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Animals
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From the Nose to the Brain: Animals' Olfactory and Vomeronasal...
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From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Animal Physiology".

Deadline for manuscript submissions: closed (28 February 2022) | Viewed by 95220

Special Issue Editor

Prof. Dr. Pablo Sánchez Quinteiro

E-Mail Website
Guest Editor
Department of Anatomy, Animal Production and Clinical Veterinary Sciences, Faculty of Veterinary, University of Santiago de Compostela, Av. Carballo Calero s/n, 27002 Lugo, Spain
Interests: animal anatomy; neuroscience; histology; immunohistochemistry; olfactory system
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The award of the Nobel Prize in 2004 to Richard Axel and Linda Buck marked a huge advance in the knowledge of the sense of smell. As a consequence, the last 15 years have witnessed an exponential progression in the number of studies about the olfactory and vomeronasal systems, which have forced a reformulation of prevalent ideas and hypotheses about both the processing of the olfactory signals and the chemocommunication mediated by the vomeronasal system.

However, we are still far from resolving such basic questions as the morphological and functional diversity of the olfactory subsystems, the molecular and biophysical natures of olfactory sensory transduction and, the still unresolved, anatomical and physiological basis of the human vomeronasal system.

Recently, with the advent of the dramatic COVID-19 pandemic, one of the cardinal symptoms of which is the loss of smell, to elucidate the cellular and molecular mechanisms of the coronavirus-induced anosmia may be instrumental in understanding the infectivity of SARS-CoV-2

For all this, we welcome experts in the fields to participate in this Special Issue, by means of original works and revision papers dealing with the anatomy, physiology, pathology, and molecular biology of the olfactory subsystems.

Prof. Pablo Sánchez Quinteiro
Guest Editor

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Keywords

  • olfactory system
  • vomeronasal system
  • chemocommunication
  • anosmia

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Published Papers (9 papers)

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Research

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17 pages, 12945 KiB  
Article
Flehmen, Osteophagia, and Other Behaviors of Giraffes (Giraffa giraffa angolensis): Vomeronasal Organ Adaptation
by Lynette A. Hart and Benjamin L. Hart
Animals 2023, 13(3), 354; https://doi.org/10.3390/ani13030354 - 19 Jan 2023
Cited by 3 | Viewed by 12786
Abstract
The size of adult male giraffes (Giraffa giraffa angolensis) far exceeds the size of the females. At the Namutoni waterholes in Etosha National Park, bulls were seen many times each day screening adult females for their pending sexual receptivity by provoking [...] Read more.
The size of adult male giraffes (Giraffa giraffa angolensis) far exceeds the size of the females. At the Namutoni waterholes in Etosha National Park, bulls were seen many times each day screening adult females for their pending sexual receptivity by provoking them to urinate; this mainly involved sniffing their genitalia. If the female accedes to the male’s invitation, she widens her hindleg stance, braces her body, and then urinates, usually for at least five seconds. The male places his muzzle and tongue in the urine stream, and then performs flehmen, often raising his head high in the air. Males never investigated urine on the ground. The bilateral papillae on the giraffe’s hard palate connect with the nasopalatine ducts, which enter the bilateral vomeronasal organ (VNO). Unlike many mammals, the giraffe’s VNO lacks a prominent connection to the nasal cavity and its connections to the oral cavity are primarily via the incisive papillae. Most days, some giraffes were observed searching for bones for extended periods, chewing them, and sometimes being troubled by a bone stuck in their mouth. A giraffe killed by lions was frequented for several days by a procession of giraffes investigating the carcass. A very dark-colored bull giraffe emitted loud pulsed growls that drove off most of the surrounding giraffes. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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16 pages, 1579 KiB  
Article
Canine Smell Preferences—Do Dogs Have Their Favorite Scents?
by Agata Kokocińska, Martyna Woszczyło, Silvestre Sampino, Michał Dzięcioł, Mikołaj Zybała, Anna Szczuka, Julita Korczyńska and Iwona Rozempolska-Rucińska
Animals 2022, 12(12), 1488; https://doi.org/10.3390/ani12121488 - 8 Jun 2022
Cited by 5 | Viewed by 10608
Abstract
The available evidence on dogs’ scent preferences is quite limited. The purpose of this study was to verify the canine response to selected odors that may also be preferred by humans. The experiment was performed using 14 adult dogs (10 female and 4 [...] Read more.
The available evidence on dogs’ scent preferences is quite limited. The purpose of this study was to verify the canine response to selected odors that may also be preferred by humans. The experiment was performed using 14 adult dogs (10 female and 4 male) of different breeds, body size, and age (1–14 years). During the experiment, dogs were exposed to 33 odor samples: a neutral sample containing pure dipropylene glycol (control) and 32 samples containing dipropylene glycol and fragrance oils. The dog was brought to the experimental area by its handler, who then stopped at the entrance, unleashed the dog, and remained in the starting position. The dog freely explored the area for 30 s. All dog movements and behavior were recorded and analyzed. The methodology of observing the dogs freely exploring the experimental area allowed us to determine the smells that were the most attractive to them (food, beaver clothing). Our study shows that dogs interacted more frequently with the scents of blueberries, blackberries, mint, rose, lavender, and linalol. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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25 pages, 14992 KiB  
Article
Comparative Neuroanatomical Study of the Main Olfactory Bulb in Domestic and Wild Canids: Dog, Wolf and Red Fox
by Irene Ortiz-Leal, Mateo V. Torres, Linda Noa López-Callejo, Luis Eusebio Fidalgo, Ana López-Beceiro and Pablo Sanchez-Quinteiro
Animals 2022, 12(9), 1079; https://doi.org/10.3390/ani12091079 - 21 Apr 2022
Cited by 7 | Viewed by 9373
Abstract
The sense of smell plays a fundamental role in mammalian survival. There is a considerable amount of information available on the vomeronasal system of both domestic and wild canids. However, much less information is available on the canid main olfactory system, particularly at [...] Read more.
The sense of smell plays a fundamental role in mammalian survival. There is a considerable amount of information available on the vomeronasal system of both domestic and wild canids. However, much less information is available on the canid main olfactory system, particularly at the level of the main olfactory bulb. Comparative study of the neuroanatomy of wild and domestic canids provides an excellent model for understanding the effects of selection pressure associated with domestication. A comprehensive histological (hematoxylin–eosin, Nissl, Tolivia and Gallego’s Trichrome stains), lectin (UEA, LEA) and immunohistochemical (Gαo, Gαi2, calretinin, calbindin, olfactory marker protein, glial fibrillary acidic protein, microtubule-associated protein 2) study of the olfactory bulbs of the dog, fox and wolf was performed. Our study found greater macroscopic development of the olfactory bulb in both the wolf and fox compared to the dog. At the microscopic level, all three species show a well-developed pattern of lamination and cellularity typical of a macrosmatic animal. However, greater development of cellularity in the periglomerular and mitral layers of wild canids is characteristic. Likewise, the immunohistochemical study shows comparable results between the three species, but with a noticeably higher expression of markers in wild canids. These results suggest that the reduction in encephalization experienced in dogs due to domestication also corresponds to a lower degree of morphological and neurochemical differentiation of the olfactory bulb. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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18 pages, 2900 KiB  
Article
The Arrangement of the Peripheral Olfactory System of Pleuragramma antarcticum: A Well-Exploited Small Sensor, an Aided Water Flow, and a Prominent Effort in Primary Signal Elaboration
by Stefano Aicardi, Matteo Bozzo, Andrea Amaroli, Lorenzo Gallus, Beatrice Risso, Erica Carlig, Davide Di Blasi, Marino Vacchi, Laura Ghigliotti and Sara Ferrando
Animals 2022, 12(5), 663; https://doi.org/10.3390/ani12050663 - 6 Mar 2022
Cited by 4 | Viewed by 3892
Abstract
The olfactory system is constituted in a consistent way across vertebrates. Nasal structures allow water/air to enter an olfactory cavity, conveying the odorants to a sensory surface. There, the olfactory neurons form, with their axons, a sensory nerve projecting to the telencephalic zone—named [...] Read more.
The olfactory system is constituted in a consistent way across vertebrates. Nasal structures allow water/air to enter an olfactory cavity, conveying the odorants to a sensory surface. There, the olfactory neurons form, with their axons, a sensory nerve projecting to the telencephalic zone—named the olfactory bulb. This organization comes with many different arrangements, whose meaning is still a matter of debate. A morphological description of the olfactory system of many teleost species is present in the literature; nevertheless, morphological investigations rarely provide a quantitative approach that would help to provide a deeper understanding of the structures where sensory and elaborating events happen. In this study, the peripheral olfactory system of the Antarctic silverfish, which is a keystone species in coastal Antarctica ecosystems, has also been described, employing some quantitative methods. The olfactory chamber of this species is connected to accessory nasal sacs, which probably aid water movements in the chamber; thus, the head of the Antarctic silverfish is specialized to assure that the olfactory organ keeps in contact with a large volume of water—even when the fish is not actively swimming. Each olfactory organ, shaped like an asymmetric rosette, has, in adult fish, a sensory surface area of about 25 mm2, while each olfactory bulb contains about 100,000 neurons. The sensory surface area and the number of neurons in the primary olfactory brain region show that this fish invests energy in the detection and elaboration of olfactory signals and allow comparisons among different species. The mouse, for example—which is considered a macrosmatic vertebrate—has a sensory surface area of the same order of magnitude as that of the Antarctic silverfish, but ten times more neurons in the olfactory bulb. Catsharks, on the other hand, have a sensory surface area that is two orders of magnitude higher than that of the Antarctic silverfish, while the number of neurons has the same order of magnitude. The Antarctic silverfish is therefore likely to rely considerably on olfaction. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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14 pages, 1612 KiB  
Article
Assessment of Biostimulation Methods Based on Chemical Communication in Female Doe Reproduction
by Paula R. Villamayor, Julián Gullón, Uxía Yáñez, María Sánchez, Pablo Sánchez-Quinteiro, Paulino Martínez and Luis Quintela
Animals 2022, 12(3), 308; https://doi.org/10.3390/ani12030308 - 27 Jan 2022
Cited by 3 | Viewed by 3576
Abstract
Biostimulation is an animal management practice that helps improve reproductive parameters by modulating animal sensory systems. Chemical signals, mostly known as pheromones, have a great potential in this regard. This study was conducted to determine the influence of short-term female rabbit exposure to [...] Read more.
Biostimulation is an animal management practice that helps improve reproductive parameters by modulating animal sensory systems. Chemical signals, mostly known as pheromones, have a great potential in this regard. This study was conducted to determine the influence of short-term female rabbit exposure to different conditions, mainly pheromone-mediated, on reproductive parameters of inseminated does. Groups of 60 females/each were exposed to (1) female urine, (2) male urine, (3) seminal plasma and (4) female–female (F–F) separated, just before artificial insemination, and compared to a ‘golden method’ female–female interaction. The following reproductive parameters were analyzed for each group: receptivity (vulvar color), fertility (kindling rate), prolificacy and number of born alive and dead kits/litter. Our results showed that the biostimulation methods employed in this experiment did not significantly improve any of the analyzed parameters. However, female doe exposure to urine, especially to male urine, showed no significant higher fertility values (95.4%) when compared to the rest of the experimental conditions (on average 92.4%). Female–female interaction before artificial insemination, which is a common practice in rabbit farms, showed similar results as not establishing social interaction (F–F separated), which suggests that F–F interaction could be replaced by F–F separated, therefore avoiding unnecessary animal management and time cost. On the other hand, fertility ranges were lower for animals with a pale vulvar color whereas no differences were noticed among the other three colors which measure receptivity (pink, red, purple), thus suggesting that these three colors could be grouped together. Future studies should aim at determining potential chemical cues/pheromones released through bodily secretions that influence reproduction in rabbits, therefore contributing to animal welfare and to a natural image of animal production. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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29 pages, 13212 KiB  
Article
Neuroanatomical and Immunohistological Study of the Main and Accessory Olfactory Bulbs of the Meerkat (Suricata suricatta)
by Mateo V. Torres, Irene Ortiz-Leal, Andrea Ferreiro, José Luis Rois and Pablo Sanchez-Quinteiro
Animals 2022, 12(1), 91; https://doi.org/10.3390/ani12010091 - 31 Dec 2021
Cited by 9 | Viewed by 4966
Abstract
We approached the study of the main (MOB) and accessory olfactory bulbs (AOB) of the meerkat (Suricata suricatta) aiming to fill important gaps in knowledge regarding the neuroanatomical basis of olfactory and pheromonal signal processing in this iconic species. Microdissection techniques [...] Read more.
We approached the study of the main (MOB) and accessory olfactory bulbs (AOB) of the meerkat (Suricata suricatta) aiming to fill important gaps in knowledge regarding the neuroanatomical basis of olfactory and pheromonal signal processing in this iconic species. Microdissection techniques were used to extract the olfactory bulbs. The samples were subjected to hematoxylin-eosin and Nissl stains, histochemical (Ulex europaeus agglutinin, Lycopersicon esculentum agglutinin) and immunohistochemical labelling (Gαo, Gαi2, calretinin, calbindin, olfactory marker protein, glial fibrillary acidic protein, microtubule-associated protein 2, SMI-32, growth-associated protein 43). Microscopically, the meerkat AOB lamination pattern is more defined than the dog’s, approaching that described in cats, with well-defined glomeruli and a wide mitral-plexiform layer, with scattered main cells and granular cells organized in clusters. The degree of lamination and development of the meerkat MOB suggests a macrosmatic mammalian species. Calcium-binding proteins allow for the discrimination of atypical glomerular subpopulations in the olfactory limbus between the MOB and AOB. Our observations support AOB functionality in the meerkat, indicating chemosensory specialization for the detection of pheromones, as identified by the characterization of the V1R vomeronasal receptor family and the apparent deterioration of the V2R receptor family. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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9 pages, 3876 KiB  
Article
Morphological and Histological Features of the Vomeronasal Organ in African Pygmy Hedgehog (Atelerix albiventris)
by Daisuke Kondoh, Yusuke Tanaka, Yusuke K. Kawai, Takayuki Mineshige, Kenichi Watanabe and Yoshiyasu Kobayashi
Animals 2021, 11(5), 1462; https://doi.org/10.3390/ani11051462 - 19 May 2021
Cited by 12 | Viewed by 4811
Abstract
The vomeronasal organ (VNO) detects specific chemicals such as pheromones and kairomones. Hedgehogs (Eulipotyphla: Erinaceidae) have a well-developed accessory olfactory bulb that receives projections from the VNO, but little is known about the hedgehog VNO. Here, we studied the histological features of the [...] Read more.
The vomeronasal organ (VNO) detects specific chemicals such as pheromones and kairomones. Hedgehogs (Eulipotyphla: Erinaceidae) have a well-developed accessory olfactory bulb that receives projections from the VNO, but little is known about the hedgehog VNO. Here, we studied the histological features of the VNO in five individual African pygmy hedgehogs by hematoxylin-eosin, periodic acid-Schiff, and Alcian blue stains. The hedgehog VNO comprises a hyaline cartilage capsule, soft tissue and epithelial lumen, and it branches from the site just before the incisive duct opening into the nasal cavity. The soft tissues contain several small mucous (or mucoserous) glands and a large serous gland, and many venous sinuses all around the lumen. The VNO lumen is round to oval throughout the hedgehog VNO, and the sensory epithelium lines almost the entire rostral part and medial wall of the middle part. These findings indicate that the VNO is functional and plays an important role in the hedgehog. Notably, the VNO apparently has a characteristic flushing mechanism with serous secretions like those of gustatory glands, which the hedgehog might frequently use to recognize the external environment. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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12 pages, 5765 KiB  
Article
Histological and Immunohistochemical Characterization of Vomeronasal Organ Aging in Mice
by Violaine Mechin, Patrick Pageat, Eva Teruel and Pietro Asproni
Animals 2021, 11(5), 1211; https://doi.org/10.3390/ani11051211 - 22 Apr 2021
Cited by 7 | Viewed by 3381
Abstract
The vomeronasal organ (VNO) plays a crucial role in animal behavior since it is responsible for semiochemical detection and, thus, for intra- and interspecific chemical communication, through the vomeronasal sensory epithelium (VNSE), composed of bipolar sensory neurons. This study aimed to explore a [...] Read more.
The vomeronasal organ (VNO) plays a crucial role in animal behavior since it is responsible for semiochemical detection and, thus, for intra- and interspecific chemical communication, through the vomeronasal sensory epithelium (VNSE), composed of bipolar sensory neurons. This study aimed to explore a well-recognized cause of neuronal degeneration, only rarely explored in this organ: aging. Murine VNOs were evaluated according to 3 age groups (3, 10, and 24 months) by histology to assess VNSE changes such as cellular degeneration or glycogen accumulation and by immunohistochemistry to explore nervous configuration, proliferation capability, and apoptosis with the expression of olfactory marker protein (OMP), Gαi2, Gαo, Ki-67, and cleaved caspase-3 proteins. These markers were quantified as percentages of positive signal in the VNSE and statistical analyses were performed. Cellular degeneration increased with age (p < 0.0001) as well as glycogen accumulation (p < 0.0001), Gαo expression (p < 0.0001), and the number of cleaved-caspase3 positive cells (p = 0.0425), while OMP and Gαi2 expressions decreased with age (p = 0.0436 and p < 0.0001, respectively). Ki67-positive cells were reduced, even if this difference was not statistically significant (p = 0.9105). Due to the crucial role of VNO in animal life, this study opens the door to interesting perspectives about chemical communication efficiency in aging animals. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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Review

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18 pages, 2606 KiB  
Review
The Shape of the Nasal Cavity and Adaptations to Sniffing in the Dog (Canis familiaris) Compared to Other Domesticated Mammals: A Review Article
by Anna Buzek, Katarzyna Serwańska-Leja, Anita Zaworska-Zakrzewska and Małgorzata Kasprowicz-Potocka
Animals 2022, 12(4), 517; https://doi.org/10.3390/ani12040517 - 19 Feb 2022
Cited by 17 | Viewed by 38870
Abstract
Dogs are a good starting point for the description and anatomical analysis of turbinates of the nose. This work aimed at summing up the state of knowledge on the shape of the nasal cavity and airflow in these domestic animals and dealt with [...] Read more.
Dogs are a good starting point for the description and anatomical analysis of turbinates of the nose. This work aimed at summing up the state of knowledge on the shape of the nasal cavity and airflow in these domestic animals and dealt with the brachycephalic syndrome (BOAS) and anatomical changes in the initial airway area in dogs with a short and widened skull. As a result of artificial selection and breeding concepts, the dog population grew very quickly. Modern dog breeds are characterized by a great variety of their anatomical shape. Craniological changes also had a significant impact on the structure and physiology of the respiratory system in mammals. The shape of the nasal cavity is particularly distinctive in dogs. Numerous studies have established that dogs and their olfactory ability are of great importance in searching for lost people, detecting explosives or drugs as well as signaling disease in the human body. The manuscript describes the structure of the initial part of the respiratory system, including the nasal turbinates, and compares representatives of various animal species. It provides information on the anatomy of brachycephalic dogs and BOAS. The studies suggest that further characterization and studies of nasal turbinates and their hypertrophy are important. Full article
(This article belongs to the Special Issue From the Nose to the Brain: Animals' Olfactory and Vomeronasal Systems)
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