Learning dynamics of electrophysiological brain signals during human fear conditioning

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Abstract

Electrophysiological studies in rodents allow recording neural activity during threats with high temporal and spatial precision. Although fMRI has helped translate insights about the anatomy of underlying brain circuits to humans, the temporal dynamics of neural fear processes remain opaque and require EEG. To date, studies on electrophysiological brain signals in humans have helped to elucidate underlying perceptual and attentional processes, but have widely ignored how fear memory traces evolve over time. The low signal-to-noise ratio of EEG demands aggregations across high numbers of trials, which will wash out transient neurobiological processes that are induced by learning and prone to habituation. Here, our goal was to unravel the plasticity and temporal emergence of EEG responses during fear conditioning. To this end, we developed a new sequential-set fear conditioning paradigm that comprises three successive acquisition and extinction phases, each with a novel CS+/CS- set. Each set consists of two different neutral faces on different background colors which serve as CS+ and CS-, respectively. Thereby, this design provides sufficient trials for EEG analyses while tripling the relative amount of trials that tap into more transient neurobiological processes. Consistent with prior studies on ERP components, data-driven topographic EEG analyses revealed that ERP amplitudes were potentiated during time periods from 33–60 ms, 108–200 ms, and 468–820 ms indicating that fear conditioning prioritizes early sensory processing in the brain, but also facilitates neural responding during later attentional and evaluative stages. Importantly, averaging across the three CS+/CS- sets allowed us to probe the temporal evolution of neural processes: Responses during each of the three time windows gradually increased from early to late fear conditioning, while long-latency (460–730 ms) electrocortical responses diminished throughout fear extinction. Our novel paradigm demonstrates how short-, mid-, and long-latency EEG responses change during fear conditioning and extinction, findings that enlighten the learning curve of neurophysiological responses to threat in humans.

ID 205

Authors

Matthias F. J. Sperl, Department of Psychology, Personality Psychology and Assessment, University of Marburg, 35032 Marburg, Germany; Department of Psychology, Clinical Psychology and Psychotherapy, University of Giessen, 35394 Giessen, Germany Adrian Wroblewski, Department of Psychiatry and Psychotherapy, Translational Neuroimaging Marburg, University of Marburg, 35039 Marburg, Germany Madeleine Mueller, Department of Psychiatry and Psychotherapy, Translational Neuroimaging Marburg, University of Marburg, 35039 Marburg, Germany; Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany Benjamin Straube, Department of Psychiatry and Psychotherapy, Translational Neuroimaging Marburg, University of Marburg, 35039 Marburg, Germany Erik M. Mueller, Department of Psychology, Personality Psychology and Assessment, University of Marburg, 35032 Marburg, Germany

Year

2020

DOI of Publication

10.1016/j.neuroimage.2020.117569

Persistent Identifier to Dataset

10.5281/zenodo.4308063

Where was the data collected?

University of Marburg, Germany

How to Cite

Sperl, M. F. J., Wroblewski, A., Mueller, M., Straube, B., & Mueller, E. M. (2020). Learning Dynamics of Electrophysiological Brain Signals During Human Fear Conditioning (Open Data and Open Materials) [Data set]. In NeuroImage (1.0.0, Bd. 226, S. 117569). Zenodo. https://doi.org/10.5281/zenodo.4308063

Participant Information

Participant Age

Participant Sex

Experimental Group

Within-Subject Design: Participants underwent three successive acquisition training phases (ACQ1, ACQ2, and ACQ3), each with a novel conditioned stimulus (CS+/CS-) set (differently tinted neutral faces)

Stimuli

Drug Administration

No

Conditioning Protocol

Differential

Instructions CS-US Contingencies

Fully instructed (whole exp)

Number of Different US

1

US Modality

electrotactile

Number of Different CS+

3

CS+ 1: Reinforcement Rate (%)

46.67

CS+ 2: Reinforcement Rate (%)

46.67

CS+ 3: Reinforcement Rate (%)

46.67

Number of Different CS-

3

CS Modality

visual

Data Collected During MRI

No

Physiological Measures

measured trialwise & untransformed

Skin Conductance Response

Yes No

Skin Conductance Level

No No

Pupil Size

No No

Fear Potentiated Startle/Startle EMG

No No

Heart Rate

No No

Ratings

US Expectancy

Yes

US Intensity Rating

No

CS Valence

Yes

CS Arousal

Yes

CS Fear

No

CS Stress

No

CS Anxiety

No

Contingency Awareness

No

Questionnaires