https://doi.org/10.1177/0269881119862527
Journal of Psychopharmacology
1–9
©
The Author(s) 2019
Article reuse guidelines:
sagepub.com/journals-permissions
DOI: 10.1177/0269881119862527
journals.sagepub.com/home/jop
Introduction
Dopaminergic neurotransmission has been implicated in the pro-
cessing of conditioned and unconditioned aversive stimulation.
For instance, a cue for fear decreased dopamine (DA) transmis-
sion in the nucleus accumbens (NAc) core, but increased it in the
NAc shell (Badrinarayan et al., 2012). Similarly, extracellular
DA was decreased in the NAc core but not shell by the withhold-
ing of anticipated reward (Biesdorf et al., 2015). Changes in NAc
DA release occurred upon presentation of predictors of aversion
(Wenzel et al., 2015), and predicted the extent of avoidance
behavior (Pultorak et al., 2018). Pharmacological studies have
also implicated DA in the various fear/anxiety-related behaviors,
including conditioned and unconditioned fear-related responses
(Brandão et al., 2015; Brandão and Coimbra, 2019; Garcia et al.,
2005; Reis et al., 2004).
DA has also been demonstrated to attenuate responses to aver-
sive stimulation. Recently, we found in rats that intranasally
applied DA (IN-DA) attenuated unconditioned fear responses,
considering that it reduced escape behavior from bright light and
ultrasound vocalizations in response to aversive restraint (Talbot
et al., 2017). The present study follows up on this finding by
examining the effects of acute IN-DA on (a) freezing induced by
electric shock to the foot (as a measure of conditioned fear) one,
two, and eight days after the conditioning session, and (b)
freezing, escape, and post-stimulation freezing (unconditioned
Intranasal dopamine attenuates fear responses
induced by electric shock to the foot and
by electrical stimulation of the dorsal
periaqueductal gray matter
Milene Cristina de Carvalho
1,2,3
, Rebeca Machado de Figueiredo
1,2
,
Norberto Cysne Coimbra
1,2,3
, Christie Ramos Andrade Leite-Panissi
1,3,4
,
Maria Angélica de Souza Silva
5
, Joseph P Huston
5
, Claudia Mattern
6,7
and Marcus Lira Brandão
1,3
Abstract
Purpose: Intranasally applied dopamine (IN-DA), which likely reaches the brain via nasal–brain pathways and bypasses the blood–brain barrier, has
been found to increase extracellular DA and bind to the DA2 transporter in the striatum. Recent studies suggest that DA plays a significant role in the
processing of signaled and unconditioned aversive stimulation, including evidence that may attenuate responses to painful input. The purpose of this
study was to examine the effects of IN-DA on fear-related behaviors induced by electric shock to the foot or by electrical stimulation of the dorsal
periaqueductal gray matter (dPAG).
Methods: DA hydrochloride suspended in a viscous castor oil gel (1 or 2 mg/kg) was applied (IN-DA) in a volume of 5 μL into the nostrils of adult
Wistar male rats in order to evaluate its effects on (a) freezing induced by electric shock to the foot and (b) thresholds of freezing and escape and
duration of post-stimulation freezing induced by electrical stimulation of the dPAG.
Results: IN-DA attenuated freezing induced by electric shock to the foot in the three test trials, indicating that it reduced long-term fear responses.
IN-DA also increased the threshold of dPAG stimulation-induced escape responses and reduced post-stimulation freezing.
Conclusions: IN-DA, which has previously been shown to facilitate learning and to have antidepressive-like effects, attenuated unconditioned fear
responses elicited by peripheral and intramesencephalic (dPAG) stimulation and reduced long-term conditioned fear responses.
Keywords
Unconditioned fear, conditioned fear, fear extinction, dopamine, dPAG, nasal drug application
1
Instituto de Neurociências e Comportamento (INeC), Ribeirão Preto, Brazil
2
Laboratory of Neuroanatomy and Neuropsychobiology, Department of
Pharmacology, Ribeirão Preto Medical School of the University of São
Paulo, Ribeirão Preto, Brazil
3
NAP-USP-Neurobiology of Emotions Research Centre (NuPNE), Ribeirão
Preto School of Medicine of the University of São Paulo (FMRP-USP),
Ribeirão Preto, Brazil
4
Department of Psychology, Ribeirão Preto School of Philosophy,
Science and Literature of the University of São Paulo, Ribeirão Preto,
Brazil
5
Center for Behavioral Neuroscience, Institute of Experimental
Psychology, University of Düsseldorf, Düsseldorf, Germany
6
M et P Pharma AG, Emmetten, Switzerland
7
Oceanographic Center, Nova Southeastern University, Fort Lauderdale,
FL, USA
Corresponding author:
Milene Cristina de Carvalho, Instituto de Neurociências e
Comportamento-INeC, Av. do Café, Ribeirão Preto, 2450, Brazil.
Email: mccarva@usp.br
862527JOP 0 0 10.1177/0269881119862527Journal of PsychopharmacologyCarvalho et al.
research-article 2019
Original Paper