Feedback contribution to surface motion perception in the human early visual cortex
- Maastricht University, Netherlands
- University Health Network, Canada
Abstract
Human visual surface perception has neural correlates in early visual cortex, but the role of feedback during surface segmentation in human early visual cortex remains unknown. Feedback projections preferentially enter superficial and deep anatomical layers, which provides a hypothesis for the cortical depth distribution of fMRI activity related to feedback. Using ultra-high field fMRI, we report a depth distribution of activation in line with feedback during the (illusory) perception of surface motion. Our results fit with a signal re-entering in superficial depths of V1, followed by a feedforward sweep of the re-entered information through V2 and V3. The magnitude and sign of the BOLD response strongly depended on the presence of texture in the background, and was additionally modulated by the presence of illusory motion perception compatible with feedback. In summary, the present study demonstrates the potential of depth-resolved fMRI in tackling biomechanical questions on perception.
Data availability
The fMRI dataset, experimental stimuli, and analysis code are publicly available. The fMRI dataset is available on Zenodo (https://doi.org/10.5281/zenodo.3366301). The software used for the presentation of retinotopic mapping stimuli, and for the corresponding analysis, is available on github (https://github.com/ingo-m/pyprf). Example videos of the main experimental stimuli are available on Zenodo (https://doi.org/10.5281/zenodo.2583017). If you would like to reproduce the experimental stimuli, the respective PsychoPy code can be found on github (https://github.com/ingo-m/PacMan/tree/master/stimuli/experiment). The respective repository also contains the analysis code and a brief description how to reproduce the analysis (https://github.com/ingo-m/PacMan). High-level visualisations (e.g. cortical depth profiles & signal timecourses) and group-level statistical tests are implemented in a separate repository (https://github.com/ingo-m/py_depthsampling/tree/PacMan).
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Dataset: Feedback contribution to surface motion perception in the human early visual cortexZenodo, doi.org/10.5281/zenodo.3366301.
Article and author information
Author details
Funding
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-11-002)
- Kâmil Uludağ
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (406-14-085)
- Ingo Marquardt
- Kâmil Uludağ
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: Healthy participants gave informed consent before the experiment, and the study protocol was approved by the local ethics committee of the Faculty for Psychology & Neuroscience, Maastricht University. (reference number: ERCPN 180_03_06_2017 ).
Copyright
© 2020, Marquardt et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Feedback contribution to surface motion perception in the human early visual cortex
eLife 9:e50933.
https://doi.org/10.7554/eLife.50933
Further reading
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The infralimbic cortex (IL) is essential for flexible behavioral responses to threatening environmental events. Reactive behaviors such as freezing or flight are adaptive in some contexts, but in others a strategic avoidance behavior may be more advantageous. IL has been implicated in avoidance, but the contribution of distinct IL neural subtypes with differing molecular identities and wiring patterns is poorly understood. Here, we study IL parvalbumin (PV) interneurons in mice as they engage in active avoidance behavior, a behavior in which mice must suppress freezing in order to move to safety. We find that activity in inhibitory PV neurons increases during movement to avoid the shock in this behavioral paradigm, and that PV activity during movement emerges after mice have experienced a single shock, prior to learning avoidance. PV neural activity does not change during movement toward cued rewards or during general locomotion in the open field, behavioral paradigms where freezing does not need to be suppressed to enable movement. Optogenetic suppression of PV neurons increases the duration of freezing and delays the onset of avoidance behavior, but does not affect movement toward rewards or general locomotion. These data provide evidence that IL PV neurons support strategic avoidance behavior by suppressing freezing.
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Recognizing and responding to threat cues is essential to survival. Freezing is a predominant threat behavior in rats. We have recently shown that a threat cue can organize diverse behaviors beyond freezing, including locomotion (Chu et al., 2024). However, that experimental design was complex, required many sessions, and had rats receive many foot shock presentations. Moreover, the findings were descriptive. Here, we gave female and male Long Evans rats cue light illumination paired or unpaired with foot shock (eight total) in a conditioned suppression setting using a range of shock intensities (0.15, 0.25, 0.35, or 0.50 mA). We found that conditioned suppression was only observed at higher foot shock intensities (0.35 mA and 0.50 mA). We constructed comprehensive temporal ethograms by scoring 22,272 frames across 12 behavior categories in 200-ms intervals around cue light illumination. The 0.50 mA and 0.35 mA shock-paired visual cues suppressed reward seeking, rearing, and scaling, as well as light-directed rearing and light-directed scaling. These shock-paired visual cues further elicited locomotion and freezing. Linear discriminant analyses showed that ethogram data could accurately classify rats into paired and unpaired groups. Using complete ethogram data produced superior classification compared to behavior subsets, including an immobility subset featuring freezing. The results demonstrate diverse threat behaviors – in a short and simple procedure – containing sufficient information to distinguish the visual fear conditioning status of individual rats.
