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Neuroscience and Biobehavioral Reviews 155 (2023) 105438

Contents lists available at ScienceDirect

Neuroscience and Biobehavioral Reviews


journal homepage: www.elsevier.com/locate/neubiorev

Review article

On natural attunement: Shared rhythms between the brain and


the environment
Efrosini Charalambous a, Zakaria Djebbara b, c, *
a
University of Cyprus, Faculty of Engineering, Cyprus
b
Aalborg University, Department of Architecture, Design, Media, and Technology, Denmark
c
Technical University of Berlin, Biological Psychology and Neuroergonomics, Germany

A R T I C L E I N F O A B S T R A C T

Keywords: Rhythms exist both in the embodied brain and the built environment. Becoming attuned to the rhythms of the
Architecture environment, such as repetitive columns, can greatly affect perception. Here, we explore how the built envi­
Neural entrainment ronment affects human cognition and behavior through the concept of natural attunement, often resulting from
Ecological psychology
the coordination of a person’s sensory and motor systems with the rhythmic elements of the environment. We
Affordances
argue that the built environment should not be reduced to mere states, representations, and single variables but
Resonance
Attunement instead be considered a bundle of highly related continuous signals with which we can resonate. Resonance and
Built environment entrainment are dynamic processes observed when intrinsic frequencies of the oscillatory brain are influenced by
Neuroarchitecture the oscillations of an external signal. This allows visual rhythmic stimulations of the environment to affect the
brain and body through neural entrainment, cross-frequency coupling, and phase resetting. We review how real-
world architectural settings can affect neural dynamics, cognitive processes, and behavior in people, suggesting
the crucial role of everyday rhythms in the brain-body-environment relationship.

1. Introduction theories of cognition, to flesh out a mechanism for Gibson’s concept of


resonance (Falandays et al., 2023; Raja, 2021), can benefit from a closer
Recasting and expanding the boundaries of the embodied mind re­ look into the properties of the built environment itself. Features of the
quires a reconsideration of the body-brain coupling processes (Klimesch, built environment can affect cognition and behavior. Yet, the literature
2018), and a deeper understanding of the constraints and affordances of neuroscience broadly ignores the richness of the environment,
that emerge relative to the material reality (e.g., the built environment) reducing it instead to mere states, representations, and single variables.
with which the embodied brain is constitutively coupled (Dotov et al., With patterns and rhythms naturally omnipresent in our environment,
2010; Malafouris, 2013). It requires an acknowledgment of the rela­ we ask: How do visual rhythmic stimulations of the environment couple
tional nature of embodied cognition as a larger organism-environment with and affect the brain and body? To answer this, we need to explore
system. The concept of ‘affordances’ coined by (J. Gibson, 1986) has how the design of the built environment can potentially cause rhythmic
emerged as a key aspect in the field of embodied cognition, providing a sensorimotor stimulation that can be translated into an environmental
framework to understand how the brain, body, and environment input flow. The dynamic processes of resonance by which a person’s
interact. Although this includes a neuroscientific perspective too, the sensory and motor systems coordinate with the rhythmic elements of
camp of ecological psychology has largely neglected the important their environment, often underlie and act as a scaffolding for the expe­
function of the central nervous system, perhaps as a strategic move to­ riential quality in natural attunement.
wards emphasizing the importance of environmental features in adap­ With the maturing of neuroimaging techniques (Gramann et al.,
tive behavior. This approach has revealed numerous important 2014; Makeig et al., 2009), the inclusion of the environment for
theoretical advances (Djebbara et al., 2022; Rietveld and Kiverstein, ecologically valid experimentation is a necessary next step to under­
2014; Withagen et al., 2017) and empirical results (Djebbara et al., standing the brain in real-world settings (Brunswik, 1956; de Wit et al.,
2019, 2021; Haken et al., 1985; W. H. J. Warren, 1984). 2017; Raja and Anderson, 2019). This has been coined by Gramann et al.
Recent interest to reintroduce neural dynamics into ecological (2014) as ‘natural cognition’ from which we have borrowed the wording

* Corresponding author at: Aalborg University, Department of Architecture, Design, Media, and Technology, Denmark.
E-mail address: [email protected] (Z. Djebbara).

https://doi.org/10.1016/j.neubiorev.2023.105438
Received 10 August 2023; Received in revised form 19 October 2023; Accepted 24 October 2023
Available online 26 October 2023
0149-7634/© 2023 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
E. Charalambous and Z. Djebbara Neuroscience and Biobehavioral Reviews 155 (2023) 105438

‘natural’ in the concept of ‘natural attunement.’ This concept attempts to for example, the ability of the brain to selectively engage with or
foreground the significant role of the environment by situating the self-tune to the environmental variables. The idea of the perceiver as "a
rhythmic properties of the built environment as central in the literature self-tuning system"1 (J. J. Gibson, 1966, p. 271; original emphasis) has
on the rhythmic and oscillatory nature s of the human body and the been central in Gibson’s discussions regarding the role of perceptual
brain. The main argument is that externally generated rhythmic stimu­ systems during active exploration. Our perceptual system (as a set of
lations can entrain internal neural rhythms that, in turn, affect cognition organs that include sensory receptors) as a self-tuning system attends to
and behavior. and detects certain classes of information that are available and useful to
The most intuitive conceptualization of rhythm is repetition through the perceiver as affordances (J. J. Gibson, 1966). Being sensitive and
intervals or durations. Although the notion of rhythm can entail much responsive to relevant cues and affordances an organism adjusts its
more complicated aspects, we focus on the rhythm as repetition since perceptual and motor systems to the information in the environment. It
this has potentially stronger links to the phenomenon of entrainment. By is a continuous and dynamic process of becoming attuned to the prop­
‘rhythm,’ in this paper, we mean a recurrent pattern of change through erties and possibilities of the environment.
time of a signal, but we cannot exclude the possibility that non-recurrent On the other hand, in the empirical neuroscience literature, the focus
patterns as rhythms may have a similar effect. Drawing the environment has been on the phenomenon of neural entrainment, which can be
in terms of rhythms allows for considering their immediate interaction defined as "[…] the alignment of one or more oscillating systems to an
with neural (and other) oscillatory dynamics. The upshot is furthermore external rhythm, whereby the interactions are unidirectional, that is, the
that the environment is not considered a static state, but rather a bundle external rhythm influences the oscillating system(s) but not vice versa"
of highly related continuous signals with which we can resonate. While (Lakatos et al., 2019). In the case of neural entrainment, the endogenous
resonating with others is possible too (Czeszumski et al., 2020; Dumas, neural oscillations become temporally aligned to the systemic regular­
2011), we focus here on the relationship between a single agent and the ities in the environment (Obleser and Kayser, 2019; Thut et al., 2011).
built environment. Interestingly, evidence from studies on neural entrainment also suggests
Philip Thiel, for example, whose work is substantially influenced by that the “act of resonating” (Reed, 1989, p. 115) is supported by pro­
concepts and ideas of environmental psychology, argues about the cesses of active sensing and dynamic attending (Lakatos et al., 2019;
importance of focusing on how we experience the built environment Large and Jones, 1999).
over time and not just as a snapshot from a fixed viewpoint. Thiel’s Both entrainment and resonance are properties of non-linear dy­
comment that "Architecture may well be ’frozen music’, like a phono­ namic systems. However, both concepts still lack a clear definition in
graph record; but man is the pickup whose movement realizes the cognitive neuroscience (Helfrich et al., 2019). It is not within the scope
experience" (Thiel, 1961, p. 33), revolves around the idea of perception of the paper to provide a detailed definition of these properties or
as active information picking up over time and thus creates an imme­ describe their relationship in full detail. However, we think it is
diate reference to theories of direct perception, e.g., ecological psy­ important to clarify that we consider entrainment and resonance as
chology (Michaels and Carello, 1981). Similarly, a feature of the built measurable empirical properties that support coordination while we use
environment that plays a significant role in our experience is rhythm as the term attunement to refer to the experiential dimension of such
repetition, which in turn makes movement and time important aspects. phenomena.
As we will argue, the design of the built environment can shape the type Despite the rich evidence that rhythms alter behavior, the vast ma­
of sensory and motor change we experience. However, the change itself jority of empirical neuroscience has yet to acknowledge the richness of
requires more than designed external signals. It requires active partici­ the environment. Thus, to place the environment back into its rightful
pation and coupling with the external signal, which in ecological psy­ place as a resonant structure in the interaction between agent and
chology is often referred to as resonance (Heft, 2001; Raja, 2018, 2021). environment, we organize our paper in the following way. Section 1
The idea of resonance as a property of perceptual and neural systems offers a detailed account of the phenomenon of resonance at different
has gained popularity in the literature on brain-body-environment re­ scales and from different viewpoints. We first provide an ecological
lationships. Although it is a widely observed phenomenon of dynamic psychology perspective on resonance and then briefly review evidence
systems, the term has been mainly used as a metaphor in ecological of resonance and entrainment at the neuronal scale. This section ex­
psychology, to denote the form of coupling between active perceptual emplifies the many ways in which we can naturally attune to the envi­
systems and informational variables in the energy flows of the envi­ ronment. Section 2 shifts the focus from lab-based findings to real-world
ronment (J. Gibson, 1986; Raja, 2021). It occurs when there is an complex dynamics to situate the possibility of natural attunement. The
alignment between the organism’s behavioral patterns and the infor­ objective here is to examine how the ’act of resonating’ with useful
mational structure of the environment, resulting in a smooth and effi­ perceptual information can lead to environmental resonance. Finally,
cient interaction between the two. Ecological informational variables the discussion naturally leads back to the built environment component.
are thus the bridge between agents and their environment and are Section 3 considers the experiential dimension of the coupling processes
important for the specification of both (Michaels and Carello, 1981, p. as a possibility for natural attunement in real-world architectural spaces.
38). The agent’s perceptual systems are attuned to the perceptual in­
formation, or as Gibson comments: "[…] the perceptual system simply 2. From resonance to neural entrainment
extracts the invariants from the flowing array; it resonates to the
invariant structure or is attuned to it" (J. Gibson, 1986, p. 249; original The phenomenon of resonance can be observed at different scales,
emphasis). from the ecological scale of body-brain-environment interactions to
The term attunement, which is defined in more detail in Section 4, is spontaneous oscillations of neuronal networks (Thompson and Varela,
a concept with a more intentional connotation (Heft, 2001) capturing, 2001; Varela, 1995) and even to spiking bursts of single neurons

1
Gibson notes that we should not consider this as a passive process: “The
"resonating" or "tuning" of a system suggests the analogy of a radio receiver.
This model is inadequate because there would have to be a little man to twiddle
the knobs. A perceiver is a self-tuning system. What makes it resonate to the
interesting broadcasts that are available instead of to all the trash that fills the
air? The answer might be that the pickup of information is reinforcing” (J. J.
Gibson, 1966, p. 271)

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E. Charalambous and Z. Djebbara Neuroscience and Biobehavioral Reviews 155 (2023) 105438

(Izhikevich et al., 2003). This section examines key properties under­ a global level, changes in resonance frequency depend on the current
lying these interactions, such as spontaneous oscillations, nonlinearity, transient network configuration, which is influenced by cognitive con­
and entrainment, which are also linked to evidence of neural entrain­ tent, perceptual flow, and top-down control mechanisms such as
ment from the field of empirical cognitive neuroscience. While the attention (Helfrich et al., 2019). On a local level, the rhythmic modu­
phenomenon of neural entrainment can lead to absolute coordination lations in local excitability result in spontaneous neural oscillations
there are also cases characterized by relative coordination or entrain­ within specific frequency bands contributing to a self-organizing brain
ment in a broader sense. system. They are considered instrumental to brain functions and their
intrinsic synchronization most likely plays a key role in perception3 and
2.1. Agent-environment interactions different cognitive phenomena (Buzsáki, 2006; Schroeder and Lakatos,
2009).
The compatibility between dynamic systems theory (DST) and It is imperative to emphasize that these are spontaneous oscillations,
ecological psychology is not new (Di Paolo et al., 2017; see for instance; not driven by external factors or interactions. These oscillations are
Thelen and Smith, 1994), and the advantage is the materialization of believed to give rise to a nonlinear phenomenon, i.e., stochastic noise or
concepts like resonance. Resonance in DST refers to the resonance, that appears to help transfer information and optimize a
frequency-specific response of a driven system when triggered by a system’s response to a weak signal (Deco et al., 2009; McDonnell and
single transient event as well as repeated events (Helfrich et al., 2019). Abbott, 2009; Moss, 1997). Spontaneous activity has also recently been
However, Raja (2018) suggests that the foundation for resonance in proposed as the basic model for self-specificity, i.e., how the embodied
ecological psychology rests on informational coupling, which is when brain distinguishes between internal and external stimuli (Northoff,
the dynamics of both agent-environment interactions are coupled to the 2016, 2018; Raichle et al., 2001).
dynamics of the agent’s central nervous system (CNS) in terms of the
same ecological information. Raja’s (2018, 2019) proposal of an oper­ 2.2.2. Internal nonlinear coupling
ational account of ecological resonance is heavily based on behavioral Internal couplings of neural assemblies often rely on coordinating
dynamics, evident in the work of Warren (2006) as well as Anderson’s mechanisms of phase alignment. (Fries, 2005; Uhlhaas et al., 2009;
neural reuse (Anderson, 2010), and coordination dynamics (Kelso and Varela, 1995). Phase alignment describes how action potentials from
Tognoli, 2007) offering an appropriate account at the neuronal level. different neurons are timed to fire at the same phase of a rhythmic cycle,
This level is often omitted from discussions within ecological psychol­ which can give rise to oscillatory entrainment. Oscillatory entrainment
ogy. Furthermore, it is grounded in theories of system dynamics entails two important underlying mechanisms (Calderone et al., 2014):
(Chemero, 2013), suggesting interactions between different hierarchical phase-reset and cross-frequency coupling (Fig. 1A-D & 2B). Phase-reset
scales: the two systems of agent and environment constrain each other refers to the modulation or resetting of the timing of oscillatory activity
(according to behavioral dynamics), and the dynamics at this ecological in response to a stimulus or perturbation.4 Cross-frequency coupling
or intentional scale constrain the nested scales of the muscular or occurs through temporal alignments across different amplitudes and
neuronal systems (Raja, 2018). frequencies, which can exhibit nonlinear patterns of resonance. Neural
Neuronal dynamics are thus understood as being constrained by the assemblies can become phase-locked not only to the intrinsic frequency
information generated in agent-environment interactions. An illustra­ but to the harmonics of the entraining frequency as well (Klimesch,
tive case of ecological resonance is the study by van der Weel and van 2018; Large, 2008).
der Meer (Van der Weel and van der Meer, 2009) on infants’ brain re­ Thus, brain regions with different intrinsic dynamics can be quasi-
sponses to looming objects. Researchers reported that the theta rhythm synchronized through different cross-frequency couplings such as
oscillations in babies’ visual cortex correlated with perceptual infor­ amplitude-amplitude coupling, phase-phase coupling, or phase-
mation. That is the ecological variable tau2 (Lee, 2009), a relational amplitude coupling (Fig. 1A-D; Lakatos et al., 2019). In
measure between sensory and motor information generated at the amplitude-amplitude coupling and phase-phase coupling, a phasic
agent-environment scale. Although tau is not our phenomenon of focus, relationship is needed between the frequencies of the two oscillations,
it serves as a good example of the importance of the CNS in under­ whereas in the phase-amplitude coupling, the amplitude of a higher
standing resonance and the mechanisms of neural entrainment. frequency, e.g., gamma (~40 Hz), is modulated by the phase of a lower
frequency, e.g., theta (~4 Hz). Additionally, it is worth noting that if an
2.2. Mechanisms underlying rhythmic activity external signal or mechanism successfully affects the lower rhythms of
the brain, it can potentially modulate the phase-amplitude coupling with
2.2.1. Spontaneous oscillations higher frequencies, which are thought to be related to sensation and
At the scale of populations of neurons, oscillations occur due to perception (Rodriguez et al., 1999). Our grip and understanding of the
communication through their electrochemical interactions (Buzsáki, world appear to hinge on the neural capacity of frequency coupling.
2006). Neurons’ action potentials can be in the form of a single spike or a Notably, such cross-frequency couplings have been documented be­
burst of spikes that exhibit specific resonant interspike frequencies tween body-brain oscillations, forming a single rhythmic hierarchy
(Izhikevich et al., 2003). They generate spontaneous oscillation at their
preferred frequency and they respond better to inputs with frequencies
3
falling within a specific frequency range. This results in communication For example, Cosmelli et al. (2007) describe such a case as a resonant as­
between neurons being selective based on their resonance frequencies, sembly where the transient binding of different neuronal populations associated
which plays a key role in coherent brain dynamics (Fries, 2005; with features of a visual object (shape, color, motion) can be involved in the
transient perception of the visual object.
Hutcheon and Yarom, 2000). However, under certain conditions (e.g., 4
Phase reset is observed across different modalities (e.g., visual, and auditory
chemical changes in the neuron’s membrane) the neuron’s natural fre­
during speech). An ongoing oscillatory behavior is observed to reset its phase in
quency can shift in and out of its resonance range enabling resonance at tandem with an external stimulus.
the scale of different neuronal networks (Lau and Zochowski, 2011). On

2
The perceptual variable tau is defined as the relative rate of expansion of an
approaching object (looming figure) projected on the screen constraining the
perceptual system (Raja, 2019) or more generally as “the time-to-closure of the
action-gap at the current rate of closure” (Lee, 2009).

3
E. Charalambous and Z. Djebbara Neuroscience and Biobehavioral Reviews 155 (2023) 105438

Fig. 1. There are mainly three kinds of couplings between signals, namely amplitude-amplitude coupling, phase-phase coupling, and phase-amplitude coupling. A.
Several spectral properties can be extracted from signals, among others the phase and the amplitude. B. Amplitude-amplitude coupling is the coupling through
synchronization of the amplitude of two different frequency bands. For example, when alpha (8–12 Hz) and beta (13–30 Hz) oscillations are both active, they may
synchronize their amplitude such that peaks and troughs of the two frequencies align. C. Phase-amplitude coupling refers to the modulation of the phase (timing) of
one frequency by the amplitude (power) of another frequency. For example, when alpha oscillations modulate the phase of gamma oscillations, the timing of gamma
oscillations may be influenced by the amplitude of alpha oscillations. D. Phase-phase coupling refers to the synchronization of the phase (timing) of two different
frequency bands. For example, when theta (4–8 Hz) and gamma (30–80 Hz) oscillations are both active, they may synchronize their phase such that the peaks of one
frequency align with the peaks of the other frequency.

(Klimesch, 2018).5 behavioral performance (De Graaf et al., 2013; Mathewson et al., 2012;
Spaak et al., 2014).
While the scope of this paper is limited to entrainment through
2.3. Empirical evidence of neural entrainment sensory channels, we briefly mention a few studies that used electric
stimulation to generate rhythm and perturb cognitive performances to
Neural oscillations can be entrained to external rhythms across demonstrate the mechanism of neural entrainment. For instance,
different frequencies and different modalities (Calderone et al., 2014; behavioral effects of neural entrainment have been demonstrated with
Haegens and Zion Golumbic, 2018; Schroeder and Lakatos, 2009; Thut the use of transcranial alternating current stimulation (tACS), which is a
et al., 2011). Alignment of neural rhythms to environmental regularities non-invasive brain stimulation technique that uses weak electrical cur­
in the auditory domain, e.g., speech or music, is mainly observed at rents to modulate neuronal activity in the brain. Alekseichuk et al.
frequencies below 10 Hz (Doelling and Poeppel, 2015; Golumbic et al., (2016) successfully recorded improved spatial working memory per­
2013; Obleser and Kayser, 2019). Engaging in a conversation at a formance when theta and gamma waves were co-stimulated, but this
cocktail party is a very popular real-world example that demonstrates effect is observed only when repetitive gamma bursts are synchronized
our ability to tune to a specific signal in a noisy environment (Golumbic with the peaks of the theta rhythm. Additionally, the study demon­
et al., 2013). This presumably entails perceptual entrainment to a spe­ strated that the most effective high gamma frequencies for retaining
cific audiovisual rhythm of speech production supporting interpersonal multiple items range between 80 and 100 Hz in the prefrontal cortex.
interactions. Selective entrainment to behaviorally relevant events Furthermore, the use of transcranial magnetic stimulation (TMS), which
demonstrates active shaping of perceptual input and can be influenced is also a non-invasive stimulation technique used to modulate brain
by predictive mechanisms, as suggested by reduced reaction times in activity by using electromagnetic coils placed near the scalp to generate
target detection (Golumbic et al., 2013; Lakatos et al., 2008; Stefanics rapidly changing magnetic fields, has also demonstrated behavioral ef­
et al., 2010; Teng et al., 2018). fects. Albouy et al. (2017) linked theta oscillations in the dorsal stream
During visual entrainment, several researchers report increased to participants’ auditory memory manipulation abilities. Applying
sensitivity of attended cues associated with delta modulations on high- theta-rhythmic TMS over a targeted area significantly improved accu­
frequency activity associated with sensory processes (Lakatos et al., racy in memory tasks, establishing a causal relationship between theta
2008; Saleh et al., 2010). Cross-frequency modulations were also related activity in the dorsal stream and memory manipulation.
to a top-down predictive mechanism during 10 Hz flicker entrainment of The causal role of neural rhythms on cognition (Hanslmayr et al.,
parieto-occipital alpha associated with rhythmic sampling (Helfrich 2019) has also been demonstrated in a study by Riddle et al. (2020) who
et al., 2017; VanRullen, 2016). In general, most evidence suggests that sought to understand the role of theta and alpha waves during a working
rhythmic flickering light at an alpha frequency entrains intrinsic oc­ memory task. They found that the effect of rhythmic TMS on memory
cipital alpha rhythm associated with periodicity in visual perception and performance depended on the mismatch with the task-driven oscillation.
Furthermore, Di Gregorio et al. (2022), using TMS too, affected pre- and
post-stimulus alpha in a visual perception task, and successfully
5
Klimesch (2018) mentions several interesting cases such as lung-heart demonstrated that subjective experience could be linked to the alpha
coupling, muscles- motor cortex coupling as well as the coupling between rhythm of the brain. Their results suggest a split between alpha speed
phase of gastric basal rhythms and the amplitude of spontaneous alpha rhythm and alpha amplitude, connecting alpha frequency to spatiotemporal
fluctuations. He postulates that the different frequencies do not vary randomly
sampling capabilities and alpha amplitude to the internal, subjective
and that these couplings follow a doubling/halving ratio (e.g., 1:2) character­
perception, and interpretation of sensory experiences. Supramodal re­
izes the relationship between neighboring center frequencies of traditional
gions of the brain, too, can be entrained and affect cognitive processes.
brain frequency bands while non-neighboring frequencies can be harmonically
coupled at other ratios (e.g., 1:3, 1:6). For example, midline frontal theta at Albouy et al. (2022) established causal evidence for the supramodal role
6 Hz co-occurs with alpha at about 12 Hz (twice as fast) during increased of the frontoparietal network in human cognition, linking frontoparietal
working memory demands (Jensen et al., 2002). theta oscillations to auditory working memory performance and

4
E. Charalambous and Z. Djebbara Neuroscience and Biobehavioral Reviews 155 (2023) 105438

demonstrating enhancement through theta rhythmic visual stimulation. precise phenomenon. It enables approximations of rhythmic stimula­
tions rooted in the built environment to be effective too.
2.3.1. Multisensory integration and memory
Perceptual systems flexibly use temporal information of contextual 3. Environmental resonance in real-world settings
structures not only within but also across sensory modalities to predict
upcoming events, which can lead to phase alignment in relevant mo­ Neural tracking (Fig. 2A) of environmental regularities at the
dalities that are not necessarily directly stimulated (Daume et al., 2021; perceptual and behavioral level (neural entrainment in the broad sense)
Lakatos et al., 2007; Ten Oever et al., 2014). For example, such multi­ is not only amenable to the technical constraints of neuroscientific
sensory integration is manifested during speech perception, where studies (Obleser and Kayser, 2019), but it also embraces the different
continuous non-rhythmic visual input affords predictable temporal degrees of complexity that are linked with different phenomena. Para­
regularities regarding upcoming auditory events, and relevant oscilla­ phrasing Lakatos (2019), entrainment tolerates input sequences that are
tions are then modulated so that auditory input arrives at phases of high not completely predictable or isochronous. However, an underlying
excitability (Schroeder et al., 2008). Though not directly related to the assumption in some studies focusing on the perception of musical events
built environment, it attests to the possibility of getting entrained to or natural speech is that there is sufficient regularity in the auditory
non-rhythmic events in the built environment. signal and the perceptual phenomenon to fit the narrow definition of
The mechanism that supports predictability relative to the temporal entrainment but fail to quantify the regularity of the stimulus signal, e.
onset of upcoming events in sequential structures inherently involves g., continuous speech. As part of the recent attempts for a critical
aspects of episodic memory (Kurby and Zacks, 2008). At the same time, re-evaluation of entrainment, Meyer et al. (2020) ask if entrainment, in
episodic memories are also rich in contextual information about events the narrow sense, denotes synchronization of brain rhythms in the
involving the integration of different sensory modalities. Theta oscilla­ sensory systems with rhythmic stimuli features and if the external
tions are often associated with the binding of contextual information stimuli are not strictly rhythmic, then how can something that does not
and episodic memory (Staudigl and Hanslmayr, 2013). Behavioral re­ have clear physicality in the external world trigger this sort of coordi­
sults of increased memory performance have been reported in several nation? This is a relevant question in the context of the built environ­
studies that examined neural entrainment using visuoauditory stimula­ ment, as it is unlikely to have a strictly rhythmic stimulation to induce
tion at the theta frequency (Clouter et al., 2017; Guan et al., 2018; Köster neural entrainment in the narrow sense.
et al., 2019; Roberts et al., 2018). An illustrative real-world example of how we can perceive a periodic
pulse in non-periodic stimuli is the perception of the beat in music, to
2.4. Neural entrainment: a narrow and broad definition which we can spontaneously coordinate motor activity (Large et al.,
2015). While the rhythms of music are not periodic but rather complex
Brain responses to external periodic input do not necessarily always temporal auditory structures, our perceptual system has the ability to
involve phase alignment of endogenous neural oscillations. ‘Stimulus- capture the pulse or beat (perceived periodicity) and meter (perceived
tracking’ or ‘neural-tracking’, for example (Fig. 2A), can elicit repeated patterns of alternation between weak and strong pulses). According to
transient event-related responses to a series of temporal regularities but the ‘Neural Resonance Theory’ (Large, 2008; Large and Snyder, 2009),
because it is not clear if it interferes with related cognitive and pulse perception arises as spontaneous endogenous oscillatory activity
perceptual processes, it can only be considered as entrainment in the of neural populations (rhythmic bursts) resonating with rhythmic
broad sense (Bánki et al., 2022). In contrast, entrainment in the narrow stimulation while influencing attention and expectation. Because neural
sense is when the input flow ’hijacks’ the frequency of the ongoing systems exhibit higher-order resonance characteristics as nonlinear os­
neural oscillation. Several authors have argued about the importance of cillators, they can become coupled to the stimulus through phase
this distinction. This is mainly because it is only in the latter case that we entrainment not only in terms of 1:1 synchrony but also under other
can assume alternation of spontaneous neural oscillations (phase multifrequency modes of coordination with rhythmic stimuli. As a
alignment) and, most importantly, that these alterations are result, oscillations may fluctuate at frequencies that are not present in
behaviorally-relevant (Bánki et al., 2022; Haegens, 2020; Helfrich et al., the rhythmic stimulation, giving rise to ‘pulse perception’ whose fre­
2019; Keitel et al., 2014; Obleser and Kayser, 2019). quency is not physically present in the input flow (Large et al., 2015). In
A stricter definition of what constitutes true entrainment suggests other words, if the interaction with certain features of the built envi­
that besides the presence of a driving and a driven oscillator, another ronment appears rhythmic, they may not be found to affect the neural
requirement is frequency selectivity (Haegens and Zion Golumbic, oscillations at the exact same frequency, but at another.
2018). In other words, true coupling between external and internal Similar to music and natural speech, the natural sensory environ­
periodicities occurs for a range of rhythms that are close to the intrinsic ment involves dynamic visual input with temporal structures of varying
frequency of the oscillatory brain, e.g., theta (4–8 Hz). Entrainment ef­ frequencies that are very rarely, strictly rhythmic. Interestingly, it has
fects are strongest when the two oscillators overlap in frequencies, but it been demonstrated that neural entrainment is possible beyond ‘fre­
can also be observed if the stimulation frequency does not exactly match quency-tagging’ with neural phase-locking to stimulation of varying
the neural eigenfrequency. This is captured by the characteristic trian­ frequencies (Henry et al., 2014; Keitel et al., 2017). It is thought that in
gular shape of the theoretical model of entrainment called ‘Arnold cases where stimulation is not strictly rhythmic, i.e., when the input is
Tongue’ (Fig. 3B). It illustrates that the further the external frequency is complex and irregular, entrainment shifts to an average repetition value
to the neural eigenfrequency, the higher its intensity needs to be in order (Lakatos et al., 2008, 2013). This can be demonstrated with temporal
to entrain the endogenous oscillator (Notbohm et al., 2016; Zoefel et al., predictability being evident in a more naturalistic context where sensory
2018). input is not strictly rhythmic (Calderone et al., 2014; Mathewson et al.,
It is, thus, not unreasonable to consider neural entrainment as one 2012). These findings suggest that the phenomenon of neural entrain­
mechanism (at the nested neural scale) closely linked to resonance in the ment may be extended and generalized to other forms of temporally
ecological sense. For instance, Raja (2021, p. 122) states that “[…] predictive contextual structures that do not as such entail discontinuous
models of networks composed by nonlinear neural oscillators […] rhythmic stimulation.
exhibit a feature known as nonlinear resonance that accounts for some Furthermore, it has been demonstrated that a dynamic systems
network properties as stimuli filtering, neural entrainment, or stimuli model of a weakly coupled neural networks in combination with Heb­
anticipation". Gibson’s insightful metaphor of the brain as a resonant bian plasticity can be used to model rhythm perception in infants
organ is a theoretical framework that may find support in empirical (Tichko and Large, 2019), which also demonstrated that early
neuroscience. Even further, this suggests that entrainment is not a auditory-motor interactions influence infants’ rhythmic preferences

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Fig. 2. A. Stimulus or neural tracking refers to the ability to follow and measure the neural response to a specific stimulus over time. This is done through time-locked
brain responses that occur in response to a temporally regular stimulus, such as a visual or auditory cue. Such brain responses are known as Event-Related Potentials
(ERPs) and may wrongfully appear as an oscillator. B. Phase-resetting refers to the ability of an oscillatory system to reset its phase in response to a transient input or
perturbation. This phenomenon is observed when a neural oscillator receives an external input, such as a sensory stimulus or an electrical pulse, and its phase is
shifted, or reset, to a new value. The magnitude and direction of the phase shift depend on the timing and strength of the input relative to the phase of the ongoing
oscillation.

Fig. 3. A. Neural entrainment, in the narrow sense, refers to the synchronization between an eigenfrequency of a population of neurons with rhythmic external
stimuli, such as sounds or visual stimuli. This synchronization is thought to enhance cognitive processing and behavioral performance. Entrainment can occur at
various frequencies and with a variety of external stimuli. Importantly, entrainment in the narrow sense is expressed with an increase in the amplitude of the targeted
eigenfrequency. B. The Arnold tongue is a concept in the field of neural entrainment that refers to a region of parameter space where an oscillator, such as a neuron or
a population of neurons, can be entrained to an external rhythmic signal. It is a visual representation of the relationship between the frequency and phase of the
external signal and the frequency and phase of the oscillator’s response. The tongue is typically shaped like a tongue or a comb, and its shape is determined by the
strength and phase of the coupling between the oscillator and the external signal.

(Tichko et al., 2021). With outset in Neural Resonance Theory (NRT), continuous environmental stimulation as opposed to discrete structures
Tichko et al. (2022) approximate a Gibsonian embodied perspective of of sensory flows. The temporal structure of the perceptual information in
rhythms in a similar sense as presented here. In the context of NRT, real-world settings is rarely as clearly rhythmic as in lab-based condi­
living organisms adapt to consistent patterns in their surroundings by tions. Therefore, focusing on environmental resonance as a response to a
adjusting the strength of connections and the relative phases between naturalistic degree of rhythmic complexity may expand our under­
natural rhythms and biological oscillations. This adaptation takes place standing of the mechanisms underlying coordinated behavior and tem­
across various nested timescales, contributing to the development of poral prediction and, most importantly, enhance the concept of
rhythmic perception and behavior throughout the organism’s lifespan. ecological relevance. It is the quality of the experience that emerges
Essentially, by applying a systems approach, their view suggests that a from this coupling with the built environment that we refer to as ‘natural
non-linear dynamical systems approach may be useful for detecting the attunement,’ which is relevant to the discourse of perception of atmo­
emerging resonant landscape. sphere (Canepa, 2022; Griffero, 2014) and the immediate gist of scene
The temporal regularities embedded in the environment afford pre­ perception (Djebbara et al., 2019; Oliva and Torralba, 2006).
dictions and anticipation about future sensory events, which optimize
behavior (Cravo et al., 2013; Spaak et al., 2014). In contrast to complex
auditory stimuli, visual stimulation through movement (e.g., in the built 3.1. Real-world behavioral effect of resonance
environment) entails temporal structures of perceptual information.
These are amenable to alternations through movement and at the same The effect of neural entrainment on multisensory integration and
time can impact movement, e.g., sensorimotor coupling (Djebbara et al., cognitive functions related to attention (Helfrich et al., 2018; VanRullen,
2019, 2021, 2022). This suggests the possibility of resonance with 2016) and memory (for a review: Hanslmayr et al., 2019) suggests an
impact on behavior. These are, however, laboratory experiments that do

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not allow for freely moving human beings. Thus, we briefly review aperiodic patterns (Rimmele et al., 2018), enable modulation of the
real-world cases and empirical studies of high ecological validity that entrained oscillations7 through top-down control mechanisms, e.g., by
offer evidence of natural attunement in dynamic settings. During shaping attention allocation, manifested in cyclical alternations be­
movement, the perceivable structure of the built environment that tween optimal and sub-optimal behavioral performance that are not
constrains or affords different activities can change in a periodic directly linked to eye-movement or saccades (Helfrich et al., 2019;
manner. The rate of change of visual input flow in urban spaces or the VanRullen, 2016).
interior of buildings is often rhythmic or has temporal regularities able Evidence suggests that visual detection performance fluctuates at
to entrain, for example, neural oscillations of sensory receptors in pe­ 4 Hz when two different locations are alternatively visually sampled,
ripheral vision. Evidence suggests that the sensed rate of change of vi­ while an overall sampling of the visual scene is thought to operate at
sual elements in optical flow appears to modulate walking speed. 8 Hz (Landau and Fries, 2012). It has been proposed that active sensing
Ludwig et al. (2018) projected vertical lines with varying distances on of the environmental space is facilitated by dynamic periodicities in
the floor of a walkway and reported a decrease in walking speed when visuospatial attention (4 – 8 Hz) alternating between two modes of
traversing a pattern of lines with a high frequency as opposed to a low sampling: an exploratory mode as a continuous exploration of space when
frequency. That is, the fast changes in the peripheral vision suggest that visual information is unpredictable, and a rhythmic mode in the presence
one is moving fast whereas the natural behavioral adjustment is to slow of predictable events and of perceptual information relevant to the
down. Modulations in speed have also been reported in a driving agent’s intention (Gaillard and Ben Hamed, 2022; Schroeder et al.,
simulation study. By changing the width of the vertical lines that 2010; VanRullen, 2018). Even when attention is sustained at a behav­
appeared in a rhythmic visual pattern along a tunnel, it was demon­ iorally relevant location, there is a rhythmic fluctuation between periods
strated that speed adjustments could be controlled (Manser and Han­ of heightened and reduced perceptual sensitivity (Fiebelkorn and Kast­
cock, 2007). Increasing the distance between the vertical lines in the ner, 2019; Helfrich et al., 2018; Lakatos et al., 2008; Landau and Fries,
tunnel was perceived by the driver as slowing down, which conse­ 2012). During epochs of reduced perceptual sensitivity, attention can be
quently resulted in increasing driving speed. The opposite was observed shifted to explore other locations and reassess the value of the object of
when the distance between the visual elements was decreased. Simi­ attention. Furthermore, it has been speculated that the resonant fre­
larly, in a real-world case (Thaler and Sunstein, 2021), decreasing the quency of neural networks can be under top-down control of attention,
distance between the white stripes painted onto the road near dangerous which can, in turn, modulate bottom-up entrainment effects (Helfrich
curves along the east coast of Lake Michigan most likely had an effect on et al., 2017, 2018, 2019). If attention operates as a process at the
the sensorimotor dynamics associated with high velocity, which effec­ higher-level intentional scale that supports the detection of ecological
tively resulted in a reduction of drivers’ speed. Further evidence of information based on our intentions, then a constraint on the resonant
implicit behavioral effects of natural attunement was reported by Leo­ attentional networks can also modulate the entrainment of neural os­
nards and colleagues (Leonards et al., 2015), who investigated the cillations driven by sensory input flow. Brain rhythms are thus used as
impact of tile-pattern direction on the walking direction. Their findings active instruments of perceptual selection, calibrating (and calibrated
suggest that in contrast to significant rotations, subtle rotations of tile by) attention8 to external input based on its extrinsic structural salience
patterns (close to the straight line) resulted in participants veering away or its intrinsic value, e.g., the agent’s intention (Gaillard and Ben
from the straight trajectory. Overall, these behavioral effects suggest Hamed, 2022). It is worth noting that the latter case is closely linked to
that the rhythmic structure of environmental features may trigger pro­ the idea of ecological resonance, where the dynamics of a higher-level
cesses related to natural attunement (for a comprehensive review: intentional scale constrain the dynamics of the nested neural scale
Djebbara et al., 2022). (Raja, 2018).

4. Natural attunement: rhythmic built environments


3.2. The ’act of resonating’: active exploration, attention, and detection
So far, not much has been said about natural attunement. We clarify
Active sensing and dynamic attending (Lakatos et al., 2019; Large with a definition that is deeply inspired by Vara Sánchez (2023, p. 61):
and Jones, 1999) are two essential components that can modulate in a Attunement refers to the quality of an experience, perceiving our ac­
top-down fashion the intrinsic (and entrained) neural oscillations of the tions, emotions, or thoughts as being influenced by and influencing el­
perceptual systems.6 These skills also play an important role in rhythmic ements within the surrounding world. It can sometimes be associated
stimulation rooted in the built environment. Active sensing is based on a with the process of entrainment, where there is an alignment of our
collaboration of motor and sensory rhythms (e.g., sniffing, eye move­ experiences with external rhythms or patterns. Attunement captures the
ment, and saccades or microsaccades) and serves as a gating mechanism sense of connection we feel with a particular thing, event, or person.
for sensory inflow, optimizing perceptual sensitivity by temporally ‘Natural Attunement’, may arise from a state of partial or complete
aligning the high-excitability phase of oscillations. This involves actively entrainment. There are circumstances where we perceive our move­
detecting and then enhancing the sensing of behaviorally relevant ments or emotions aligning with a song, a text, or the rhythms of the city,
environmental information (while suppressing other irrelevant aspects), even in the absence of measurable entrainment. Nonetheless, in many
as well as preparing the system for future input flows through the for­ cases, the experience of attunement is a result of being entrained to some
mation of rhythmic expectations (Schroeder et al., 2010; VanRullen, degree.
2016). Rhythmic temporal predictions, inferred from both periodic and We can naturally become attuned to qualities encountered through
our rhythmic interaction and coupling with the world. Now whether and

6
The idea of active sensing is fundamental to the concept of direct perception
and resonance in ecological psychology: “That is, perceivers must learn to put
7
their perceptual systems in the appropriate resonant state-configuration. As Temporal and spatial expectations linked to entrainment of low-frequency
examples, rubbing a surface with the fingers is being in an appropriate state- neuronal oscillations may result in cross-frequency coupling influencing the
configuration for detecting texture, hefting is the state-configuration for power fluctuation of relevant faster oscillations, such as alpha power associated
detecting weight” (Michaels and Carello, 1981, p. 81). A similar idea is dis­ with inhibition mechanisms (Haegens and Zion Golumbic, 2018; Kizuk and
cussed by Gibson: "The state of a perceptual system is altered when it is attuned Mathewson, 2017; Rohenkohl and Nobre, 2011).
8
to information of a certain sort. The system has become sensitized. Differences The idea of ’calibration’ is also found in ecological psychology and refers to
are noticed that were previously not noticed. Features become distinctive that the process by which a system might change in terms of what response it
were formerly vague" (J. Gibson, 1986, p. 249). generates given a particular input variable (Jacobs and Michaels, 2007).

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E. Charalambous and Z. Djebbara Neuroscience and Biobehavioral Reviews 155 (2023) 105438

under what condition such experiential quality has its physical scaf­ rhythm through light and atmosphere (see Fig. 4A, ‘Your Black Horizon’
folding in neuronal couplings is an avenue to be explored. We assume with David Adjaye, Venice, Italy), while Santiago Calatrava manages to
that: when the specific rhythmic event is quantifiable, such as in cases of obtain a similar rhythmic effect through repetition of massive structures
repetition or predicted intervals, then this experience can be the result of (see Fig. 4B, ‘World Trade Center Transportation Hub,’ New York, US).
the phenomenon of entrainment. Furthermore, in cases where a singular Aldo Rossi, the Italian architect, rose to fame due to his rhythmic and
event in the sensory stream is powerful (e.g., due to its unexpectedness patterned structural work (see Fig. 4C, ‘San Cataldo,’ Modena, Italy).
or aesthetic experience) it is possible that the concept ‘resonance’ can be Carlo Scarpa pioneered a tight formalism of staircases that not only
used to explain this impact. The empirical and measurable dynamics of afforded sensory entrainment but motor entrainment beyond active
entrainment and resonance are often behind the process of coordination sampling (see Fig. 4D, ‘Brion cemetery,’ San Vito d’Altivole, Italy).
and of attunement. Furthermore, the use of certain materials can also engender attunement
As we have shown above, natural attunement can happen on a va­ such as the eucalyptus wood wraps on the exterior walls at the Burkina
riety of scales, from perception and action to complex neural dynamics Institute of Technology (Fig. 4E) in Koudougou, Burkina Faso by
caused by actual environments. We argue that the alignment of a per­ Diébédo Francis Kéré , which convey a unique natural rhythm experi­
son’s neural and physiological processes with the environment can in­ enced from the exterior and interior as a rhythmic shading of the cor­
fluence their cognition, perception, and behavior. A key concept to ridors. Greek architecture, too, displayed rhythmic columns (see Fig. 4F,
elucidate natural attunement stems from ecological psychology, namely the Stoa of Attalos, Athens, Greece, circa 120 BCE). Acoustic landscapes
sensing the affordances that are available in the environment. Affor­ too carry the potential for natural attunement with the environment.
dances shape the way the brain registers sensory information and the Jørgen Utzon famously drew the Sydney Opera with acoustic properties
continuous response (Bonner and Epstein, 2017; Cisek, 2007; Djebbara in mind–a technique he reused for Bagsværd Kirke, Copenhagen,
et al., 2021). Natural attunement to the affordances of the environment Denmark.
also has an impact on the affective experience. During disorientation, for Different layers of rhythm within a particular structure (or urban
example, spontaneous affordance-sensing (Proust, 2015) can be signif­ configuration and landscape) also appear in the built environment. For
icantly weakened as the active navigation process becomes unreliable, instance, as Pallasmaa comments, Alvar Aalto’s use of the forest meta­
causing feelings of anxiety and confusion (Fernández Velasco, 2022; phor at Villa Mairea (Fig. 4G) results in a "haptic fusion of tectonic
Fernandez Velasco and Casati, 2020). On the other hand, the architectural space and an amorphous and spontaneously rhythmic
re-attunement to the affordances of the visuospatial environment can ‘forest space’" (Pallasmaa, 2014, p. 31). Also, the convent of ‘Saint Marie
cause the well-known euphoric Aha!-feeling of sudden re-orientation de la Tourette’ (Fig. 4H) in Eveux-sur-l’Arbresle in Lyon, France by Le
(Charalambous et al., 2021). We can also enhance our navigational Corbusier demonstrates a multi-rhythmic structure through the ’undu­
skills by becoming attuned to different features in the environment. For lating glass panes’ of Iannis Xenakis. This holds the potential for both
example, attunement to the tile pavement for impaired people in urban phase resetting and neural interference. Based on the structure of Le
areas enhances their perception of the environment by translating the Corbusier’s corridor, and for illustrative purposes, we include here an
rhythm of the tiles into auditory and haptic sensory wave-like input example of how the visual cortex reporting on the peripheral vision can
flows. Given this extraordinary neural capacity, it is, however, also be entrained by rhythms in the built environment (Fig. 5).
possible for an external signal to interfere with internal signals and Furthermore, it is worth mentioning that there are different qualities
disrupt neural communication. Exposure to acoustic noise, for instance, of rhythm that we can experience in the built environment. Rhythm can
can negatively affect the processing of speech in the auditory cortex, be linked to the experience of a tension between oppositions and the
making it harder to understand spoken words. particular way in which something appears to us and in turn affects us
In his recent book, Vara Sánchez (2023) explores various perspec­ and our rhythms (Vara Sánchez, 2023). We can become attuned not
tives on the notion of rhythm, for instance, rhythm as movement, form, because of a repetitive wave-like rhythm, but due to the quality of the
energy, and even of rhythmic events as consisting of time-space-energy event and the invitation to look at things in a particular way. The
(i.e., Lefebre’s view) or of time-rhythms and affect-rhythms (i.e., ‘Bunker 599’ (Fig. 4I) designed by studio RAAAF (Rietveld and Rietveld,
Nietzche’s view). One of the most relevant to architectural experience is 2017) is an illustrative example that can potentially lead to partial
Plato’s view, which is that rhythm is order in movement as opposed to perceptual entrainment or transient resonance. The stairway that cuts
seeing rhythm as a regular construction of patterns (Vara Sánchez, through the banker invites the visitors to inspect the otherwise invisible
2022). As Vara Sánchez (2023) comments, it prevents movement from interior while at the same time, their attention is constrained by the built
disappearing by narrowing its possibilities down to a few relevant ones. form to a well-defined view of the exterior landscape and the water. The
Accordingly, rhythm can also refer to a quality of an event that in­ path reveals the coastline of the Netherlands and the historical signifi­
terrupts the regular flow of experience and invites a new particular way cance of the banker evoking an experience that connects the present
of looking. Such views of rhythmicity suggest a multilayer and complex with the past. Such architectural elements that constrain our movement
phenomenon particularly relevant to the discourse in aesthetics beyond and attention invite us to a particular form of experience to which we
the neural domain. Indeed, a rhythm cannot always be reduced to reg­ become attuned.
ular repetitions (Large et al., 2015; Obleser et al., 2017). However, the
more intuitive, narrow notion of rhythm as enacted repetition has a 4.2. Towards an empirical inquiry
greater possibility of leading to absolute body-brain entrainment. In the
built environment, rhythmic structures are present not only in the urban At least two things stand clear: (1) the unit and quantification of
fabric but can be also expressed in the design of doors, pavements, naturally occurring rhythmic stimulations can emerge in various forms
windows, columns, and other architectural elements (Chan, 2012). and through various modalities and (2) though used often, rhythms and
However, what empirically measurable units are these rhythms? What patterns are by no means novel to architects. However, their relation to
do these external signals consist of? the brain remains an untouched potential that could explain the trans­
historical existence of rhythms and patterns throughout numerous cul­
4.1. Built rhythms tures independently. This brings to mind Semir Zeki’s opinion on artists
throughout history. Architects, too, may have been “[…] neurologists,
Insofar, the unit and quantification of the said external signal have studying the brain with techniques that are unique to them and reaching
not been explicitly named. This is because rhythmic stimulation by the interesting but unspecified conclusions about the organization of the
built environment can occur through several mediums. For instance, brain” (Zeki, 1998, p. 77). Patterns, beyond their visual aesthetics, may
Olafur Eliasson is famous for finding innovative ways of playing with have been attractive due to the emerging natural attunement when

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Fig. 4. A. ‘Your Black Horizon’ by Olafur Eliasson + David Adjaye. Image credit: Olafur Eliasson/TBA21. B. ‘World Trade Center Transportation Hub’ by Santiago
Calatrava. Image credit: Photo © Alan Karchmer. C. ‘San Cataldo’ by Aldo Rossi. Image credit: Maria Lucia Lusetti Paolo Tedeschi. D. ‘Brion Cemetery’ by Carlo
Scarpa. Image credit: seier+seier. E. ‘Burkina Institute of Technology’ by Kéré Architecture. Image credit: Jaime Herraiz Martínez/Kéré Architecture F. Stoa of
Attalos in Athens, Greece. Image credit: Jorge Láscar. G. ‘Villa Mairea’ by Alvar Alto. Image credit: © Åke E:son Lindman H. Saint Marie de la Tourette by Le
Corbusier. Image credit: jpmm. I. ‘Bunker 599’ by RAAAF Studio. Image credit: RAAAF Studio.

interacting with the built environment. faster than the average of a normally distributed estimate of walking
Visual rhythms are more likely not to occur in a strict oscillatory speed. With the possibility of generating estimates, it allows for the
fashion. Due to the variance of the movement, saccades, and structure of design of experimental conditions where the peripheral vision can
the environment, it is difficult to precisely induce a specific frequency in fluctuate according to some desired frequency under some uncertainty.
any sensory receptor. While visual dynamics vary a great deal, the Combining this with Mobile Brain/Body Imaging (Gramann et al., 2014;
structure of the environment remains invariant. The external signal can Makeig et al., 2009) allows for simultaneous measures of neural activity,
trigger a modulation of the oscillations of the visual periphery offering body posture, and the built environment, i.e. brain, body, and envi­
possibilities of coordination with the environmental features as well as ronment, respectively, which is the hallmark of embodied cognition
the emergence of the experiential quality of attunement. However, the (Parada and Rossi, 2020; Wang et al., 2022).
phase of the external signal depends greatly on the movement of the Although built rhythms may cause a flicker in our visual periphery
body. Adults’ typical walking speeds vary depending on several vari­ throughout our everyday lives, we do not perceive it the same way as a
ables, including age, level of fitness, health, and terrain. On flat ground, flickering light in the hallway. One possible reason for that is that we
however, the typical average walking speed for adults is generally expect a change in sensory patterns and optic flow when we move in the
thought to be between 4.8 and 6.4 kilometers per hour (Fitzpatrick et al., world, which in turn corrects for detected sensory changes caused by
2006). This pace can change depending on the individual and may be self-movement. The contingency between sensory and motor processes
influenced by factors like the purpose of the walk (e.g., stroll vs. brisk is a critical feature for the emergence of perception (Di Paolo et al.,
walk), the terrain (e.g., uphill vs. downhill), and other individual factors 2017; O’Regan and Noë, 2001), and thus occurs without deliberate
such as age (Montufar et al., 2007). Due to their physical condition, attention. Due to limited cognitive resources, it is necessary for such
walking style, or personal preferences, some people may walk slower or automatic processes to strategically rely on prior experiences, habits,

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E. Charalambous and Z. Djebbara Neuroscience and Biobehavioral Reviews 155 (2023) 105438

Fig. 5. A. An example of how architectural features, such as a recurrent pattern operating in the periphery of our vision, may essentially induce a rhythmic and
entraining signal. The figure illustrates the difference between a pattern and a rhythm. While a pattern is a spatial concept, a rhythm is the enaction of patterns
through time. The transparent red triangles illustrate the peripheral limits and how these may cause a rhythmic signal, illustrated on the walls. The solid green line on
the floor represents the passed trajectory, whereas the dotted lines represent the trajectory to come. B. Externally induced peripheral signal oscillating at the cortical
alpha band. The red signal represents the rhythmic trajectory of brightness as perceived from the periphery of vision, while the green line represents the position in
space. The dotted green lines represent the future trajectory, while the solid one represents the past trajectory. The illustrated data is from a single participant, where
the walking speed was not indicated by the researchers. A natural attunement occurs, informing the movement velocity through optical resonance with the pe­
ripheral dynamics.

cultural norms, etc., which in turn allows freeing up mental capacity for rhythmic phenomenon. As the pulvinar plays a role in the alpha gen­
other purposes. According to the predictive coding hypothesis of the eration while also being sensitive to early visual processing, it can be
brain, automatic processes depend on ascending prediction errors hypothesized that built rhythms can bias, through perturbation, the
conveying unexpected information through various sensory channels ascending confidence levels of each sensory channel, which in turn may
not anticipated by descending signals (Friston, 2010). These ascending affect the generated alpha waves. Interestingly, if built rhythms can
signals modify descending predictions with varying levels of certainty affect the generation of the alpha waves at the level of the pulvinar,
encoded within them (Djebbara et al., 2022). This process is mirrored in which plays an integrative role between cortical regions, it may further
the excitability of neuronal groups, where sensory channels with high be hypothesized that cognitive processes that require the integration of
confidence levels are allowed to pass through the filter and impact the cortical regions can be affected by built rhythms. This not only speaks to
descending predictions in multiple cortical regions. Increasing evidence the importance of understanding built rhythms, but further to embrace
displays the pulvinar, which is a key nucleus for early visual processing naturalistic paradigms as the structure of the environment itself may
in the thalamus, as holding an integrative and bridge-like function be­ affect cognition to an extent that renders static laboratory experiments
tween cortical regions (Blot et al., 2021; Saalmann et al., 2012; for re­ futile.
view: Halassa and Kastner, 2017). The example provided in Fig. 5 is not the culmination of natural
While the pulvinar has for long been described as the generator of the attunement, but merely an example of how rhythms from the visual
alpha oscillation in the brain (Lopes da Silva et al., 1974), there is now periphery can have an entraining effect. As demonstrated above,
emerging evidence (e.g.: Halgren et al., 2019) that demonstrates how rhythms may dive as deep as the pulvinar and attest to the importance of
the pulvinar can generate alpha oscillation that in turn can carry advancing our understanding of their role. The empirical inquiry of
descending predictions and ascending prediction errors (Friston, 2019; natural attunement and underlying dynamic processes offers a novel
Alamia and VanRullen, 2019). These waves of predictions have been approach to understanding the interactive relationship between
coined the “travelling alpha waves” and portray predictive coding as a different rhythmic phenomena in the built environment, the body, and

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the brain, through modulations in cognition and behavior. Additionally, References


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Doktor Olsen, Dylan Chau Huynh, and Asbjørn Carstens for their valu­ Djebbara, Z., Jensen, O.B., Parada, F.J., Gramann, K., 2022. Neuroscience and
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