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- Springer Journals
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- Copyright © The Author(s) 2023
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- 1744-9081
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- 10.1186/s12993-023-00206-x
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Abstract
Background Novel flavors elicit a cautious neophobic response which is attenuated as the flavor becomes familiar and safe. The attenuation of neophobia reveals the formation of a safe memory. Previous lesion studies in rats have reported that basolateral amygdala integrity is required for taste neophobia, but not neophobia to flavor, i.e., taste linked to an odorous component. Accordingly, immunohistochemical analyses show that novel tastes induced higher basolateral amygdala activity when compared to familiar ones. However, a different role of basolateral amygdala in flavor attenuation of neophobia is suggested by lesion studies using a vinegar solution. Studies assessing basolateral amygdala activity during flavor attenuation of neophobia are lacking. Thus, we quantified cytochrome oxidase as an index of basolateral amygdala activity along the first and second vinegar exposures in order to assess flavor neopho ‑ bia and attenuation of neophobia. Methods We exposed adult male Wistar rats either once or twice to a 3% cider vinegar solution or water, and com‑ pared the basolateral amygdala, piriform cortex and caudate putamen brain metabolic activity using cytochrome c‑ oxidase histochemistry. Results We found increased flavor intake and cytochrome c‑ oxidase histochemistry activity during the second expo‑ sure in basolateral amygdala, but not in the piriform cortex and caudate/putamen. Conclusions The main finding of the study is that BLA metabolic activity was higher in the group exposed to a famil‑ iar vinegar solution than in the groups exposed to either water or a novel vinegar solution. Keywords Amygdala, Attenuation of neophobia, Cytochrome c oxidase, Flavor, Neophobia, Taste † 5 S. Menchén‑Márquez and M. Banqueri contributed equally to this work and Instituto de Neurociencias del Principado de Asturias (INEUROPA), they should both be considered as first authors University of Oviedo, Oviedo, Spain Department of Didactics, Area of Didactics of Experimental Sciences, *Correspondence: Faculty of Education Sciences, University of Cádiz, Cádiz, Spain Sergio Menchén‑Márquez smenchen@ugr.es Department of Psychobiology, Institute of Neurosciences, Center for Biomedical Research (CIBM), University of Granada, Parque Tecnológico de la Salud (PTS), Avda del Conocimiento, s/n, Armilla, 18016 Granada, Spain Instituto de Investigación Biosanitaria (IBS), Granada, Spain Laboratory of Neuroscience, Department of Psychology, University of Oviedo, Oviedo, Spain Centre for Discovery Brain Sciences, Edinburgh University, Edinburgh, UK © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Menchén‑Márquez et al. Behavioral and Brain Functions (2023) 19:2 Page 2 of 6 potential BLA involvement either in the detection of Introduction flavor novelty or flavor familiarization. Increases of the The ability to recognize familiar flavors which have been BLA metabolic activity during the first flavor exposure safe in previous encounters is critical for diet selec- would support a role in novelty detection. This would tion and survival. A novel flavor induces a neophobic be consistent with the results found using a purely response that is attenuated in a second exposure to the taste solution. On the other hand, increases of the BLA flavor without negative consequences, thus leading to metabolic activity during the second flavor exposure increased consumption. The attenuation of neophobia would point to a role in flavor familiarization. This (AN) requires the integrity of the perirhinal cortex (Prh), would be in accordance with the reported AN disrup- a brain area involved in taste and object recognition tion by BLA lesions. Given the odorous component memory. Accordingly, Prh excitotoxic [1] and lidocaine- of the flavor used, the metabolic activity of the olfac - reversible lesions [2] interfere with the increased con- tory piriform cortex (Pir) as well as caudate/putamen sumption during the second presentation of vinegar and (Cpu) as additional control areas was assessed. No sex saccharin solutions, respectively. We have also previously differences have been reported either in vinegar neo - reported a similar impairment induced by basolateral phobia or AN using the present behavioral procedure amygdala (BLA) excitotoxic lesions. These lesions disrupt [17]. Hence, male rats were used for allowing compari- the pattern of Prh activity associated with AN during the son with previous results on brain activity, thus reduc- second exposure to the vinegar solution [3]. Nonetheless, ing the number of animals used. Additionally, the use the critical mechanism disrupted is not yet known. of males avoids mildly invasive procedures required for There is evidence supporting the BLA involvement assessing the estrus cycle. in taste novelty detection. In fact, BLA permanent and reversible lesions have been found to interfere with neo- phobia to a 0.5% sodium saccharin solution [4, 5] and c-Fos expression induced in BLA by a novel saccharin Material and methods solution is higher than that induced by a familiar one [6]. Behavioral procedure However, Lin and colleagues [4] did not find effects of Twenty-one naive adult male Wistar rats were individu- BLA lesions on odor neophobia using a 0.1% amyl ace- ally housed and maintained in a 12-h-light-dark cycle tate solution. This is a relevant issue, since taste is rarely (8:00–20:00 h). Food was available ad libitum but access found isolated under natural conditions, but it is associ- to water was restricted to the daily experimental 15-min ated with other components, such as odor, becoming drinking sessions at 10:00 h and to a daily additional more appropriate to use the term “flavor”. Indeed, using 20-min rehydration session at 16:00 h. Water Baseline a cider vinegar solution, a flavor which contains the ace - (BL) was recorded during the morning sessions in which tic acid odorous component, we have reported increased the rats were handled for 3–5 min after BL1, BL3 and BL5 activity during the second exposure in the nucleus in order to avoid stress. After the water intake baseline, accumbens shell [7] and the medial prefrontal cortex [8]. the animals were randomly assigned to one of the follow- However, there is no data about the role of BLA in the ing groups: Novel (n = 8), Familiar (n = 5) and Control vinegar familiarization process. (n = 8). A cider vinegar solution (3%) was available during Cytochrome oxidase (CCO) is a marker of neural activ- one (Novel) or two (Familiar) experimental sessions. The ity that indicates ATP increases and decreases according control group drank water throughout the experiment. to the oxidative metabolic activity requirements. Thus, Ninety minutes after the experimental session each unlike other markers, CCO allows us to detect not only animal was sacrificed, the brain was removed and quickly increases but decreases of brain activity. This technique frozen in isopentane (2-methylbutane; Sigma-Aldrich, has been previously applied to assess changes of the Germany) to be stored at − 80 ºC. Brain coronal Sec- brain metabolic activity associated with taste familiarity tions (20 µm) were cut in a cryostat (Microm, HM505E, on aversive conditioning using a latent inhibition proce- Germany). From each brain, sixty sections were taken in dure [9]. Likewise, CCO histochemistry has proven to be order to assess CCO in BLA, Cpu and Pir. The stereotaxic of great value to map functional brain networks involved coordinates of the brain areas assessed according to the in spatial learning acquisition [10, 11], retrieval [12] and Paxinos and Watson atlas [18] are shown in Fig. 1. extinction [11]. It is also sensitive to the effect of various The procedures were approved by the University of treatments on spatial memory, such as social isolation Granada Ethics Committee for Animal Research and by [13], maternal separation [14], exercise [15] and pharma- the Regional Ministry of Agriculture, Fisheries and Rural cological interventions [16]. Development of Andalusia (17-02-15-195), following the Hence, CCO quantification during the first and sec - ARRIVE guidelines and in accordance with the EU Direc- ond vinegar exposures would allow us to assess the tive 2010/63/EU for animal experiments. M enchén‑Márquez et al. Behavioral and Brain Functions (2023) 19:2 Page 3 of 6 Fig. 1 Anatomical location of Regions of Interest. BLA = Basolateral amygdala (− 2.52 mm), Cpu = Caudate/Putamen (− 0.12 mm), Pir = Piriform cortex (− 2.52 mm). Anteroposterior coordinates according to bregma [17]. All coordinates were taken from coronal brain slices CCO histochemistry 12 measurements per region and subject. These regions The procedure for quantitative CCO histochemistry has were averaged to obtain one mean per region for each been described elsewhere [13, 19]. In brief, after obtain- animal. Then, OD values were converted to CCO activity ing sets of tissue homogenate standards from the Wistar units determined through the enzymatic activity of the rat at different thicknesses (10, 30, 50 and 70 µm) in order standards measured spectrometrically. to quantify the enzymatic activity, both sections and standards were incubated for 5 min in 0.1 M phosphate Experimental design and statistical analyses buffer (7.6 pH) with 10% sucrose (w/v) and 5% glutaral - Flavor neophobia and AN were assessed using a two-fac- dehyde (v/v) (Merck, Germany). The slides were then tor mixed ANOVA design that includes a between-groups rinsed 3 × in a 0.01 M phosphate buffer (7.6 pH) with factor Group with 2 levels (Control group drinking water; 10% sucrose (w/v) and 0.05 M Tris buffer (7.6 pH) with Familiar group drinking vinegar twice) and a within-sub- 275 mg/L hexahydrated cobalt chloride, 10% sucrose jects factor Days with 3 levels (Water baseline, first vine - (w/v), and 0.5% dimethylsulfoxide (v/v) for 10 min. This gar exposure, second vinegar exposure), being the rat ID was followed by 1 × 0.01 M phosphate buffer (7.6 pH). the random factor (animals were randomly assigned to Then, the sections and standards were incubated in groups). Post-hoc Bonferroni tests were applied. 0.0075% cytochrome-c (w/v), 0.002% catalase (v/v), 5% Given the need to sacrifice the animals for assess - sucrose (w/v), 0.25% dimethylsulfoxide (v/v) and 0.05% ing brain CCO activity, an additional Novel group was diaminobenzidine tetrahydrochloride (Sigma-Aldrich, required. u Th s, a two-factor mixed ANOVA design was Madrid, Spain). Both sections and standards were incu- applied including a between-groups factor Group with 3 bated for 5 min in 0.1 phosphate buffer (7.6 pH), at 37 ºC levels (Control group drinking water; Novel group drink- for 1 h. The reaction was stopped by fixing the tissue in ing vinegar once, Familiar group drinking vinegar twice) buffered 4% (v/v) formalin 30 min RT. Finally, the slides and a within-subjects factor Region of Interest (ROI) with were dehydrated, cleared with xylol and cover-slipped 3 levels (BLA, Cpu, Pir). Again, since animals were ran- with Entellan (Merck, Germany). The intensity of the domly assigned to the groups, rat ID was the random fac- CCO staining was quantified through an optic densitom - tor. Post-hoc comparisons were performed with post-hoc etry analysis using a computerized image analysis system Bonferroni tests. (MCID Elite, Interfocus Imaging Ltd., United Kingdom). The mean optical density (OD) of each region was meas - Results ured in the right hemisphere using three consecutive Figure 2 shows the mean (± SEM) intake of the Famil- sections. In each section, four non-overlapping read- iar group drinking the 3% cider vinegar solution that ings were taken using a square-shaped sampling window evidence the neophobic response and its attenuation on that was adjusted for each region size, taking a total of the second presentation in comparison with the Control Menchén‑Márquez et al. Behavioral and Brain Functions (2023) 19:2 Page 4 of 6 Fig. 2 Mean (± SEM) consumption of each group during the water baseline, the first and the second exposure to water (Control) or cider vinegar solution (Familiar). * = p < 0.05 group drinking water. A mixed 2 (Group) × 3 (Days) 3 (Group) × 3 (ROI) ANOVA analysis was carried out. ANOVA analysis showed a within-subject Day effect Levene’s tests showed homogeneity of variances for [F(2, 18) = 41.121, p = 0.001, η = 0.820] and interaction all within-subject variables. The analysis revealed a of Group × Day [F(2, 18) = 61.407, p < 0.001, η = 0.872]. significant effect of ROI, [F (2,36) = 38.858, p < 0.001, A Group effect was found too [F(1, 9) = 23.982, p < 0.002, η = 0.179]. Neither the interaction Group × ROI 2 2 η = 0.727]. Levene’s test showed homogeneity of vari- [F(4, 36) = 1.964, p > 0.05, η = 0.683] nor the main p p ances for all within-subject variables. Post-hoc Bonfer- factor Group [F(2, 18) = 3.235, p > 0.05, η = 0.264] roni tests indicated that Group interaction is due to the were significant. Post-hoc Bonferroni tests showed Familiar group drank a lower amount of the novel vin- higher metabolic activity in BLA than Pir (p < 0.001) egar solution on Day1 than both the water (Baseline) and Cpu (p < 0.01), being Pir activity higher than Cpu (p < 0.001) and the familiar vinegar solution on Day2 (p < 0.005). Although the interaction was not signifi - (p < 0.03). No differences were found in the Control group cant, one-way ANOVA analyses were applied to each (p > 0.05). ROI because testing our hypotheses required gain- Regarding the CCO results, Fig. 3 show the mean ing knowledge about the difference between groups (± SEM) CCO units in each region of interest of the in BLA. They indicated significant differences only in three groups (Control, Novel and Familiar). A mixed BLA [F(2,18) = 5.365, p < 0.05, η = 0.373], but not Fig. 3 Mean (± SEM) brain metabolic activity of each region of interest (BLA, Pir, Cpu) when exposed to water (Control) or to a cider vinegar solution either once (Novel) or twice (Familiar). * = p < 0.05 M enchén‑Márquez et al. Behavioral and Brain Functions (2023) 19:2 Page 5 of 6 solution in comparison with those drinking water while in Pir [F(2,18) = 1.374, p > 0.05, η = 0.132] or Cpu there were no changes in those drinking the novel vine- [F(2,18) = 0.148, p > 0.05, η = 0.016]. Post-hoc Bon- gar solution. We have previously reported similar results ferroni tests showed that the Familiar group exhibited in the nucleus accumbens shell [7] and the medial pre- higher metabolic BLA activity than both Novel group frontal cortex [8]. Although our results do not allow us to drinking vinegar for the first time (p < 0.05) and Control draw a circuit approach, it is conceivable that BLA would group drinking water (p < 0.05). There were no differ - form a functional network with these areas. Hence, we ences between Novel and Control groups (p > 0.05). cannot discard that the reported BLA activity changes during AN could be driven by top-down control from Discussion areas such as the prefrontal cortex. Previous reports indi- The behavioral results are consistent with those previ - cated higher BLA activity during drinking a novel sac- ously reported [3]. Flavor neophobia and AN are evi- charin solution [6] but no effect of BLA lesions on odor denced by reduced intake of the novel vinegar solution neophobia using a 0.1% amyl acetate solution [4]. The which significantly increases on the second exposure as present findings would suggest the involvement of BLA the flavor becomes familiar. The results indicate higher in flavor familiarization but not novelty detection. Thus, BLA metabolic activity in the group exposed twice to the those flavors composed of an odorous component would vinegar solution than that exposed once. This supports a involve BLA activity during the formation of the flavor selective involvement of the area in the processes leading safe memory. to the formation of the safe taste memory but not novelty Our results confirm the value of the CCO technique to detection. Our results do not allow us to draw conclu- explore changes associated with learning and memory. sions regarding the specific process associated with BLA Hence, flavor recognition memory is added to taste and activity. A potential role of BLA in the retrieval of the fla - spatial learning in which CCO has proven to be a useful vor memory formed during the first exposure is conceiv - technique for identifying the brain areas involved. In fact, able. Both retrieval and stabilization of the safe memory previous reports indicated increased CCO activity in should be taking place in the second flavor exposure. BLA during the first day of training in a spatial learning Hence, it is feasible an association between the reported task [21]. increase in BLA activity and memory retrieval. In fact, Taken together, our results would support a relevant memory formation should have been initiated during the role of the amygdala either in retrieval and/or the stabili- first exposure but BLA activity changes were not found zation process leading to a safe flavor memory. at this stage. Also, the increased BLA activity during the second vinegar exposure could be associated with a Conclusions selective stabilization process. The main finding of the study is that BLA metabolic Moreover, since no significant effects were found in Pir, activity was higher in the group exposed to a familiar vin- this undercuts the hypothesis that the increased energy egar solution than in the groups exposed to either water expenditure in BLA could be due to enhanced olfactory or a novel vinegar solution. These results are consistent processing during the second exposure. This is consist - with results of lesion studies and support the basolateral ent with our previous findings using c-Fos immunohis - amygdala involvement in those processes leading to the tochemistry [20]. We did not find significant differences attenuation of flavor neophobia. between the activity induced by one and two vinegar exposures in neither the anterior nor the posterior piri- form cortex regions evaluated. In fact, we have previ- Abbreviations ously reported increased activity induced by drinking a AN Attenuation of neophobia BLA Basolateral amygdala well familiarized vinegar solution after six exposures, but CCO Cytochrome oxidase not after two, only in the rostral part of the posterior Pir Cpu Caudate/putamen [20]. This region corresponds to the level assessed in the OD Optical density Pir Piriform cortex present study. Thus, the absence of differences after two Prh Perirhinal cortex exposures confirms no role of Pir during the familiariza - ROI Region of interest tion process. Furthermore, the fact that no effect of flavor Acknowledgements exposures was found in Cpu corroborates a selective BLA Not applicable. involvement in flavor familiarization. These findings suggest that neophobia and AN might Author contributions Corresponding author SM-M carried out the behavioral part of the experi‑ be independent processes that rely on dissociable brain ment, performed the curation of both behavioral and histochemical data, areas. Accordingly, there was a selective increase of BLA as well as most of the formal analyses, wrote the original draft, made the activity in those animals drinking the familiar vinegar figures, edited and reviewed the draft for its consideration and worked in the Menchén‑Márquez et al. Behavioral and Brain Functions (2023) 19:2 Page 6 of 6 response to reviewers’ comments. MB was in charge of culling the animals 9. Gasalla P, Begega A, Soto A, Dwyer DM, López M. Functional brain net‑ for tissue, slicing, performing the histochemistry, and CCO density measures, works underlying latent inhibition of conditioned disgust in rats. Behav analyzed CCO data and created the related figures, helped with the final draft Brain Res. 2016. https:// doi. org/ 10. 1016/j. bbr. 2016. 07. 051. and worked in the response to reviewers’ comments. SM-M and MB contribu‑ 10. Conejo NM, González‑Pardo H, González‑Lima F, Arias JL. Spatial tions are considered to be similar. BG-C designed and supervised the whole learning of the water maze: progression of brain circuits mapped with behavioral part and helped with the behavioral data analysis. JLA and MG cytochrome oxidase histochemistry. Neurobiol Learn Mem. 2010. https:// conceptualized the original experiment, supervised the experiment, provided doi. org/ 10. 1016/j. nlm. 2009. 12. 002. the necessary infrastructure and resources, in addition to arranging financing, 11. Méndez‑ Couz M, González‑Pardo H, Vallejo G, Arias JL, Conejo NM. Spatial and reviewed the draft. Moreover, MG helped in the writing and reviewed the memory extinction differentially affects dorsal and ventral hippocampal draft and worked in the response to reviewers’ comments. All authors read metabolic activity and associated functional brain networks. Hippocam‑ and approved the final manuscript. pus. 2016. https:// doi. org/ 10. 1002/ hipo. 22602. 12. Conejo NM, Cimadevilla JM, González‑Pardo H, Méndez‑ Couz M, Arias JL. Funding Hippocampal inactivation with TTX impairs long‑term spatial memory Supported by the research projects PSI2017‑86381‑P; PSI2017‑83893‑R; retrieval and modifies brain metabolic activity. PLoS ONE. 2013. https:// PSI2017‑90806‑REDT (MINECO. Spain), PID2020‑114269 GB‑I00 (MICIU. España) doi. org/ 10. 1371/ journ al. pone. 00647 49. and FPU 16/06017 (pre‑ doctoral fellowship to S. Menchén‑Márquez; MECD, 13. Zorzo C, Méndez‑López M, Méndez M, Arias JL. Adult social isolation Spain). These experiments are part of the Ph.D. research conducted by S. leads to anxiety and spatial memory impairment: Brain activity pattern of Menchén‑Márquez. The authors of this manuscript state that there are no cur ‑ Cox and c‑Fos. Behav Brain Res. 2019. https:// doi. org/ 10. 1016/j. bbr. 2019. rent or potential conflicts of interest.03. 011. 14. Banqueri M, Méndez M, Arias JL. Why are maternally separated females Availability of data and materials inflexible? Brain activity pattern of Cox and c‑Fos. Neurobiol Learn Mem. The data that support the findings of this study are available from the cor ‑ 2018. https:// doi. org/ 10. 1016/j. nlm. 2018. 06. 007. responding author upon reasonable request. 15. Sampedro‑Piquero P, Zancada‑Menendez C, Begega A, Rubio S, Arias JL. Eec ff ts of environmental enrichment on anxiety responses, spatial memory and cytochrome c oxidase activity in adult rats. Brain Rest Bull. Declarations 2013. https:// doi. org/ 10. 1016/j. brain resbu ll. 2013. 06. 006. 16. Hescham S, Temel Y, Casaca‑ Carreira J, Arslantas K, Yakkioui Y, Blokland Ethics approval and consent to participate A, Jahanshahi A. A neuroanatomical analysis of the effects of a memory The procedures were approved by the University of Granada Ethics Commit‑ impairing dose of scopolamine in the rat brain using cytochrome c tee for Animal Research (Spain) and by the Regional Ministry of Agriculture, oxidase as principle marker. J Chem Neuroanat. 2014. https:// doi. org/ 10. Fisheries and Rural Development of Andalusia (17‑02‑15‑195; Spain), following 1016/j. jchem neu. 2014. 04. 001. the ARRIVE guidelines and in accordance with the EU Directive 2010/63/EU for 17. Expósito AN, Vázquez‑Ágredos A, Menchén‑Márquez S, Gámiz F, Gallo M. animal experiments. Taste Neophobia, Latent Inhibition of Taste Aversion and Object Recogni‑ tion Memory in Adolescent Rats. Psicothema. 2022 (Accepted). Competing interests 18. Paxinos G, Watson C. The rat brain in stereotaxic coordinates: Hard cover The authors of this manuscript state that there are no current or potential edition. 6th ed. New York: Elsevier/Academic Press; 2007. competing interests. 19. González‑Lima F, Cada A. Cytochrome oxidase activity in auditory system of the mouse: a qualitative and quantitative histochemical study. Neuro‑ science. 1994. https:// doi. org/ 10. 1016/ 0306‑ 4522(94) 90550‑9. Received: 30 June 2022 Accepted: 22 January 2023 20. Grau‑Perales AB, Gómez‑ Chacón B, Morillas E, Gallo M. Flavor recognition memory related activity of the posterior piriform cortex in adult and aged rats. Behav Brain Res. 2019. https:// doi. org/ 10. 1016/j. bbr. 2018. 12. 016. 21. Méndez‑ Couz M, Conejo NM, González‑Pardo H, Arias JL. Functional interactions between dentate gyrus, striatum and anterior thalamic References nuclei on spatial memory retrieval. Brain Res. 2015. https:// doi. org/ 10. 1. Morillas E, Gómez‑ Chacón B, Gallo M. Flavor and object recognition 1016/j. brain res. 2015. 02. 005. memory impairment induced by excitotoxic lesions of the perirhinal cortex. Neorobiol Learn Mem. 2017. https:// doi. org/ 10. 1016/j. nlm. 2017. Publisher’s Note 08. 002. Springer Nature remains neutral with regard to jurisdictional claims in pub‑ 2. Ramos JMJ. Perirhinal cortex supports both taste neophobia and its lished maps and institutional affiliations. attenuation. Neurobiol Learn Mem. 2020. https:// doi. org/ 10. 1016/j. nlm. 2020. 107264. 3. Gómez‑ Chacón B, Gámiz F, Gallo M. Basolateral amygdala lesions attenu‑ ate safe taste memory‑related c‑fos expression in the rat perirhinal cortex. Behav Brain Res. 2012. https:// doi. org/ 10. 1016/j. bbr. 2012. 02. 038. 4. Lin JY, Roman C, St. Andre J, Reilly S. Taste, Olfactory and trigeminal neophobia in rats with forebrain lesions. Brain Res. 2009. https:// doi. org/ Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : 10. 1016/j. brain res. 2008. 11. 040. 5. Lin JY, Arthurs J, Reilly S. The effects of amygdala and cortical inactiva‑ fast, convenient online submission tion on taste neophobia. Neurobiol Learn Mem. 2018. https:// doi. org/ 10. 1016/j. nlm. 2018. 08. 021. thorough peer review by experienced researchers in your field 6. Lin JY, Roman C, Arthurs J, Reilly S. Taste neophobia and c‑Fos expression rapid publication on acceptance in the rat brain. Brain Res. 2012. https:// doi. org/ 10. 1016/j. brain res. 2012. 02. support for research data, including large and complex data types 7. Grau‑Perales AB, Gómez‑ Chacón B, Gallo M. Differential activity pattern • gold Open Access which fosters wider collaboration and increased citations of c‑Fos in the nucleus accumbens between adult and aged rats during maximum visibility for your research: over 100M website views per year flavor recognition memory. Behav Brain Res. 2019. https:// doi. org/ 10. 1016/j. bbr. 2019. 111935. At BMC, research is always in progress. 8. Expósito AN, Morillas E, Gómez‑ Chacón B, Gallo M. Prefrontal cortex activ‑ ity patterns during taste neophobia habituation in adult and aged rats. Learn more biomedcentral.com/submissions Behav Brain Res. 2020. https:// doi. org/ 10. 1016/j. bbr. 2020. 112717.
Journal
Behavioral and Brain Functions – Springer Journals
Published: Feb 3, 2023
Keywords: Amygdala; Attenuation of neophobia; Cytochrome c oxidase; Flavor; Neophobia; Taste