The development of human high-order cognitive processes and neuropsychological functioning are closely linked with two opposing physiological mechanisms that constitute a model of sleep-wake regulation (1): sleep homeostatic pressure and circadian rhythms (2). Here, we focus on how differences in circadian rhythm patterns and time of day influence performance on tasks that require automatic and controlled processing.
Human circadian rhythms are physiologically driven by a central pacemaker that is the suprachiasmatic nuclei (SCN) (3) and connects the organism with the 24-hour period of a day on Earth. Nevertheless, circadian functioning can be variable between individuals. Thus, we refer to the existence of different chronotypes, that is, the preferences that individuals develop for performing their daily life activities and resting earlier or later in the day (4, 5). The assessment of chronotype allows individuals to be classified into different circadian profiles that are distributed along a Gaussian curve at the population level. Intermediate-types (i.e., those who do not develop any specific circadian preference), would be located around the centre, while morning-types (i.e., those who prefer to engage in their routines in the early morning hours) and evening-types (i.e., those with a more later-day profile) occupy the extremes of the curve (6).
The study of chronotype has become interesting since the continuous development of society has forced individuals not to rely on a 24-hour diurnal cycle. For instance, when a doctor must operate at 3 AM in an emergency, a student must plan her or his study schedule for exams, or an air traffic controller must stand guard at her or his post from 5 AM, the consideration of chronotypes and how they operate can predict success. Recently, this trait has been linked to aspects of mental health (7), effects of shift work (8), and school performance (9).
Delving into the cognitive level, processes involving the prefrontal cortex have been shown to be directly related to chronotype and time-of-day, usually showing an enhancement of performance at the time of day that matches the individual’s preference (optimal time). This effect is known as the synchrony effect and has been reflected in a variety of cognitive tasks (for a review, see 10). Nevertheless, the synchrony effect is often not the same for morning- and evening-types. In contrast to evening-types, morning-types have shown better adjustment and flexibility at non-optimal times (11–13). It has been argued that personality traits such as impulsivity (14) and even hormonal secretions during the menstrual cycle in women (13) are linked to these chronotype-based differences. Furthermore, morning- and evening-types have shown differences in the neural networks activated in response to certain cognitive demands such as conflict resolution or cognitive control (15).
The results obtained both at the behavioural and physiological levels related to the prefrontal cortex and the time-of-day in general have led researchers to argue that all mental operations that require control are more vulnerable to the time of testing than those that are more automatic in nature (11, 16, 17). Automatic and controlled processes refer to the differential modes of processing information of our environment that result in an appropriate response (18). It has commonly been argued that controlled processing is the more adaptive since it prevents responses that may have important negative consequences (19), although the need for automatic processing and the importance of not overcontrolling in certain circumstances have also been highlighted (20).
In relation to people’s preferences for when to perform daily life activities, it is controlled rather than automatic processing that seems to fluctuate throughout the day. For instance, (21) showed that the decrease in performance typically observed in vigilance tasks occurred specifically when controlled processing was necessary, while decrements in vigilance performance were not observed when automatic processing was involved. Thus, using the Sustained Attention to Response Task (SART), (16) found differential effects due to the time of testing only in no-go trials, which required cognitive control and therefore controlled processing. In addition, (11) manipulated two response strategies while participants performed the SART: speed (automatic responding set) vs. accuracy (controlled responding set). Selective synchrony effects were found only when focused on accuracy. Finally, regarding memory, (17), and (22) found a pattern of increased explicit recall (controlled retrieval) at the optimal time of day for both the morning- and evening-types. However, although automatic and controlled processes have previously been linked to chronotype and time-of-day, to our knowledge, studies that have addressed the emergence and time course of both types of processing in relation to circadian rhythms in a single task are rather scarce.
In the current study, we approached this issue through the use of a paradigm commonly used to dissociate the involvement of automatic and controlled processing: the semantic priming paradigm. In this paradigm, a prime stimulus (e.g., a word) is briefly presented and followed by a target stimulus that requires a quick response by the participant. The target can be a word or a pseudoword if a lexical decision is needed. The semantic priming effect refers to the advantage in responding (shorter reaction times and better accuracy) in related prime-target trials (e.g., DOCTOR – nurse) compared to unrelated prime-target trials (e.g., DOCTOR – bread) (23–25). Although a discussion of the different models that account for the semantic priming effect is beyond the scope of the present study, semantic priming has been thought to involve the rapid activation of semantic information conveyed by the prime, which spreads to other associated words among which would be the associated target (26). Once the prime has been processed, participants may also consciously generate expectancies about candidate targets in a controlled manner; however, these expectancies require time to build up, and therefore they may only occur if there is enough time between the prime and the target onsets (27). Thus, the prime-target onset asynchrony (usually referred to as prime-target SOA) is crucial for determining whether semantic processing is mainly due to automatic or controlled processing (24), with the former being better captured with short prime-target SOAs and the latter with long prime-target SOAs (e.g., longer than 200 ms), (28). Semantic priming studies usually reveal facilitation in target responses when only the prime-target SOA is manipulated to engage either automatic or controlled semantic processing. Additionally, in relation to prime processing, the use of a mask after its presentation has proven to influence automatic and controlled processes in semantic priming tasks. The immediate appearance of a mask fosters processing of the prime in a strategy-free automatic way, whereas the delayed appearance of the mask allows the use of strategies after processing the prime and guides the individual to act in a more controlled manner (29, 30).
However, a more appropriate way of dissociating the involvement of automatic and controlled processing in a semantic priming task is to find qualitatively different patterns of results associated with each type of process (30). Whereas the use of associative links between the prime and the target usually produces facilitatory priming effects, both facilitatory and inhibitory effects can be found with category semantic priming tasks when both the relatedness proportion and the prime-target SOA are manipulated (24, 31). Facilitatory priming refers to the advantage in performance with related prime-target trials than with unrelated prime-target trials, and the other way around for inhibitory priming. In the category semantic priming task, the prime is the name of a category (e.g., ANIMAL), and the target can be either an exemplar of the prime category (e.g., cat) in the related condition or an exemplar of a different category (e.g., table) in the unrelated condition. Participants will create expectations about the forthcoming target on the basis of the frequency with which a related target follows a prime category and on the interval between the prime and the target (25). With a low rate of related targets, expectations based on the prime category will favour unrelated targets. Thus, the observation of shorter reaction times (RTs) with unrelated compared to related targets (inhibitory priming) will confirm that an expectation has been successfully generated. In contrast, any facilitatory effect despite the low rate of related targets will confirm that expectations were not developed; therefore, facilitatory priming would simply reflect the intervention of automatic processing. By using this paradigm, (32) showed facilitatory priming effects with 200- and 300-ms prime-target SOAs, whereas the effect became inhibitory with a 500-ms SOA. Using a similar design with young participants, (33) found a facilitatory priming effect only with a 100-ms SOA and inhibitory priming effects with 200- 500- and 800-ms SOAs, effects being larger as the SOA value increased.
In the current study, we employed a category semantic priming task in which the name of a semantic category served as the prime stimulus and was followed by either a related or an unrelated target exemplar. A low rate of related targets (20%) was used to promote expectancy-based priming effects, and a short prime-target SOA and long prime-target SOAs were used in different blocks of trials to assess the emergence and time course of facilitatory (automatic) priming and inhibitory (controlled) priming effects, respectively. Experiment 1 involved intermediate chronotype participants, who are not usually considered in chronotype-related studies despite representing 60% of the population (6). This experiment allowed us to test the suitability of this category semantic priming task to dissociate the two types of processes. In Experiment 2, morning-type and evening-type participants, who combined represent the 40% of the population and are referred to as extreme chronotypes, performed the task to assess whether chronotype and time of testing are crucial factors that modulate the earlier appearance of automatic processing and the later emergence of controlled processing. To ensure the appropriate selection of our sample of extreme chronotypes, we used the psychomotor vigilance task (PVT). This task has been shown to be very sensitive to circadian-related performance (34) and has been widely used in cognitive research (11, 12, 35, 36). To assess the effects of chronotype and time of testing on automatic processing, we explored facilitatory priming with a short prime-target SOA (100 ms). Moreover, when appropriate, the time course of automatic processing was addressed based on the division of a 100-ms SOA block in three consecutive subblocks. That division has not been usually done in previous related studies, however, is of special relevance here because participants performed the task in optimal (also non-optimal) arousal conditions according to their chronotype, which may promote the anticipated use of strategies even in the short prime-target SOA block. Note that the younger adult group in (33), showed inhibitory effects in the rather short 200-ms SOA. To assess the effects of chronotype and time of testing on controlled processing, we explored both the emergence and time course of inhibitory priming with longer prime-target SOAs (450, 650, and 850 ms). On the basis of previous studies, we expected synchrony effects to affect controlled but not automatic processes, but we went further and investigated how the time course of such effects may change as a function of both chronotype and time of testing. Relying on results from previous experiments that have reported differences in both neural and cognitive functioning in morning- and evening-types (11, 13, 35, 37), we proposed separate analyses for the two groups.