Omission responses in local field potentials in rat auditory cortex

Abstract Background 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 in...

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Main Authors: Ryszard Auksztulewicz, Vani Gurusamy Rajendran, Fei Peng, Jan Wilbert Hendrik Schnupp, Nicol Spencer Harper
Format: Article
Language:English
Published: BMC 2023-05-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-023-01592-4
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author Ryszard Auksztulewicz
Vani Gurusamy Rajendran
Fei Peng
Jan Wilbert Hendrik Schnupp
Nicol Spencer Harper
author_facet Ryszard Auksztulewicz
Vani Gurusamy Rajendran
Fei Peng
Jan Wilbert Hendrik Schnupp
Nicol Spencer Harper
author_sort Ryszard Auksztulewicz
collection DOAJ
description Abstract Background 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. Results 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. Conclusions Together, our findings show that omission responses are most robustly observed in LFP and AMUA signals (relative to spiking activity). This has implications for models of cortical processing that require many neurons to encode prediction errors in their spike output.
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spelling doaj.art-4d33411744254a60a47f869aaed8f5a42023-06-04T11:38:32ZengBMCBMC Biology1741-70072023-05-0121111610.1186/s12915-023-01592-4Omission responses in local field potentials in rat auditory cortexRyszard Auksztulewicz0Vani Gurusamy Rajendran1Fei Peng2Jan Wilbert Hendrik Schnupp3Nicol Spencer Harper4Center for Cognitive Neuroscience Berlin, Free University BerlinDept of Neuroscience, City University of Hong KongDept of Neuroscience, City University of Hong KongDept of Neuroscience, City University of Hong KongDept of Physiology, Anatomy and Genetics, University of OxfordAbstract Background 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. Results 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. Conclusions Together, our findings show that omission responses are most robustly observed in LFP and AMUA signals (relative to spiking activity). This has implications for models of cortical processing that require many neurons to encode prediction errors in their spike output.https://doi.org/10.1186/s12915-023-01592-4Predictive processingAuditory processingOmission responsesElectrophysiologyAuditory cortex
spellingShingle Ryszard Auksztulewicz
Vani Gurusamy Rajendran
Fei Peng
Jan Wilbert Hendrik Schnupp
Nicol Spencer Harper
Omission responses in local field potentials in rat auditory cortex
BMC Biology
Predictive processing
Auditory processing
Omission responses
Electrophysiology
Auditory cortex
title Omission responses in local field potentials in rat auditory cortex
title_full Omission responses in local field potentials in rat auditory cortex
title_fullStr Omission responses in local field potentials in rat auditory cortex
title_full_unstemmed Omission responses in local field potentials in rat auditory cortex
title_short Omission responses in local field potentials in rat auditory cortex
title_sort omission responses in local field potentials in rat auditory cortex
topic Predictive processing
Auditory processing
Omission responses
Electrophysiology
Auditory cortex
url https://doi.org/10.1186/s12915-023-01592-4
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AT feipeng omissionresponsesinlocalfieldpotentialsinratauditorycortex
AT janwilberthendrikschnupp omissionresponsesinlocalfieldpotentialsinratauditorycortex
AT nicolspencerharper omissionresponsesinlocalfieldpotentialsinratauditorycortex