Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study

Fonken, Yvonne M.; Mukerji, Arjun; Jimenez, Richard; Lin, Jing; Brunner, Peter; Schalk, Gerwin; Rt, Knight

doi:10.1101/733212

Cited by 8 publications

(10 citation statements)

References 49 publications

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“…Intracranial studies in humans confirmed mixed contributions of deviance detection and adaptation to mismatch responses in auditory cortices (Ishishita et al, 2019). Furthermore, such studies provided indications that cortical processing is not spatially homogeneous (Hughes et al, 2001;Flinker et al, 2011;Fonken et al, 2019) and that adaptation and deviance detection responses can be differently distributed (Blenkmann et al, 2019;Ishishita et al, 2019), indicating the existence of specialized, interconnected sub-regions within the auditory stream for the processing of contextual information. Thus, animal studies make it possible to dissect the distinctive contributions of different interneuron populations to networklevel SSA (Natan et al, 2017) and deviance detection mechanisms (Ross and Hamm, 2020) that are likely to underlie similar processes observed in humans.…”

Section: Mmn As a Major Biomarker Of Predictionmentioning

confidence: 92%

Neural Substrates and Models of Omission Responses and Predictive Processes

Braga

Schönwiesner

2022

Front. Neural Circuits

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Predictive coding theories argue that deviance detection phenomena, such as mismatch responses and omission responses, are generated by predictive processes with possibly overlapping neural substrates. Molecular imaging and electrophysiology studies of mismatch responses and corollary discharge in the rodent model allowed the development of mechanistic and computational models of these phenomena. These models enable translation between human and non-human animal research and help to uncover fundamental features of change-processing microcircuitry in the neocortex. This microcircuitry is characterized by stimulus-specific adaptation and feedforward inhibition of stimulus-selective populations of pyramidal neurons and interneurons, with specific contributions from different interneuron types. The overlap of the substrates of different types of responses to deviant stimuli remains to be understood. Omission responses, which are observed both in corollary discharge and mismatch response protocols in humans, are underutilized in animal research and may be pivotal in uncovering the substrates of predictive processes. Omission studies comprise a range of methods centered on the withholding of an expected stimulus. This review aims to provide an overview of omission protocols and showcase their potential to integrate and complement the different models and procedures employed to study prediction and deviance detection.This approach may reveal the biological foundations of core concepts of predictive coding, and allow an empirical test of the framework’s promise to unify theoretical models of attention and perception.

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Section: Mmn As a Major Biomarker Of Predictionmentioning

confidence: 92%

Neural Substrates and Models of Omission Responses and Predictive Processes

Braga

Schönwiesner

2022

Front. Neural Circuits

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“…To our knowledge, only one study using EEG has found what may be an MMN or P3a‐like response to a stimulus using an SOA of 1 s, but the responses were small and variable, limiting the researchers' interpretation of the ERPs (Busse & Woldorff, 2003). However, intracranial recordings (Fonken et al, 2019; Halgren et al, 1995) have found specific responses, including increased high frequency power, to sound omissions, even with SOAs larger than 200 ms. Thus, it remains an open question whether MMN and P3a measured in EEG reflect predictive errors for unexpected omissions.…”

Section: Introductionmentioning

confidence: 99%

The sound of silence: Predictive error responses to unexpected sound omission in adults

Prete

Heikoop

McGillivray

et al. 2022

Eur J of Neuroscience

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The human auditory system excels at detecting patterns needed for processing speech and music. According to predictive coding, the brain predicts incoming sounds, compares predictions to sensory input and generates a prediction error whenever a mismatch between the prediction and sensory input occurs. Predictive coding can be indexed in electroencephalography (EEG) with the mismatch negativity (MMN) and P3a, two components of event‐related potentials (ERP) that are elicited by infrequent deviant sounds (e.g., differing in pitch, duration and loudness) in a stream of frequent sounds. If these components reflect prediction error, they should also be elicited by omitting an expected sound, but few studies have examined this. We compared ERPs elicited by infrequent randomly occurring omissions (unexpected silences) in tone sequences presented at two tones per second to ERPs elicited by frequent, regularly occurring omissions (expected silences) within a sequence of tones presented at one tone per second. We found that unexpected silences elicited significant MMN and P3a, although the magnitude of these components was quite small and variable. These results provide evidence for hierarchical predictive coding, indicating that the brain predicts silences and sounds.

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“…This is in contrast to a recent study that used relatively low-spatial resolution surface electrodes to measure broad local field potentials in human superior temporal gyrus, which contains higher auditory areas than we typically examined. This study reported neuronal populations that responded only to omitted sounds, but not to presented sounds (Fonken et al, 2019).…”

Section: Discussionmentioning

confidence: 96%

“…Earlier human studies have suggested that omission responses can be observed only for relatively fast stimulus presentation rates, well above 5 Hz (Yabe et al, 1997), which was interpreted as a limited window of temporal integration. However, mounting evidence demonstrates that omission responses can also be observed in awake humans following longer inter-stimulus intervals, in the sub-second (Fonken et al, 2019; Halgren et al, 1995) and supra-second range (Busse and Woldorff, 2003). Omission responses at different time scales may be differentially influenced by cognitive factors: for instance, omissions following short ISIs (periodicity > 5 Hz) have been suggested to be elicited entirely automatically, while slower time scales (periodicity < 2 Hz) may be modulated by attention (Chennu et al, 2016; Chien et al, 2019; Karamürsel and Bullock, 2000), but see (Hughes et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

“…However, rather than altering the expected stimulus, it can instead be omitted, enabling observations of the form and timing of predictive signals that are not confounded by processing of incoming stimuli (Schröger et al, 2015). Although omission responses have often been reported using measurements of neural activity in humans that are non-invasive (Bendixen et al, 2009; Chennu et al, 2016; Dercksen et al, 2020; Raij et al, 1997; Sanmiguel et al, 2013; Todorovic et al, 2011; Wacongne et al, 2012; Yabe et al, 1997) or from the cortical surface (Fonken et al, 2019; Hughes et al, 2001), there has been little investigation at a detailed level by using penetrating electrodes.…”

Section: Introductionmentioning

confidence: 99%

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Omission responses in field potentials but not spikes in rat auditory cortex

Auksztulewicz

Rajendran

Peng

et al. 2022

Preprint

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Non-invasive recordings of gross neural activity in humans often show responses to omitted stimuli in steady trains of identical stimuli. This has been taken as evidence for the neural coding of prediction or prediction error. However, evidence for such omission responses from invasive recordings of cellular-scale responses in animal models is scarce. Here, we sought to characterise omission responses using extracellular recordings in the auditory cortex of anaesthetised rats. We profiled omission responses across local field potentials (LFP), analogue multiunit activity (AMUA), and single/multi-unit spiking activity, using stimuli that were fixed-rate trains of acoustic noise bursts where 5% of bursts were randomly omitted. Significant omission responses were observed in LFP and AMUA signals, but not in spiking activity. These omission responses had a lower amplitude and longer latency than burst-evoked sensory responses, and omission response amplitude increased as a function of the number of preceding bursts. Contrary to theories of neural entrainment, rhythmic stimulus presentation did not increase low-frequency phase-locking of neural activity specific to the stimulus presentation rate. Together, our findings show that omission responses are observed in LFP and AMUA signals, with laminar specificity, but are not observed in spiking activity, and do not show evidence for low-frequency phase locking. This has implications for models of cortical processing that require many neurons to encode prediction error in their spike output, and is consistent with models involving representation of prediction error in apical dendrites electrotonically distant from the soma.

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Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study

Cited by 8 publications

References 49 publications

Neural Substrates and Models of Omission Responses and Predictive Processes

Neural Substrates and Models of Omission Responses and Predictive Processes

The sound of silence: Predictive error responses to unexpected sound omission in adults

Omission responses in field potentials but not spikes in rat auditory cortex

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