Skip to main content
SpringerLink
Log in

Taste association capabilities differ in high- and low-yawning rats versus outbred Sprague–Dawley rats after prolonged sugar consumption

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Yawning is a stereotypical behavior pattern commonly associated with other behaviors such as grooming, sleepiness, and arousal. Several differences 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. Differences 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 differences, 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 significantly 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 inhibition 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 affects associative learning, particularly after long-term exposure to sweet stimuli which reflects high familiarization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anias J, Holmgren B, Urba Holmgren R, Eguibar JR (1984) Circadian variation of yawning behavior. Acta Neurobiol Exp (Wars) 44(4):179–186

    CAS  Google Scholar 

  • Baenninger R (1987) Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J Comp Psychol 101(4):349

    Google Scholar 

  • Bello NT, Walters AL, Verpeut JL, Caverly J (2014) Dietary-induced binge eating increases prefrontal cortex neural activation to restraint stress and increases binge food consumption following chronic guanfacine. Pharmacol Biochem Behav 125:21–28

    CAS  PubMed  Google Scholar 

  • Berman DE, Hazvi S, Neduva V, Dudai Y (2000) The role of identified neurotransmitter systems in the response of insular cortex to unfamiliar taste: activation of ERK1-2 and formation of a memory trace. J Neurosci 20(18):7017–7023

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bures J, Bermúdez-Rattoni F, Yamamoto T (1998) Conditioned taste aversion: memory of a special kind. Oxford University Press, Oxford

    Google Scholar 

  • Caynas-Rojas S, Rodríguez-García G, Delint-Ramírez I, Miranda MI (2018) Differential function of medial prefrontal cortex catecholaminergic receptors after long-term sugar consumption. Behav Brain Res 356:495–503

    PubMed  Google Scholar 

  • Colantuoni C, Schwenker J, McCarthy J, Rada P, Ladenheim B, Cadet J-L, Schwartz G, Moran T, Hoebel B (2001) Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain. NeuroReport 12(16):3549–3552

    CAS  PubMed  Google Scholar 

  • Colantuoni C, Rada P, McCarthy J, Patten C, Avena NM, Chadeayne A, Hoebel BG (2002) Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res 10(6):478–488

    CAS  PubMed  Google Scholar 

  • Cole KC, Bakner L, Vernon A, Riccio DC (1993) The effect of US preexposure on conditioned taste aversion: lack of postconditioning recovery of the aversion. Behav Neural Biol 60(3):271–273

    CAS  PubMed  Google Scholar 

  • Collins GT, Eguibar JR (2010) Neurophamacology of yawning. Front Neurol Neurosci 28:90–106

    PubMed  Google Scholar 

  • De la Casa G, Lubow RE (1995) Latent inhibition in conditioned taste aversion: the roles of stimulus frequency and duration and the amount of fluid ingested during preexposure. Neurobiol Learn Mem 64(2):125–132

    PubMed  Google Scholar 

  • De la Casa LG, Lubow RE (2001) Latent inhibition with a response time measure from a within-subject design: effects of number of preexposures, masking task, context change, and delay. Neuropsychology 15(2):244–253

    PubMed  Google Scholar 

  • De la Casa L, Lubow R (2005) Delay-induced super-latent inhibition as a function of order of exposure to two flavours prior to compound conditioning. Quart J Exp Psychol Sect B 58(1):1–18

    Google Scholar 

  • Doger E, Urba-Holmgren R, Eguibar JR, Holmgren B (1989) GABAergic modulation of yawning behavior. Pharmacol Biochem Behav 34(2):237–240

    CAS  PubMed  Google Scholar 

  • Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009) Effects of pretest manipulation on elevated plus-maze behavior in adolescent and adult male and female Sprague-Dawley rats. Pharmacol Biochem Behav 92(3):413–423

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eguibar JR, Moyaho A, Carbente JCR (2002). Influencias Medio Ambientales y Farmacológicas Sobre el Bostezo y el Aseo en Dos Sublíneas de Ratas con Una Frecuencia de Bostezo Espontáneo Diferente

  • Eguibar JR, Moyaho A (1997) Inhibition of grooming by pilocarpine differs in high- and low-yawning sublines of Sprague-Dawley rats. Pharmacol Biochem Behav 58(2):317–322

    CAS  PubMed  Google Scholar 

  • Eguibar JR, Romero-Carbente JC, Moyaho A (2003) Behavioral differences between selectively bred rats: D1 versus D2 receptors in yawning and grooming. Pharmacol Biochem Behav 74(4):827–832

    CAS  PubMed  Google Scholar 

  • Escobar M, Arcediano F, Miller RR (2002) Latent inhibition and contextual associations. J Exp Psychol Anim Behav Process 28(2):123–136

    PubMed  Google Scholar 

  • Frank GK, Shott ME, Hagman JO, Mittal VA (2013) Alterations in brain structures related to taste reward circuitry in ill and recovered anorexia nervosa and in bulimia nervosa. Am J Psychiatry 170(10):1152–1160

    PubMed  PubMed Central  Google Scholar 

  • Hajnal A, Norgren R (2001) Accumbens dopamine mechanisms in sucrose intake. Brain Res 904(1):76–84

    CAS  PubMed  Google Scholar 

  • Holmgren B, Urba-Holmgren R, Trucios N, Zermeno M, Eguibar JR (1985) Association of spontaneous and dopaminergic-induced yawning and penile erections in the rat. Pharmacol Biochem Behav 22(1):31–35

    CAS  PubMed  Google Scholar 

  • Holmgren B, Budelli R, Urba-Holmgren R, Eguibar JR, Holmgren M, Baz-Tellez G, Anias J (1991) Food anticipatory yawning rhythm in the rat. Acta Neurobiol Exp (Wars) 51(3–4):97–105

    CAS  Google Scholar 

  • Izidio GS, Spricigo L Jr, Ramos A (2005) Genetic differences in the elevated plus-maze persist after first exposure of inbred rats to the test apparatus. Behav Processes 68(2):129–134

    CAS  PubMed  Google Scholar 

  • Killcross S (2001) Loss of latent inhibition in conditioned taste aversion following exposure to a novel flavour before test. Q J Exp Psychol B 54(3):271–288

    CAS  PubMed  Google Scholar 

  • Killcross AS, Kiernan MJ, Dwyer D, Westbrook RF (1998) Loss of latent inhibition of contextual conditioning following non-reinforced context exposure in rats. Q J Exp Psychol B 51(1):75–90

    CAS  PubMed  Google Scholar 

  • Krestel H, Weisstanner C, Hess CW, Bassetti CL, Nirkko A, Wiest R (2015) Insular and caudate lesions release abnormal yawning in stroke patients. Brain Struct Funct 220(2):803–812

    PubMed  Google Scholar 

  • Krestel H, Bassetti CL, Walusinski O (2018) Yawning-its anatomy, chemistry, role, and pathological considerations. Prog Neurobiol 161:61–78

    CAS  PubMed  Google Scholar 

  • Kwok DW, Boakes RA (2019) Situational relevance: context as a factor in serial overshadowing of taste aversion learning. Q J Exp Psychol (Hove) 72(2):263–273

    Google Scholar 

  • Lubow RE (1965) Latent inhibition: effects of frequency of nonreinforced pre-exposure of the CS. J Comp Physiol Psychol 60(3):454

    CAS  PubMed  Google Scholar 

  • Lubow RE (1973) Latent inhibition. Psychol Bull 79(6):398–407

    CAS  PubMed  Google Scholar 

  • Lubow R, De la Casa L (2005) Time-induced super-latent inhibition is dependent on the distinctiveness of the retention-interval context from the other experimental contexts. Learn Motiv 36(3):322–330

    Google Scholar 

  • Lubow RE, Moore AU (1959) Latent inhibition: the effect of nonreinforced pre-exposure to the conditional stimulus. J Comp Physiol Psychol 52:415–419

    CAS  PubMed  Google Scholar 

  • Lubow RM, Kretzchmar SL, Brown FH (1989) Use of apical sliding flaps in connection with overdenture abutment teeth. Quintessenz 40(5):881–887

    CAS  PubMed  Google Scholar 

  • Manrique T, Molero A, Ballesteros MA, Moron I, Gallo M, Fenton AA (2004) Time of day-dependent latent inhibition of conditioned taste aversions in rats. Neurobiol Learn Mem 82(2):77–80

    PubMed  Google Scholar 

  • Mark GP, Blander DS, Hoebel BG (1991) A conditioned stimulus decreases extracellular dopamine in the nucleus accumbens after the development of a learned taste aversion. Brain Res 551(1–2):308–310

    CAS  PubMed  Google Scholar 

  • Miranda MI, Bermudez-Rattoni F (1999) Reversible inactivation of the nucleus basalis magnocellularis induces disruption of cortical acetylcholine release and acquisition, but not retrieval, of aversive memories. Proc Natl Acad Sci USA 96(11):6478–6482

    CAS  PubMed  Google Scholar 

  • Miranda MI, Ferreira G, Ramirez-Lugo L, Bermudez-Rattoni F (2002) Glutamatergic activity in the amygdala signals visceral input during taste memory formation. Proc Natl Acad Sci USA 99(17):11417–11422

    CAS  PubMed  Google Scholar 

  • Molero A, Moron I, Angeles Ballesteros M, Manrique T, Fenton A, Gallo M (2005) Hippocampus, temporal context and taste memories. Chem Senses 30(Suppl 1):i160–i161

    PubMed  Google Scholar 

  • Molero-Chamizo A (2017) Circadian-temporal context and latent inhibition of conditioned taste aversion: effect of restriction in the intake of the conditioned taste stimulus. Learn Behav 45(2):157–163

    PubMed  Google Scholar 

  • Molero-Chamizo A, Rivera-Urbina GN (2017) Effects of temporal contexts and contextual habituation on latent inhibition. Psicothema 29(3):346–351

    PubMed  Google Scholar 

  • Molero-Chamizo A (2018a) Changes in the time of day of conditioning with respect to the pre-exposure interfere with the latent inhibition of conditioned taste aversion in rats. Behav Proc 146:22–26

    Google Scholar 

  • Molero-Chamizo A (2018b) Changes in the time of day of conditioning with respect to the pre-exposure interfere with the latent inhibition of conditioned taste aversion in rats. Behav Processes 146:22–26

    PubMed  Google Scholar 

  • Moyaho A, Valencia J (2002) Grooming and yawning trace adjustment to unfamiliar environments in laboratory Sprague-Dawley rats (Rattus norvegicus). J Comp Psychol 116(3):263–269

    PubMed  Google Scholar 

  • Moyaho A, Eguibar J, Diaz J (1995) Induced grooming transitions and open field behaviour differ in high-and low-yawning sublines of Sprague-Dawley rats. Anim Behav 50(1):61–72

    Google Scholar 

  • Nelson AJ, Thur KE, Horsley RR, Spicer C, Marsden CA, Cassaday HJ (2011) Reduced dopamine function within the medial shell of the nucleus accumbens enhances latent inhibition. Pharmacol Biochem Behav 98(1):1–7

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nunez-Jaramillo L, Ramirez-Lugo L, Herrera-Morales W, Miranda MI (2010) Taste memory formation: latest advances and challenges. Behav Brain Res 207(2):232–248

    PubMed  Google Scholar 

  • Oliveira Ldos S, da Silva LP, da Silva AI, Magalhaes CP, de Souza SL, de Castro RM (2011) Effects of early weaning on the circadian rhythm and behavioral satiety sequence in rats. Behav Processes 86(1):119–124

    PubMed  Google Scholar 

  • Portillo W, Camacho F, Eguibar JR, Paredes RG (2010) Behavioral characterization of non-copulating male rats with high spontaneous yawning frequency rate. Behav Brain Res 214(2):225–230

    PubMed  Google Scholar 

  • Pritchett CE, Hajnal A (2011) Obesogenic diets may differentially alter dopamine control of sucrose and fructose intake in rats. Physiol Behav 104(1):111–116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puron-Sierra L, Sabath E, Nunez-Jaramillo L, Miranda MI (2010) Blockade of nucleus basalis magnocellularis or activation of insular cortex histamine receptors disrupts formation but not retrieval of aversive taste memory. Neurobiol Learn Mem 93(2):216–220

    PubMed  Google Scholar 

  • Rada P, Barson JR, Leibowitz SF, Hoebel BG (2010) Opioids in the hypothalamus control dopamine and acetylcholine levels in the nucleus accumbens. Brain Res 1312:1–9

    CAS  PubMed  Google Scholar 

  • Rodriguez-Garcia G, Miranda MI (2016) Opposing roles of cholinergic and gabaergic activity in the insular cortex and nucleus basalis magnocellularis during novel recognition and familiar taste memory retrieval. J Neurosci 36(6):1879–1889

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roman C, Lin J-Y, Reilly S (2009) Conditioned taste aversion and latent inhibition following extensive taste preexposure in rats with insular cortex lesions. Brain Res 1259:68–73

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stryjek R, Modlińska K, Turlejski K, Pisula W (2013) Circadian rhythm of outside-nest activity in wild (WWCPS), albino and pigmented laboratory rats. PLoS ONE 8(6):e66055

    CAS  PubMed  PubMed Central  Google Scholar 

  • Swithers SE, Baker CR, Davidson TL (2009) General and persistent effects of high-intensity sweeteners on body weight gain and caloric compensation in rats. Behav Neurosci 123(4):772–780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tuerke KJ, Limebeer CL, Fletcher PJ, Parker LA (2012) Double dissociation between regulation of conditioned disgust and taste avoidance by serotonin availability at the 5-HT(3) receptor in the posterior and anterior insular cortex. J Neurosci 32(40):13709–13717

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tulloch AJ, Murray S, Vaicekonyte R, Avena NM (2015) Neural responses to macronutrients: hedonic and homeostatic mechanisms. Gastroenterology 148(6):1205–1218

    CAS  PubMed  Google Scholar 

  • Ugarte A, Eguibar JR, Cortes Mdel C, Leon-Chavez BA, Melo AI (2011) Comparative analysis of maternal care in the high-yawning (HY) and low-yawning (LY) sublines from Sprague-Dawley rats. Dev Psychobiol 53(2):105–117

    PubMed  Google Scholar 

  • Urba-Holmgren R, Trucios N, Holmgren B, Eguibar JR, Gavito A, Cruz G, Santos A (1990) Genotypic dependency of spontaneous yawning frequency in the rat. Behav Brain Res 40(1):29–35

    CAS  PubMed  Google Scholar 

  • Urba-Holmgren R, Santos A, Holmgren B, Eguibar JR (1993) Two inbred rat sublines that differ in spontaneous yawning behavior also differ in their responses to cholinergic and dopaminergic drugs. Behav Brain Res 56(2):155–159

    CAS  PubMed  Google Scholar 

  • Vera-Rivera G, Miranda MI, Rangel-Hernandez JA, Badillo-Juarez D, Fregoso-Urrutia D, Caynas-Rojas S (2018) Effects of caloric or non-caloric sweetener long-term consumption on taste preferences and new aversive learning. Nutr Neurosci 4:1–11

    Google Scholar 

Download references

Acknowledgments

In memoriam of Shaun Harris. We thank Dr. Michael Jeziorski, and Jessica Gonzalez-Norris for editing the English version of this manuscript. We also thank Leonor Casanova, Alejandra Castilla, José Martín García and Lourdes Ayala for their technical assistance.

Funding

PAPIIT IN201018 and CONACyT 252379 to MIM. CONACYT 243247 and 243333 to JRE and MCC, respectively, and by BUAP-VIEP to Cuerpo Académico en Neuroendocrinología-BUAP-CA-288.

Author information

Authors and Affiliations

  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

    María-Isabel Miranda, Alejandro Rangel-Hernández & Gabriela Vera-Rivera

  2. Instituto de Fisiología, Benemérita Universidad Autónoma de Puebla, Puebla, Mexico

    Carmen Cortes & Jose R. Eguibar

  3. Dirección General de Investigación, Vicerrectoría de Investigación y Estudios de Posgrado, Benemérita Universidad Autónoma de Puebla, Puebla, Mexico

    Jose R. Eguibar

Authors
  1. María-Isabel Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alejandro Rangel-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriela Vera-Rivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carmen Cortes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jose R. Eguibar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María-Isabel Miranda.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miranda, MI., Rangel-Hernández, A., Vera-Rivera, G. et al. Taste association capabilities differ in high- and low-yawning rats versus outbred Sprague–Dawley rats after prolonged sugar consumption. Anim Cogn 24, 41–52 (2021). https://doi.org/10.1007/s10071-020-01415-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-020-01415-x

Keywords

Search

Navigation