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).”

“2011), and magnetoencephalographic (MEG) (Todorovic et al. 2011) recordings.”

“Similarly, violating expectations of auditory repetition causes enhanced gamma-band responses in early auditory cortex (Todorovic et al., 2011).”

“This is in line with recent neurophysiological studies in monkeys and humans, highlighting that valid expectations lead to a reduction in spiking activity (Meyer and Olson, 2011) as well as gamma-band oscillatory activity (Todorovic et al., 2011).”

“Omission responses fit quite naturally within the predictive coding framework: If stimulus-evoked brain activity indexes the difference between a sensory signal and its top-down prediction, then, when the sensory signal is omitted, the evoked activity should reflect the pure prediction signal within the same cortical…”

“MMN to omission One of the most remarkable properties of the auditory system is that it can generate evoked responses to an absent but expected stimulus (Joutsiniemi and Hari, 1989; Raij et al., 1997; Yabe et al., 1997; Hughes et al., 2001; Todorovic et al., 2011; Wacongne et al., 2011).”

“, 2010; Meyer and Olson, 2011), auditory (Ulanovsky et al., 2003; Baldeweg, 2006; Todorovic et al., 2011), and somatosensory perception (Akatsuka et al.”

“…et al., 2010; Knill and Pouget, 2004; Rao and Ballard, 1999; Sterzer et al., 2008; Summerfield et al., 2006), there is growing support for the role of such a framework in explaining, for example, auditory (Moran et al., 2013; Todorovic et al., 2011) and interoceptive (Seth et al., 2011) responses.”

“In some cases, the absence of an expected stimulus should generate error activity (den Ouden et al., 2010; Todorovic et al., 2011; Wacongne et al., 2012).”

“, 2016), MEG (Wacongne et al., 2011; Todorovic et al., 2011; Todorovic and de Lange, 2012; Andreou et al, 2015; Chennu et al., 2016) and ECoG (Hughes et al.”

“These models account for several extraclassical receptive field effects (Rao and Ballard 1999; Spratling 2010) and are in line with empirical findings that predicted stimuli evoke reduced neural responses (Alink et al. 2010; den Ouden et al. 2010; Todorovic et al. 2011).”

“, 2006) where neural activity ceases in response to expected input in a manner consistent with prediction error minimization (Summerfield et al., 2008; Todorovic et al., 2011).”

“RS appears most noticeably present when stimulus repetitions are expected, and attenuated when they are infrequent (Summerfield et al., 2008; Todorovic et al., 2011).”

“MEG studies in humans have shown suppression of gamma-band synchrony (as well as evoked responses) in auditory cortex following an expected stimulus repetition, consistent with a successful mini-misation of the prediction error (Todorovic, van Ede, Maris, & de Lange, 2011).”

“This finding is convergent with previous MEG evidence of attenuation of early auditory responses to expected versus unexpected stimuli (Todorovic et al., 2011; Todorovic and de Lange, 2012).”

“This suggests that prior expectations modify sensory processing at the earliest stages by affecting not only the amplitude of neural responses (Summerfield et al., 2008; den Ouden et al., 2009; Alink et al., 2010; Todorovic et al., 2011; Kok et al., 2012b), or their sharpness (Kok et al.”

“12 Neuron 100, 1–15, December 5, 2018 Numerous human ECoG andMEG studies have demonstrated the correlation between prediction errors and the magnitude of g-band oscillations in audition (D€ urschmid et al., 2016; Edwards et al., 2005; Todorovic et al., 2011), vision (Brodski et al.”

“This is supported by human electro/magnetoencephalography (MEG/EEG) studies and a recent monkey electrocorticography study (Arnal and Giraud, 2012; Auksztulewicz and Friston, 2016; Bauer et al., 2006; Brodski et al., 2015; Chao et al., 2018; Mayer et al., 2016; van Pelt et al., 2016; Todorovic et al., 2011).”

“…studies have found evidence for biasing of activity of both the sensory areas encoding the evidence (Shulman et al., 1999; Preuschhof et al., 2010; Todorovic et al., 2011; Kok et al., 2012a,b) and associative areas related to action planning (Domenech and Dreher, 2010; Forstmann et al., 2010;…”

“Todorovic et al. (2011) studied prediction effects with tone pairs.”

“…Friston, 2016; Garrido, Kilner, Kiebel, et al., 2009; Grill-Spector, Henson, & Martin, 2006; Summerfield, Monti, Trittschuh, Mesulam, & Egner, 2008; Todorovic et al., 2011), that is, the attenuation of the evoked response to a certain repeated stimulus feature, and namely to a certain repeated…”

“In the third task (auditory task, ~6 min), brief tones (frequency 1000 Hz, duration 5 ms, ~70 dB SPL) were presented binaurally via MEG-compatible air tubes (Todorovic et al., 2011).”

“Other sequential effects, such as repetition suppression, may similarly be cast as the result of this same prior (Summerfield et al., 2008; Todorovic et al., 2011; Henson, 2015): if the world is generally stable, objects are more likely to repeat than change.”

“This theory is consistent with the repeated finding that BOLD signals to expected information tend to be suppressed rather than enhanced (Summerfield and Egner, 2009; Summerfield et al., 2008; Todorovic et al., 2011), as well as with a recent report that despite this ‘‘expectation suppression,’’ more probable signals…”

“In another recent report (Todorovic et al., 2011), expectation modulated RS of auditory evoked potentials observed using MEG, although these effects occurred somewhat earlier, perhaps because stimuli were presented in the auditory modality.”

“This dissociation, with fast frequencies relaying prediction errors and slower frequencies relaying predictions, is consistent with studies that have examined oscillatory responses during repetition suppression, auditory processing of expected and unexpected stimulus sequences, and auditory/visual speech processing (A…”

“Perceptual expectations influence the magnitude of neural adaptation (Costa-Faidella et al., 2011; Summerfield et al., 2008; Todorovic et al., 2011).”

“When a sequence of sounds is prematurely interrupted, early ( 100 ms) activity has been observed (Raij et al., 1997; Hughes et al., 2001; Bendixen et al., 2009; Todorovic et al., 2011; Wacongne et al., 2011).”

“…decade, research using techniques as diverse as noninvasive functional magnetic resonance imaging (fMRI) [1–4] and electro-and magnetoencephalography [5–8] in humans, as well as invasive animal electrophysiology [9–13], has revealed that prior expectations strongly modulate sensory processing [14].”

“The MMN can be explained by sensory adaptation (for a review see May and Tiitinen, 2010) or by an involvement of top–down expectations or their violation (e.g., Schröger and Wolff, 1996; see also Todorovic et al., 2011; Todorovic and de Lange, 2012).”

“The observed results could therefore be accounted for by assuming that continuous changes in expectancy attenuate the evoked responses to the offset tones closer to the SI (Lange, 2009; but see Bendixen et al., 2009; Todorovic et al., 2011; Wacongne et al., 2011; Todorovic and de Lange, 2012).”

“Neural activity in sensory cortex can be strongly modulated by prior expectations (Summerfield et al., 2008; den Ouden et al., 2009; Alink et al., 2010; Meyer and Olson, 2011; Todorovic et al., 2011; Wacongne et al., 2011; Kok et al., 2012, 2013; Bell et al., 2016; Kaposvari et al., 2016).”

“Prediction errors were coded in absolute differences, motivated by previous studies in the visual and auditory system (den Ouden et al., 2010; Todorovic et al., 2011; Todorovic and de Lange, 2012; Boll et al., 2013; Geuter et al., 2017).”

“In general, top-down connections are likely to play a significant role in mediating several forms of on-line learning of statistics (Todorovic et al. 2011, Hamm et al. 2018).”

“First evidence for PE signaling in GBA has been provided in recent MEG studies (Arnal et al., 2011; Todorovic et al., 2011; Bauer et al., 2014).”

“…question is particularly crucial because it has been suggested that reduction of neural signals at the lower level can be explained in terms of error minimization (Murray et al., 2002; Summerfield et al., 2008; den Ouden et al., 2009; Alink et al., 2010; Todorovic et al., 2011; Kok et al., 2012b).”

“…to sensory stimuli (Warren, 1970; Haist et al., 2001; Alain and Izenberg, 2003; Alain, 2007; Davis and Johnsrude, 2007; Fritz et al., 2007; Todorovic et al., 2011; Chennu et al., 2013; Kok et al., 2013), likely via modulation of infra- and supragranular pyramidal cells due to the…”

“This resembles repetition suppression (Grill-Spector et al. 2006), which has been proposed to reflect an effect of top-down perceptual expectations (Friston 2005; Summerfield et al. 2008; Todorovic et al. 2011).”

“Similarly, we have previously observed that activity elicited by tone omissions scales with the (im)probability of the omission [29].”

“However, timing prediction errors may be 635 observable in EEG/MEG through their effect on gamma oscillations [90, 91].”

“Todorovic et al. (2011) applied auditory stimulation and found that prior expectations increase the RS of both the evoked activity and gamma-band synchrony of the MEG signal.”

“Neural responses to omissions are taken to reflect pure neural prediction error, produced by the mismatch between top-down predictions and (absent) bottom-up input (Bendixen, Schröger, & Winkler, 2009; Friston, 2005; Todorovic, van Ede, Maris, & de Lange, 2011; Wacongne et al., 2011).”

“In the RS case, stimuli are more predictable because they are repeating and this leads to less prediction error and, therefore, less AC activity [108–111].”

“…previous studies which report modulations of the amplitude of sensory signals by expectation at ∼100-150 ms (Samaha et al., 2018; Stojanoski and Niemeier, 2015; Bar et al., 2006; Todorovic et al. 2011; Todorovic and De Lange, 2012; Wacongne et al., 2011; Meyer and Olson, 2011; Aru et al., 2016).”

“Concerning implicit timing tasks, it is important to mention earlier studies using oddball-like stimulation protocols to investigate timing or time-related processing [40,57–60].”

“A prediction for this experiment is that the CNV signal would be higher for rare, unexpected repeats than for common, expected ones, similar to other stimulus domains (Todorovic et al., 2011).”

“We expected to find strongest SSVEP amplitudes over the occipital region (as the primary visual cortex is known to be a principal source of SSVEP [Di Russo et al., 2007]) and strongest SWIFT amplitudes over more temporal and parietal regions (as SWIFT has been shown to increasingly activate higher…”

“…increasing stimulus repetition rate, leads to neural modulations in cortical regions where the expected stimulus is represented, that is, repetition effects (Friston, 2005; Henson, Shallice, & Dolan, 2000; Summerfield et al., 2008; Todorovic et al., 2011; Turk-Browne, Yi, Leber, & Chun, 2007).”

“On the other hand, the suppression may be a consequence of top-down predictions and could be explained via the theory of predictive coding (Summerfield et al., 2008; Todorovic et al., 2011).”

“…at least in human macroscopic brain responses, is stronger for expected than for unexpected stimuli (Costa-Faidella et al. 2011; Lange 2009; Summerfield et al. 2008; Todorovic et al. 2011; Wacongne et al. 2011; however, see Farley et al. 2010 for contrary evidence in animal multiunit recordings).”

“A boost of gamma oscillations at the expense of lower frequencies [51,52] has often been reported as a correlate of predictability of targets [9,15,50,53,54].”

“…have found an increased neural response to unexpected stimuli (Summerfield et al., 2008;den Ouden et al., 2009;Alink et al., 2010;Meyer and Olson, 2011;Todorovic et al., 2011;Wacongne et al., 2011), including some using an almost identical paradigm as the current study (Kok et al., 2012, 2016b).”

“…size of adaptation effect on hemodynamic responses (visual: Summerfield et al., 2008; Kovács et al., 2012; Grotheer and Kovács, 2014; Mayrhauser et al., 2014; auditory: Andics et al., 2013) and electrophysiological responses (visual: Summerfield et al., 2011; auditory: Todorovic et al., 2011).”

“…higher frequencies under predictable stimulation conditions is consistent with previous reports of gammaband synchronization and alpha-band desynchronization due to contextual predictability (Arnal et al., 2011; Todorovic et al., 2011; Bauer et al., 2014; Brodski et al., 2015; Sedley et al., 2016).”

“Whether neural adaptation mechanistically supports the generation of sensory predictions is a question that requires further studies in which manipulation of predictability are not confounded with physical stimulus manipulations (see also Todorovic et al., 2011).”

“Although response attenuation in self-generation paradigms is partially attributable to expectation-related feedback (Todorovic et al., 2011; Rummell et al., 2016), recent experiments suggest that it also depends at least in part on independent feedback generated by motor responses (Rummell et al.”

“Interestingly, for tonal material it has recently been revealed that the supposedly simple mechanism of repetition suppression at least partly reflects higher-level predictions rather than just physical effects (Todorovic et al., 2011).”

“when presenting pairs of tones), than when they are unexpected, suggesting the role of top-down expectations [46].”

“For example, auditory adaptation in response to repeated sounds is larger for expected versus unexpected stimuli (Todorovic et al., 2011).”

“the opportunity to not only detect non–phase-locked oscillatory responses but to also to record phase-locked evoked responses and to determine their role in signaling sensory information, expectations, and PEs as previously done in other modalities (59, 60).”