assessing the clinical impact of atypical interoception.

The primary physiological focus of most studies on interoception is the cardiovascular system. In a single heartbeat/cardiac cycle two main phases are observed. In the systolic phase the heart contracts and ejects the blood, whereas in the diastole phase the heart expands while being filled. Both phases comprise a whole heartbeat, with the R-peak (peak in electrocardiogram depicting the contraction at systole) indicating the start of a new heartbeat. Since early evidence of a modulatory effect of the carotid sinus in both autonomous and central nervous system (Koch, 1932; Kreindler, 1946), research in humans have shown that participants' response to stimuli changes according to the phase of the heartbeat in which the information is presented (Azevedo, Badoud, & Tsakiris, 2017; Critchley & Garfinkel, 2018; Salomon et al., 2016). For instance, in the sensorimotor domain, processing information during systole has been associated to the reduction of sensitivity towards pain, visual, and auditory stimuli (Edwards, Ring, McIntyre, & Carroll, 2001; Edwards, Ring, McIntyre, Carroll, & Martin, 2007; McIntyre, Edwards, Ring, Parvin, & Carroll, 2006; Pramme, Larra, Schächinger, & Frings, 2014). Cardiac afferent signals seem to play an important role in the interaction of the heart-brain axis, moderating cognitive processes, competing for the allocation of attentional and representational resources, and dampening/enhancing sensory processing (Critchley & Garfinkel, 2018; Critchley & Harrison, 2013; Khalsa et al., 2018; Seth, 2013).

The demonstrations that perception and cognition are modulated as a function of the cardiac cycle have been achieved by deliberately time-locking the presentation of stimuli to the participants during diastole or systole phases. However, in our everyday experiences sensory information is not presented phase-locked to the cardiac cycle. Therefore, although of considerable interest, it is unclear how these findings impact on our cognition outside of the laboratory setting. If the phase of the cardiac cycle is an important modulator of perception and cognition, as previously proposed, then the way in which we freely and actively sample the world should be similarly modulated by the phase of the cardiac cycle. The current study was designed to test this hypothesis. To our knowledge only two studies have recently started to examine this. Ohl et al., (2016) reported the generation of involuntary phase-locked microsaccades to the systolic phase of the cardiac cycle. Similarly, Kunzendorf et al., (2019) reported the generation of more keypresses, which led to the onset of images to-be-sampled, during the systolic phase. Here we tested the hypothesis that the timing of eye movements in a free visual search task would be modulated during the different phases of the cardiac cycle. We hypothesized that the generation of more phase-locked eye movements (saccades) during systole and the opposite pattern (absence of eye movements; fixations) during diastole; i.e., we tested whether or not the timing of eye movements in a free visual search task would be modulated by the phases of the cardiac cycle. To this end, we coregistered oculomotor behaviour and electrocardiogram (ECG) while human participants performed a visual search task comparable to ‘spot the difference’. Specifically, we recorded the position of the eyes to detect saccades, fixations, and blinks while participants compared differences in colouration between two bilateral arrays (Fig. 1a). For each heartbeat, we computed the point at the phase of the cardiac cycle in which each oculomotor event occurred. The prediction was that if participants' behaviour is modulated by their cardiac signals, the eye movements generated during the present free visual task would reflect this (more saccades, fixations, and blinks occurring consistently in particular phases of the cardiac cycle).

Section snippets

Participants

32 healthy adults participated (24 females; age range = 18–39). All participants reported both normal or corrected-to-normal vision and normal cardiac condition. All subjects gave informed consent, were reimbursed for the participation, and volunteer to take part in the experiment. Ethical approval for the methods/procedures was obtained from the UCL research ethics committee.

Task and procedure

Participants received instructions and completed two practice trials. Next, they completed 5 blocks of 20 trials while

Data analysis

To examine whether or not there was a significant statistical relationship between the saccades, fixations, blinks, and the phase of the cardiac cycle, we calculated the phase of these oculomotor events as a function of the R-R interval (see e.g., Kunzendorf et al., 2019). Circular statistics were employed in order to exploit the iterating nature of the cardiac cycle. For each oculomotor event, the time of the preceding and subsequent R-peak were calculated. Then, the phase of the generated

Descriptive results

The mean number of computed heartbeats across the experiment was 1211, SD = ±315.3. The mean heart rate of the participants was 72 bpm; 834 ms from R to R peak, SD = ±145 ms. The removal of oculomotor events in noisy sections of the ECG (see Methods) comprised 7% of the total number of events. After removal of noisy sections of the ECG, the average number of saccades and fixations computed was 3109.8, SD = ±750. The average number of blinks was 109.3, SD = ±118.1. The average duration of the

Discussion

The effect of the cardiac cycle upon cognition has been observed by meticulously time-locking the presentation of information to each cardiac phase (Azevedo, Garfinkel, et al., 2017; Garfinkel et al., 2014; Park et al., 2017). Here we foster a more ecological framework in which participants may ‘take in’ information at their own pace according to cardiac signalling. To examine this, we allowed participants to freely sample task-relevant visual information while recording their oculomotor

Conclusions

By coregistration of eye movements and ECG, we found statistical evidence for a significant coupling of oculomotor behaviour with the heartbeat. Our results highlight the role of phasic changes within the cardiac cycle, and potentially, the cardioballistic ejection of the blood across the body, in modulating behaviour. More saccades were generated during the systolic phase and the concurrent upstroke of cardiac signalling. Contrary to this, fixations were more phase-locked to the quiescent

CRediT authorship contribution statement

Alejandro Galvez-Pol:Conceptualization, Investigation, Methodology, Software, Formal analysis, Visualization, Writing - original draft, Writing - review & editing.Ruth McConnell:Investigation, Validation, Visualization.James M. Kilner:Conceptualization, Methodology, Software, Formal analysis, Visualization, Writing - review & editing, Project administration, Funding acquisition.

Declaration of competing interest

The authors declare no competing financial interests.

Acknowledgments

We would like to thank all those who participated in and helped to advance this study. This research was supported by the Leverhulme Trust – Grant code RPG-2016-120, United Kingdom.

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