Prior Expectation Mediates Neural Adaptation to Repeated Sounds in the Auditory Cortex: An MEG Study

“It is well possible that expectation-related modulations are more pervasive in early sensory than later stages of cortical processing (Rao and Ballard, 1999).”

“…of repeated stimuli was unexpected (functional magnetic resonance imaging (fMRI): Summerfield et al., 2008; Kovács et al., 2012; Grotheer and Kovács, 2014; Mayrhauser et al., 2014; magnetoencephalography (MEG): Todorovic et al., 2011; electroencephalography (EEG): Summerfield et al., 2011).”

“Auditory expectations sharpen neural responses to relevant stimulus features (Fritz et al., 2003; Todorovic et al., 2011), which may underlie our behavioral outcomes showing overall faster response times when the target words were preceded by an adapting carrier phrase.”

“…i.e. the fact that the neural responses observed for various stimuli are often found to be attenuated when repeated (Dehaene et al., 2001; Orfanidou et al., 2006; Raichle et al., 1994; Schacter and Buckner, 1998; Summerfeld et al., 2011; Summerfield et al., 2008; Todorovic et al., 2011).”

“This seems like the omission MMN, which is elicited when an expected stimulus is omitted in an oddball experimental paradigm (Raij et al., 1997; May and Tiitinen, 2010; Todorovic et al., 2011; SanMiguel et al., 2013).”

“Todorovic et al. (2011) presented trials of two tones where the second tone was either an identical repetition of the first one or omitted.”

“In the whole-cortex mapping, individual subjects' noise-normalized MNEs (dSPM) of the difference responses between the ARepeatVChange and AVRepeat conditions were averaged over time windows, to mitigate the inter-subject variability of regional time courses and to reduce the number of statistical comparisons (see, e.g…”

“…initial perceptual processing occurring around 100 – 150 ms after stimulus onset (Alilovi ´ c et al., 2019; Aru et al., 2016; Hsu et al., 2015; Todorovic et al., 2011; Wacongne et al., 2011), or earlier at the level of C1 component ( < 80 ms post-stimulus; Jabar et al., 2017), or even before…”

“For another, it can establish an internal model of expected stimulation, such that each expected repetition further reduces the neural response [expectation suppression (Todorovic et al., 2011)], while an unpredicted deviant triggers an increase in neural response known as prediction error (Wacongne et al.”

“Moreover, to minimize the risk of error-driven fluctuations in neural responses, optimum perceptual adjustments to some subtle or rare environmental alterations, like our skew distortions, might be rather slow (Todorovic et al., 2011; Wark et al., 2009).”

“…a neuronal correlate of expectancy for the S2 stimulus that ollows the presentation of the S1 stimulus ( Mento, 2013 ; Mento et al., 015 ; van Boxtel and Brunia, 1994 a, Bickel et al., 2012 ; Chennu et al., 013 ; Tecce, 1972 ; Donchin et al., 1972 ; Naatanen and Gaillard, 1974 ; amano et…”

“Den Ouden, Kok, & De Lange, 2012; Kok, Jehee, & de Lange, 2012; Meyer & Olson, 2011; Richter, Ekman, & de Lange, 2018; Todorovic, van Ede, Maris, & de Lange, 2011), which is typically observed during the initial processing cascade in sensory cortices associated with the unexpected stimulus (Tang,…”

“The rise of the predictive brain frameworks stimulated numerous studies designed to detect correlates, networks, and consequences of predictions and prediction errors (e.g., Alink et al., 2010; de Gardelle et al. 2013; Todorovic et al. 2011).”

“As updating predictions involves modifying sensory representations, this should affect perceptual sensitivity on subsequent trials (Alink et al., 2010; St. John-Saaltink et al., 2016; Summerfield et al., 2008; Todorovic et al., 2011; Wacongne et al., 2011).”

“Gamma activity increases in sensory areas during presentation of unexpected stimuli (Arnal et al., 2011; Gurtubay et al., 2001; Todorovic et al., 2011), and therefore we expected visual gamma activity in supragranular layers to be greater following incongruent instruction cues than after congruent…”

“Recent studies suggest that the reduction in cortical activity results from the stimulus becoming progressively more precisely predicted (Todorovic and de Lange 2012; Todorovic et al. 2011; Andics et al. 2013; Summerfield et al. 2011; Sum-merfield et al. 2008).”

“Some fMRI or MEG studies also examined how predictability influences early perceptual processing and found that predicted stimuli evoke reduced neural responses in the early visual/auditory cortex (Alink et al., 2010; den Ouden et al., 2010; Todorovic et al., 2011; Sohoglu et al., 2012).”

“Mounting evidence of the N1/N1m predictability effect further supports that it indicates the operation of an internal predictive mechanism, as predicted stimuli were associated with robust N1/N1m suppression (Schafer and Marcus, 1973; Schafer et al., 1981; Lange, 2009; Todorovic et al., 2011; Todorovic and de Lange, 2…”

“More recent studies have shown that top-down processes contribute toward repetition suppression (32, 33).”

“…(Malmierca et al., 2009), functional magnetic resonance imaging (fMRI) (Larsson and Smith, 2012; Grotheer and Gyula, 2015), electroencephalography (Costa-Faidella et al., 2011; Summerfield et al., 2011), and magnetoencephalography (Todorovic et al., 2011; Todorovic and de Lange, 2012).”

“The two tone frequencies have been used in prior auditory oddball studies (Todorovic et al., 2011; Cervenka et al., 2013).”

“…as expected stimuli also led to suppressed activity, possibly signalling the reduced prediction errors (Schafer and Marcus, 1973; Schafer et al., 1981; Lange, 2009; Todorovic et al., 2011; Todorovic and de Lange, 2012; SanMiguel et al., 2013; Timm et al., 2013; Hsu et al., 2014a, 2014b, 2016).”

“The illustration of sound feature specific neural activity during ‘ surprising ’ silent periods goes beyond the demonstration of a general reaction of the brain, known as evoked or induced omission responses (Raij et al., 1997; Todorovic et al., 2011).”

“The Bayesian framework was first applied to the visual system and has since gained acceptance across a wide range of research areas, including auditory, interoceptive, neuropsychiatric, and even social fields [4–7].”

“…assessed and verified in the field of sensory perception, particularly for vision (Rao and Ballard, 1999; Murray et al., 2002) and audition (Todorovic et al., 2011) and subsequently, with mutual conceptual input, for interoception (Seth et al., 2011, reviewed in Van den Bergh et al., 2017)…”

“” Finding no index of implicit expectation, diverges from previous studies that have shown that stimulus repetition can build strong expectations and influence the brain response without attention focused on the sounds (Todorovic et al., 2011).”

“Recent findings indicate that beta oscillations correlate not only with different types of movement but also with the temporal structure of the task (Arnal et al., 2011; Todorovic et al., 2011).”

“Stimulus repetition is thought to result in the attenuation of PE (Summerfield et al., 2008, 2011; Costa-Faidella et al., 2011; Todorovic et al., 2011; Wacongne et al., 2012; Andics et al., 2013; Emberson et al., 2019).”

“The OR in the absence of attention is localized in the auditory cortex (AC) (Raij et al., 1997; Todorovic et al., 2011), which may be involved in prediction and pre-attentive perceptual grouping.”

“This is in line with the notion that responses to repeated sounds are not only caused by simple mechanisms as neural fatigue, but are likely to be caused by fulfilled expectations (Auksztulewicz & Friston, 2016; Summerfield et al., 2008; Todorovic et al., 2011) including forward message passing of prediction error and…”

“Recently, evidence supporting this has come from Todorovic and colleagues [13], who showed that repetition suppression depends on expectation.”

“In an MEG study with pure tones, Todorovic et al., (2011) employed a comparable design and observed a robust RS in the auditory cortex for repeated tones, with a significantly greater reduction in evoked neural activity and gamma-band synchrony for expected than for unexpected repetitions.”

“For example, prior expectations drive attention and active sensing 36,37 , which modulates sensory encoding 11,15,38,39 and improves sensory acuity 12–14,”

“Alaminos et al., 2021; Garrido et al., 2008, 2009; Lieder et al., 2013; Todorovic et al., 2011; Winkler & Czigler, 2012).”

“Both studies related to general sensory processing and those related to speech processing have demonstrated that prediction reduces sensory activities (e. g., Alink et al. 2010; den Ouden et al. 2010; Todorovic et al. 2011; Sohoglu et al. 2012), and thus have provided supporting evidence for the predictive coding theo…”

“…on the P3, where P3 activity is modulated when the model or context of a stimulus environment needs to be updated (Donchin, 1981; Donchin and Coles, 1988; Polich and Kok, 1995; Todorovic et al., 2011; Seppänen et al., 2012; Silverstein et al., 2015; Bang and Rahnev, 2017; Li et al., 2018).”

“However, (Bendixen et al., 2009) experiment and other previous studies (SanMiguel, Saupe, & Schröger, 2013; Todorovic et al., 2011; Todorovic & Lange, 2012; Wacongne et al., 2011) The present study implemented a stimulation protocol that unambiguously allowed us to assess the first neural response…”

“Because we were mainly interested in the cortical distribution of the omission-related response, which was found in the time window of 100–200 ms after the omission onset in the previous studies (Yabe et al., 1998; R€usseler et al., 2001; Bendixen et al., 2009; Horv ath et al., 2010; Todorovic et al., 2011; Wacongne e…”

“In contrast, temporal predictability has also been reported to suppress cortical and brainstem potentials (Lange 2009; Costa-Faidella et al. 2011; Todorovic et al. 2011; Gorina-Careta et al. 2016), which could be evidence of the predictive coding hypothesis, which posits that the neural responses to expected stimuli s…”

“…areas measuring the mismatch negativity (MNN), a component of the event-related potentials assumed to encode prediction error (Cornella et al. 2012; Costa-Faidella et al. 2011; Dürschmid et al. 2016; Lecaignard et al. 2015; Phillips et al. 2016; Todorovic and de Lange 2012; Todorovic et al. 2011).”

“Similar adaptation has been previously described with repeated acoustic stimulations [46] as well as with 40 Hz combined visual and auditory entrainment [18].”

“Additionally, the participant-related variables such as expectations and attention also play a role (e.g. Costa-Faidella, Baldeweg, et al., 2011; Hari et al., 1979; Herholz et al., 2009; Todorovic et al., 2011).”

“Decreased neural responses for predictable sensory events are considered as the hallmark of predictive processing, and indeed they have been reported in numerous studies (e.g., Alink et al., 2010; Todorovic et al., 2011; de Gardelle et al., 2013).”

“Prior research indicates a top-down mediation of repetition suppression by probabilistic manipulation in the early auditory cortex (Todorovic et al., 2011).”

“Reduction in repetition suppression by unexpected stimuli has also been found using fMRI (Andics et al., 2013) and M/EEG (Summer fi eld et al., 2008; Todorovic et al., 2011; Todorovic & de Lange, 2012).”

“The adjusted prediction would then be transmitted down-ward to generate expectations at a lower level, suppressing the prediction error (Garrido et al., 2007, 2009; Parmentier et al., 2011; Todorovi ć et al., 2011).”

“, 2006), MEG (Rosburg, 2004; Todorovic et al., 2011) and fMRI (Grill-Spector et al.”

“This finding aligns with other neuroimaging evidence supporting the sharpening account ( den Ouden et al., 2008; Todorovic et al., 2011).”

“Second, the phonological modulation on N1 habituation is unlikely to be caused by general cognitive functions, such as expectation [29] and selective attention [26], which are not specific to linguistic processing.”

“This coding scheme can account for many properties of how neurons behave in early visual cortex [2, 4], and has received indirect support from neuroimaging [3, 5–8] and electrophysiology [9, 10] in humans, and from electrophysiology in monkeys [11].”