Cargando…

Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex

Perception has been proposed to result from the integration of feedforward sensory signals with internally generated feedback signals. Feedback signals are believed to play an important role in driving false percepts, that is, seeing things that are not actually there. Feedforward and feedback influ...

Descripción completa

Detalles Bibliográficos
Autores principales: Haarsma, Joost, Deveci, Narin, Corbin, Nadege, Callaghan, Martina F., Kok, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10669763/
https://www.ncbi.nlm.nih.gov/pubmed/37739797
http://dx.doi.org/10.1523/JNEUROSCI.0998-23.2023
_version_ 1785149251672604672
author Haarsma, Joost
Deveci, Narin
Corbin, Nadege
Callaghan, Martina F.
Kok, Peter
author_facet Haarsma, Joost
Deveci, Narin
Corbin, Nadege
Callaghan, Martina F.
Kok, Peter
author_sort Haarsma, Joost
collection PubMed
description Perception has been proposed to result from the integration of feedforward sensory signals with internally generated feedback signals. Feedback signals are believed to play an important role in driving false percepts, that is, seeing things that are not actually there. Feedforward and feedback influences on perception can be studied using layer-specific fMRI, which we used here to interrogate neural activity underlying high-confidence false percepts while healthy human participants (N = 25, male and female) performed a perceptual orientation discrimination task. Auditory cues implicitly signaled the most likely upcoming orientation (referred to here as expectations). These expectations induced orientation-specific templates in the deep and superficial layers of V2, without affecting perception. In contrast, the orientation of falsely perceived stimuli with high confidence was reflected in the middle input layers of V2, suggesting a feedforward signal contributing to false percepts. The prevalence of high-confidence false percepts was related to everyday hallucination severity in a separate online sample (N = 100), suggesting a possible link with abnormal perceptual experiences. These results reveal a potential feedforward mechanism underlying false percepts, reflected by spontaneous stimulus-like activity in the input layers of the visual cortex, independent of top-down signals reflecting cued orientations. SIGNIFICANCE STATEMENT False percepts have been suggested to arise through excessive feedback signals. However, feedforward contributions to false percepts have remained largely understudied. Laminar fMRI has been shown to be useful in distinguishing feedforward from feedback activity as it allows the imaging of different cortical layers. In the present study we demonstrate that although cued orientations are encoded in the feedback layers of the visual cortex, the content of the false percepts are encoded in the feedforward layers and did not rely on these cued orientations. This shows that false percepts can in principle emerge from random feedforward signals in the visual cortex, with possible implications for disorders hallmarked by hallucinations like schizophrenia and Parkinson's disease.
format Online
Article
Text
id pubmed-10669763
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Society for Neuroscience
record_format MEDLINE/PubMed
spelling pubmed-106697632023-11-22 Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex Haarsma, Joost Deveci, Narin Corbin, Nadege Callaghan, Martina F. Kok, Peter J Neurosci Research Articles Perception has been proposed to result from the integration of feedforward sensory signals with internally generated feedback signals. Feedback signals are believed to play an important role in driving false percepts, that is, seeing things that are not actually there. Feedforward and feedback influences on perception can be studied using layer-specific fMRI, which we used here to interrogate neural activity underlying high-confidence false percepts while healthy human participants (N = 25, male and female) performed a perceptual orientation discrimination task. Auditory cues implicitly signaled the most likely upcoming orientation (referred to here as expectations). These expectations induced orientation-specific templates in the deep and superficial layers of V2, without affecting perception. In contrast, the orientation of falsely perceived stimuli with high confidence was reflected in the middle input layers of V2, suggesting a feedforward signal contributing to false percepts. The prevalence of high-confidence false percepts was related to everyday hallucination severity in a separate online sample (N = 100), suggesting a possible link with abnormal perceptual experiences. These results reveal a potential feedforward mechanism underlying false percepts, reflected by spontaneous stimulus-like activity in the input layers of the visual cortex, independent of top-down signals reflecting cued orientations. SIGNIFICANCE STATEMENT False percepts have been suggested to arise through excessive feedback signals. However, feedforward contributions to false percepts have remained largely understudied. Laminar fMRI has been shown to be useful in distinguishing feedforward from feedback activity as it allows the imaging of different cortical layers. In the present study we demonstrate that although cued orientations are encoded in the feedback layers of the visual cortex, the content of the false percepts are encoded in the feedforward layers and did not rely on these cued orientations. This shows that false percepts can in principle emerge from random feedforward signals in the visual cortex, with possible implications for disorders hallmarked by hallucinations like schizophrenia and Parkinson's disease. Society for Neuroscience 2023-11-22 /pmc/articles/PMC10669763/ /pubmed/37739797 http://dx.doi.org/10.1523/JNEUROSCI.0998-23.2023 Text en Copyright © 2023 Haarsma et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Haarsma, Joost
Deveci, Narin
Corbin, Nadege
Callaghan, Martina F.
Kok, Peter
Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex
title Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex
title_full Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex
title_fullStr Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex
title_full_unstemmed Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex
title_short Expectation Cues and False Percepts Generate Stimulus-Specific Activity in Distinct Layers of the Early Visual Cortex
title_sort expectation cues and false percepts generate stimulus-specific activity in distinct layers of the early visual cortex
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10669763/
https://www.ncbi.nlm.nih.gov/pubmed/37739797
http://dx.doi.org/10.1523/JNEUROSCI.0998-23.2023
work_keys_str_mv AT haarsmajoost expectationcuesandfalseperceptsgeneratestimulusspecificactivityindistinctlayersoftheearlyvisualcortex
AT devecinarin expectationcuesandfalseperceptsgeneratestimulusspecificactivityindistinctlayersoftheearlyvisualcortex
AT corbinnadege expectationcuesandfalseperceptsgeneratestimulusspecificactivityindistinctlayersoftheearlyvisualcortex
AT callaghanmartinaf expectationcuesandfalseperceptsgeneratestimulusspecificactivityindistinctlayersoftheearlyvisualcortex
AT kokpeter expectationcuesandfalseperceptsgeneratestimulusspecificactivityindistinctlayersoftheearlyvisualcortex