Cited by 109Memory and Neural MechanismsAnimal Vocal Communication and BehaviorNeuroscience and Music Perception

Positive and negative ultrasonic social signals elicit opposing firing patterns in rat amygdala

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Parsana, Ashwini J., Li, Nanxin, Brown, Thomas H.·2012·Behavioural Brain Research

Abstract

Rat ultrasonic vocalizations (USVs) are ethologically-essential social signals. Under natural conditions, 22kHz USVs and 50kHz USVs are emitted in association with negative and positive emotional states, respectively. Our first experiment examined freezing behavior elicited in naïve Sprague-Dawley rats by a 22kHz USV, a 50kHz USV, and frequency-matched tones. None of the stimuli elicited freezing, which is the most commonly-used index of fear. The second experiment examined single-unit responses to these stimuli in the amygdala (AM), which is well-known for its role in innate and acquired fear responses. Among 127 well-discriminated single units, 82% were auditory-responsive. Elicited firing patterns were classified using a multi-dimensional scheme that included transient (phasic) responses to the stimulus onsets and/or offsets as well as sustained (tonic) responses during the stimulus. Tonic responses, which are not ordinarily evaluated in AM, were 4.4-times more common than phasic responses. The 22kHz stimuli tended to elicit tonic increases in the firing rates, whereas the 50kHz stimuli more often elicited tonic decreases in firing rates. These opposing tonic responses correspond with the ethological valence of USVs in the two frequency bands. Thus, a relatively-small sample of single-unit responses in AM furnished a more sensitive index of emotional valence than freezing behavior. Latency analysis suggested that stimuli in the two frequency bands are processed through different pathways to AM. One possible interpretation is that phasic responses in AM reflect the detection of a stimulus change, whereas tonic responses indicate the valence of the detected stimulus.

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  1. [30]Sales GD The effect of 22kHz calls and artificial 38kHz signals on activity in rats Behav Processes 1991 24 83 93 24923696
  2. [67]Morris JS Friston KJ Buchel C Frith CD Young AW Calder AJ Dolan RJ A neuromodulatory role for the human amygdala in processing emotional facial expressions Brain 1998 121 47 57 9549487
  3. [73]Shi CJ Cassell MD Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat J Comp Neurol 1999 406 299 328 10102498

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Authors
Parsana, A. J., Li, N., & Brown, T. H.
Affiliations
Yale University (US)
Corresponding author
Brown, Thomas H.
Venue
Behavioural Brain Research
Publisher
Elsevier BV
Published
2012-01
Volume
226
Issue
1
Pages
77-86
ISSN
0166-4328 (ISSN-L)
OpenAlex
W2150062107
Cited by
108
References
78
Citations by year
2026: 2 · 2025: 4 · 2024: 5 · 2023: 9 · 2022: 7 · 2021: 8 · 2020: 8 · 2019: 4 · 2018: 10 · 2017: 8 · 2016: 12 · 2015: 7 · 2014: 6 · 2013: 10 · 2012: 8
FWCI
3.90
Type
journal article
Language
en
Open access
Locations
  • Behavioural Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Mental Health (R01MH058405)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
Keywords
ultrasonic vocalizations, social signals, amygdala, single-unit responses, emotional valence, freezing behavior, fear, auditory processing, rats
MeSH terms
Acoustic Stimulation, Amygdala, Animals, Behavior, Animal, Fear, Male, Neurons, Social Behavior, Vocalization, Animal, Rats, Sprague-Dawley, Freezing Reaction, Cataleptic, Rats

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