Vol.:(0123456789) 1 3
Animal Cognition
https://doi.org/10.1007/s10071-020-01415-x
ORIGINAL PAPER
Taste association capabilities difer in high‑ and low‑yawning
rats versus outbred Sprague–Dawley rats after prolonged sugar
consumption
María‑Isabel Miranda
1
· Alejandro Rangel‑Hernández
1
· Gabriela Vera‑Rivera
1
· Carmen Cortes
2
· Jose R. Eguibar
2,3
Received: 28 October 2019 / Revised: 3 June 2020 / Accepted: 10 July 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract
Yawning is a stereotypical behavior pattern commonly associated with other behaviors such as grooming, sleepiness, and
arousal. Several diferences in behavioral and neurochemical characteristics have been described in high-yawning (HY) and
low-yawning (LY) sublines from Sprague–Dawley (SD) rats that support they had changes in the neural mechanism between
sublines. Diferences in behavior and neurochemistry observed in yawning sublines could also overlap in processes needed
during taste learning, particularly during conditioned taste aversion (CTA) and its latent inhibition. Therefore, the aim of
this study was to analyze taste memory diferences, after familiarization to novel or highly sweet stimuli, between yawning
sublines and compare them with outbred SD rats. First, we evaluated changes in appetitive response during long-term sugar
consumption for 14 days. Then, we evaluated the latent inhibition of CTA strength induced by this long pre-exposure, and we
also measured aversive memory extinction rate. The results showed that SD rats and the two sublines developed similar CTA
for novel sugar and signifcantly stronger appetitive memory after long-term sugar exposure. However, after 14 days of sugar
exposure, HY and LY sublines were unable to develop latent inhibition of CTA after two acquisition trials and had a slower
aversive memory extinction rate than outbreed rats. Thus, the inability of the HY and LY sublines to develop latent inhibi-
tion of CTA after long-term sugar exposure could be related to the time/context processes involved in long-term appetitive
re-learning, and in the strong inbreeding that characterizes the behavioral traits of these sublines, suggesting that inbreeding
afects associative learning, particularly after long-term exposure to sweet stimuli which refects high familiarization.
Keywords Novelty · Appetitive memory · Sugar preference · Latent inhibition · Extinction · Sucrose · Aversive
conditioning
Introduction
Yawning is an innate behavioral pattern with very low
frequency in all species, including rats (Baenninger 1987),
and it is commonly associated with other behaviors such
as grooming, penile erection, sleepiness, and arousal (Hol-
mgren et al. 1985; Eguibar and Moyaho 1997; Portillo
et al. 2010; Krestel et al. 2018). In outbred Sprague–Daw-
ley (SD) rats, spontaneous yawning behavior is around 1
yawn/h, but we selectively bred 2 sublines, over 88 genera-
tions, that difer in their spontaneous yawning frequency,
the high-yawning (HY) subline with 20 yawns/h, and the
low-yawning (LY) subline with less than 1 yawn/h (Urba-
Holmgren et al. 1990; Eguibar et al. 2002). Using the HY
subline, we clearly demonstrated that yawning behavior
has a circadian oscillation with a clear peak before dusk
(Anias et al. 1984), and restricted feeding schedule is a
stronger zeitgeber (Holmgren et al. 1991). Furthermore,
several diferences in behavioral characteristics have been
described between sublines. For example, HY male rats
had more grooming bouts after exposure to a novel envi-
ronment or after wetting their fur with respect to LY rats
* María-Isabel Miranda
mirandami@unam.mx
1
Departamento de Neurobiología Conductual y Cognitiva,
Instituto de Neurobiología, Universidad Nacional Autónoma
de México, Campus Juriquilla, Boulevard Juriquilla No.
3001, A.P. 1-1141, Juriquilla, Querétaro 76230, Mexico
2
Instituto de Fisiología, Benemérita Universidad Autónoma de
Puebla, Puebla, Mexico
3
Dirección General de Investigación, Vicerrectoría de
Investigación y Estudios de Posgrado, Benemérita
Universidad Autónoma de Puebla, Puebla, Mexico