Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output

Faced with potential harm, individuals must estimate the probability of threat and initiate an appropriate fear response. In the prevailing view, threat probability estimates are relayed to the ventrolateral periaqueductal gray (vlPAG) to organize fear output. A straightforward prediction is that vl...

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Main Authors: Kristina M Wright, Michael A McDannald
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/45013
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author Kristina M Wright
Michael A McDannald
author_facet Kristina M Wright
Michael A McDannald
author_sort Kristina M Wright
collection DOAJ
description Faced with potential harm, individuals must estimate the probability of threat and initiate an appropriate fear response. In the prevailing view, threat probability estimates are relayed to the ventrolateral periaqueductal gray (vlPAG) to organize fear output. A straightforward prediction is that vlPAG single-unit activity reflects fear output, invariant of threat probability. We recorded vlPAG single-unit activity in male, Long Evans rats undergoing fear discrimination. Three 10 s auditory cues predicted unique foot shock probabilities: danger (p=1.00), uncertainty (p=0.375) and safety (p=0.00). Fear output was measured by suppression of reward seeking over the entire cue and in one-second cue intervals. Cued fear non-linearly scaled to threat probability and cue-responsive vlPAG single-units scaled their firing on one of two timescales: at onset or ramping toward shock delivery. VlPAG onset activity reflected threat probability, invariant of fear output, while ramping activity reflected both signals with threat probability prioritized.
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spelling doaj.art-5c791c96c609470faa4b159a1f97392f2022-12-22T02:03:14ZengeLife Sciences Publications LtdeLife2050-084X2019-03-01810.7554/eLife.45013Ventrolateral periaqueductal gray neurons prioritize threat probability over fear outputKristina M Wright0https://orcid.org/0000-0003-1446-3009Michael A McDannald1https://orcid.org/0000-0001-8525-1260Psychology Department, Boston College, Chestnut Hill, United StatesPsychology Department, Boston College, Chestnut Hill, United StatesFaced with potential harm, individuals must estimate the probability of threat and initiate an appropriate fear response. In the prevailing view, threat probability estimates are relayed to the ventrolateral periaqueductal gray (vlPAG) to organize fear output. A straightforward prediction is that vlPAG single-unit activity reflects fear output, invariant of threat probability. We recorded vlPAG single-unit activity in male, Long Evans rats undergoing fear discrimination. Three 10 s auditory cues predicted unique foot shock probabilities: danger (p=1.00), uncertainty (p=0.375) and safety (p=0.00). Fear output was measured by suppression of reward seeking over the entire cue and in one-second cue intervals. Cued fear non-linearly scaled to threat probability and cue-responsive vlPAG single-units scaled their firing on one of two timescales: at onset or ramping toward shock delivery. VlPAG onset activity reflected threat probability, invariant of fear output, while ramping activity reflected both signals with threat probability prioritized.https://elifesciences.org/articles/45013single-unitthreatfearconditioned suppressionmidbrainassociative learning
spellingShingle Kristina M Wright
Michael A McDannald
Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output
eLife
single-unit
threat
fear
conditioned suppression
midbrain
associative learning
title Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output
title_full Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output
title_fullStr Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output
title_full_unstemmed Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output
title_short Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output
title_sort ventrolateral periaqueductal gray neurons prioritize threat probability over fear output
topic single-unit
threat
fear
conditioned suppression
midbrain
associative learning
url https://elifesciences.org/articles/45013
work_keys_str_mv AT kristinamwright ventrolateralperiaqueductalgrayneuronsprioritizethreatprobabilityoverfearoutput
AT michaelamcdannald ventrolateralperiaqueductalgrayneuronsprioritizethreatprobabilityoverfearoutput