ArticlePDF Available

The dog vomeronasal organ: A review

January 2016

DOI:10.4454/db.v2i1.27

Authors:

Alessandra Coli

University of Pisa

Elisabetta Giannessi

University of Pisa

The vomeronasal organ (VNO) or Jacobson's organ is an auxiliary olfactory sense organ in many vertebrates. This organ is involved in the Flehmen response and it is necessary for the detection of pheromones, chemical signals released to members of the same species for social and sexual communication. In this review the Authors report on the VNO in dog pointing out the morphogenesis, the structure and the neural pathway toward dog accessory olfactory bulb (AOB). By recent immunohistochemical studies it is highlighted that dog VNO neurons express only VR1 genes in their genome, unlike the rodents where VR1 and VR2 genes are expressed. Besides, the organization of AOB is lower than that of the rodents. This feature might be the result of VNO regressive process of a macrosmatic mammal, like dog.

Dog nasal septum (lateral view), sensory (yellow-brown) and respiratory (red-orange) mucosa, VNO localization (panel). From Barrios et al., 2014b.

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Dog VNO with incisive duct. From Evans: Miller's Anatomy of the dog, Saunders, Elsevier, 1993.

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Dog VNO (transverse section, caudal portion). Lateral epithelium (le) with few ciliated columnar cells (cc) and non-ciliated columnar cells (nc). Medial epithelium (me). From Adams & Wiekamp, 1984.

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Dog VNO (transverse section); left is lateral, up is dorsal. Lumen (asterisk); nerves (1); vessels (2); gland (3); connective tissue (4); cartilage (whitearrow). E/E. Scale bar: 500μm. From Barrios et al., 2014.

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The dog vomeronasal organ: a review

Alessandra Coli1,*, Maria Rita Stornelli1, Elisabetta Giannessi1

1Dipartimento di Scienze Veterinarie, Università di Pisa - Italy

Abstract: The vomeronasal organ (VNO) or Jacobson’s organ is an auxiliary olfactory sense organ in many verte-

brates. This organ is involved in the Flehmen response and it is necessary for the detection of pheromones, chemical sig-

nals released to members of the same species for social and sexual communication.

In this review the Authors report on the VNO in dog pointing out the morphogenesis, the structure and the neural

pathway toward dog accessory olfactory bulb (AOB). By recent immunohistochemical studies it is highlighted that dog

VNO neurons express only VR1 genes in their genome, unlike the rodents where VR1 and VR2 genes are expressed. Be-

sides, the organization of AOB is lower than that of the rodents. This feature might be the result of VNO regressive

process of a macrosmatic mammal, like dog.

Key Words: dog; morphofunctional study; vomeronasal organ.

* Corresponding Author: alessandra.coli@unipi.it

Introduction

The vomeronasal organ (VNO) consists of a pair of blind, tubular, mucomembranous ducts of

olfactory epithelium lying on each side of the rostral base of the nasal septum. It is surrounded by a

thin plate of cartilage and opens rostrally into the incisive duct of the same side that connects the

nasal and oral cavity.

VNO is considered a second olfactory organ involved in parental, social and sexual communica-

tion as a chemosensory organ which has the chemoreceptors necessary for the detection of

pheromones, chemical signals

released into the environment

to members of the same

species and of flavor of food.

The VNO is also related to

‘Flehmen reaction’, a peculiar

retraction of upper lip (Ylmaz

et al., 2007).

VNO neurons are closely

related to the hypothalamus

and participate in its activa-

tion via the accessory olfacto-

ry bulb (AOB) and the amyg-

dala (Keverne, 1999).

Dog Behavior, 1-2016, pp. 24-31

doi 10.4454/db.v2i1.27

Received, 01/25/2016

Accepted, 03/09/2016

Fig. 1. Dog nasal septum (lateral view), sensory (yellow-brown) and

respiratory (red-orange) mucosa, VNO localization (panel). From Bar-

rios et al., 2014b.

04Stornelli 24_colore_Layout 1 12/04/16 10:17 Pagina 24

VNO in the animal kingdom

VNO was first described by Jacobson (1813) in mammals nose: he assessed that the VNO was a

sensory and secretory organ.

Fig. 2. Jacobson’s drawing of the deer head (Cervus sp.). From Døving & Trotier, 1998.

Fig. 2 is a reproduction of Jacobson’s drawing of the head of a deer (Cervus sp.), showing the lo-

calization of VNO with its nerves running to the olfactory bulb. Jacobson also pointed out that the

VNO diameter became greater cranio-caudally and that many glands were localized in the dorsal

and ventral VNO mucosa, with small secretory ducts ending in the lumen of the organ. Jacobson

described the VNO in many domesticated animals (cat, cow, dog, goat, horse, pig and sheep), and

not domesticate, (tiger, camel, buffalo, deer and seal) but not in birds (Jones & Roper, 1997) al-

though it is present in the embryo at a very early stage of development. The presence of VNO was

confirmed in most mammals (Von Mihalkovics, 1899; Pearlman, 1934) and it is well developed in

some primates (Nycticebus tardigradus and the Cebus capucinus) but reduced or absent in

Macaca mulatta (Jordan, 1972; Stark, 1975). Retzius (1894) demonstrated the chemosensory func-

tion of the organ in reptiles (snake embryo) for the similarity in morphology between the olfactory

neurons and VNO neurons running to the accessory olfactory bulb. Von Mihalkovics (1899) evi-

denced that the sensory ciliated cells were on the medial concave surface of the VNO cavity while

the lateral convex surface is lined with no sensory cells. He also described a cavernous tissue, or

“eminentia fungiformis”, under the mucosa.

VNO development: morphogenesis

With regard to the VNO development (Garrosa et al., 1998), the VNO originates from the me-

dial wall of the olfactory pit (VNO placode) and consists of a cellular bud growing dorsally, cau-

dally and medially that forms the VNO groove. During morphogenesis the VNO groove closes

forming a blind-ended tube laterally the nasal septum, which opens into the oral cavity by the

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incisive duct in dog. In cross section the VNO shows a shape similar to a kidney and the epitheli-

um on the concave side, in a medial position, become wider and neuroblasts, supporting and un-

differentiated cells develop. The epithelium on the convex side (‘‘non-sensory’’ epithelium), is in

a lateral position and become thinner. During late morphogenesis, VNO acquires adult shape

and at birth, medial and lateral epithelia becomes similar to the adult. Histochemical and ultra-

structural features suggest that full performance of the VNO does not occur at birth but in pre-

pubertal ages.

VNO histology

The structure of the dog VNO has been reported in several studies (Barone et al., 1966; Klein,

1881; Ramser, 1935), where VNO is described as reduced, containing no true olfactory receptors

(Barone et al., 1966) and histologically and ultrastructurally similar to that of the cat, guinea-pig,

mouse and rabbit (Ciges et al., 1977).

Fig. 3. Dog VNO with incisive duct. From Evans: Miller’s Anatomy of the dog, Saunders, Elsevier, 1993.

Adams & Wiekamp (1984) prove that dog VNO is highly developed. They study the VNO in

mature dogs with the optical, transmission electron and scanning electron microscopes. The au-

thors report a crescent-shaped lumen adjacent to the nasal septum and enclosed partially by a J-

shaped vomeronasal cartilage, lacking in the dorsal lateral wall. In cross section dog VNO lumen

shows a lateral convexity along most of its length and a concavity medially in anterior portions and

ventrally in caudal portions.

Both convex and concave surfaces of the epithelium show a well vascularized lamina propria.

Small nerves deep to the medial epithelium are unmyelinated while those deep to the lateral epithe-

lium usually contains some myelinated fibers. Dorsal and lateral to the VNO glands present ducts

opened into the lumen through the epithelial commissures and the lateral epithelium, less fre-

quently through the medial epithelium. The lumen is filled with fluid from the VNO glands.

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As reported by Adams & Wiekamp (1984), the epithelium of the lateral convex mucosa, named

Non-Sensorial Epithelium (NSE) (Barrios et al., 2014b) is pseudostratified contained basal, non-cil-

iated columnar, ciliated columnar and goblet cells. Ciliated cells had a like-dome apex with numer-

ous cilia and long basal bodies. The non-ciliated cells have a surface border of microvilli and are the

most represented. The cilia irregularly distributed might favor the mixing of fluid in VNO lumen

so that the contact between molecules and receptor cells is enhanced.

As reported by Keverne (1999), the epithelium of the medial concave mucosa, named Sensorial

Epithelium (SE) (Barrios et al., 2014b) is pseudostratified containing basal or stem cells along the

basal membrane, supporting cells lying in superficial layer of the epithelium, and receptor cells.

This epithelium extends far caudally, unlike rat (Vaccarezza et al., 1981) and hamster (Taniguchi &

Mochizuki, 1982). The receptor neurons show apical microvilli, unlike the presence of only one cil-

ium on the surface of other mammalian VNO receptors (Ciges et al., 1977; Vaccarezza et al., 1981;

Salazar et al., 1984).

Fig. 4. Dog VNO (transverse section,

caudal portion). Lateral epithelium (le)

with few ciliated columnar cells (cc)

and non-ciliated columnar cells (nc).

Medial epithelium (me). From Adams &

Wiekamp, 1984.

Fig. 5. Dog VNO (transverse section); left is lateral, up is dor-

sal. Lumen (asterisk); nerves (1); vessels (2); gland (3); connec-

tive tissue (4); cartilage (whitearrow). E/E. Scale bar: 500μm.

From Barrios et al., 2014.

04Stornelli 24_colore_Layout 1 12/04/16 10:17 Pagina 27

Sano and Okano (1995) divide dog VNO in a vestibular, rostral, body and caudal portion, with

SE only in the medial wall of the body portion, which is comprised between the level of the canine

teeth and the edge of the third premolar teeth.

In mammals, by in situ hybridization, two families of G protein-linked receptors (VR1 and VR2)

are expressed in a distinct region of the VNO; each neuron expresses only one receptor (Dulac &

Axel, 1995). Barrios et al. (2014) point out that in the dog VNO only VR1 is expressed.

The neural patways: from the VNO to the brain

The neural pathways from the VNO mucosa to the brain are distinct from those of normal olfac-

tory mucosa (Scalia & Winans, 1975). This pathway projects to an accessory olfactory bulb (AOB)

(Salazar et al., 1992) by two or three nerves branches merging before the ethmoid bone. The nerves

penetrate the lamina cribosa by a single orifice to run along the media part of the olfactory bulb.

Dog AOB position and morphology remained vague for a long time (Cajal, 1902; Miodonoski,

1968). Salazar et al. (1992 and 1994) show that dog AOB has a lower organization compared to that

of the rodents; it presents a thick glomerular layer and thinner layer of mitral/tufted granular and

scattered glial cells. For this reason the dog AOB has a very simple structure with reduced lamina-

tion; in particular plexiform and mitral/tufted layers are indistinguishable. Nakajima et al. (1998)

by an immuno-histochemical study demonstrate the distribution of neurons in dog AOB: they

point out that the granular cells are present but in small number in respect to other mammals. Be-

cause the granular cells are inhibitory interneurons in the olfactory pathway, some differences of

the AOB function between dog and other animals are conceivable.

The mammalian olfactory system shows differences among mammals; in particular in rodents

are detected four different nasal areas: main olfactory epithelium (MOE), septal organ (SO),

Grüneberg’s ganglion (GG) and vomeronasal organ (VNO). Barrios et al. (2014b) point out that

dog olfactory system lacks of the SO and the GG, besides the absence of VR2 genes in the canine

genome. All these features might be the result of a regressive process of the dog olfactory system

(Salazar et al., 1984), despite that dog is a considered a macrosmatic mammal for its particular

sense of smell. The larger size of the canine nasal cavity might allow a better physical discrimina-

tion among odors than in the mouse (Schoenfeld & Cleland, 2005).

Another possible explanation of the dog VNO regression might be related to its domestication

dating back to 15.000 years ago because a smaller range of olfactory stimuli than undomesticated ani-

mals like rodents are required (Leonard et al., 2002; Savolainen et al., 2002). Also Salazar et al. (1984)

assumes that the more domesticate the specie the smaller the functional importance of the VNO.

Confirming this hypothesis Shi & Zhang (2008) and Niimura (2012) report that dog has 811 func-

tional olfactory receptor genes instead the mouse that has 1035 functional olfactory receptor genes.

The Authors agree with Barrios et al. (2014b) that a study of wolf VNO would significant to de-

termine whether the dog VNO might be a result of domestication.

Unresolved issues and future directions

Actually there are many evidences that the main olfactory system is involved also in pheromonal

communication. Indeed, previous works considered the “dual olfactory hypothesis”, sustaining that

the main and accessory olfactory bulb project in non overlapping areas of the brain in the basal te-

lencephalon. According to this hypothesis the olfactory and vomeronasal systems were organized

as anatomical pathways serving different functions. Recently (Martinez-Marcos, 2009; Tirindelli et

al., 2009), reported that, by genetic studies, the olfactory and vomeronasal epithelia are able to

process both olfactory cues as pheromones. A hypothesis predicts that main olfactory and

04Stornelli 24_colore_Layout 1 12/04/16 10:17 Pagina 28

vomeronasal pathways converge overlapping in the rostral basal telencephalon defining a new cate-

gory of mixed chemosensory cortex. Other hypothesis states that the two pathways of the accessory

olfactory bulb projects primary to amygdala as target and then tertiary pathways directed to ventral

striatum converge to a same sensory cortex. These hypotheses indicate that anatomical and func-

tional distinction between the olfactory and vomeronasal systems should be rewieved and they

could justify that, despite the reduction of the VNO development resulting in domestication, dog

should be considered a macrosmatic species.

The VNO function can also be evaluated by the studying behavioral alterations in spontaneous

or experimentally induced VNO lesions. Wysocki et al. (1991) in rodents, after VNO removing,

conclude that vomeronasal organ is determinant for modulating the behavior in reproductive func-

tion by the perception of pheromones. Booth et al. (2000) evidence the role of the sheep VNO in

lacking of recognition of neonatal offspring by cauterization of the nasoincisive duct which makes

nonfunctional this organ. Asproni et al. (2015) study the effects of inflammatory lesions of cat

VNO and point out the association between inflammatory lesions with intraspecific aggressive be-

havior. This type of investigation could also be applied to the dogs to determine the actual involve-

ment of the VNO in intraspecific communication and in the adaptive mechanism to new environ-

ments, as a recent study suggests (Osella et al., 2015).

Acknowledgments: we are grateful to Dr. Carla Lenzi for her contribution to bibliography re-

search.

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L’organo vomeronasale nel cane: una review

Alessandra Coli1*, Maria Rita Stornelli1, Elisabetta Giannessi1

1Dipartimento di Scienze Veterinarie, Università di Pisa - Italia

Sintesi

L’organo vomeronasale (VNO) consiste di un paio di dotti tubulari, a fondo cieco, mucomembranosi, rivestiti di epi-

telio olfattivo che sono collocati, uno per lato, nella porzione rostrale della base del setto nasale. Il VNO è circondato da

un sottile strato di cartilagine e si apre rostralmente nella cavità nasale o in quella buccale.

Il VNO è considerato un secondo organo olfattivo, coinvolto nella comunicazione in ambito parentale, sociale e ses-

suale, possedendo chemiorecettori necessari per il rilevamento dei feromoni.

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Il VNO fu descritto per la prima volta da Jacobson nel 1813 nel naso dei mammiferi e fu da lui ritenuto un organo con

attività sensoriale e secretoria.

La presenza del VNO fu confermata nella maggior parte dei mammiferi da studi posteriori ed è ora noto come sia ben

sviluppato in alcune specie di primati non umani-

Qualche decennio dopo le osservazioni di Jacobson, un altro anatomista, Retzius, lo descrisse nei rettili. Nel 1899 Von

Mihalkovics evidenziò che l’epitelio ciliato era posizionato sulla superficie concava mediale dell’organo mentre la superfi-

cie laterale era rivestita di cellule senza funzioni chemiorecettoriali, al di sotto delle quali è presente un tessuto cavernoso

detto “eminentia fungiformis”.

La struttura del VNO del cane è riportato in diversi studi dove è descritto come un organo di dimensioni ridotte, non

contenente veri recettori olfattivi e istologicamente simile a quello del gatto, cavia, topo e coniglio.

L’epitelio che riveste la porzione laterale, denominato Epitelio Non Sensoriale (NSE) è pseudistratificato e contiene

cellule basali, colonnari non ciliate, colonnari ciliate e globose. Le cellule ciliate hanno un apice a cupola con numerose ci-

lia e corpi basali. Le cellule non ciliate sono le più numerose e hanno una superficie cosparsa di microvilli. Le cilia, distri-

buite in modo irregolare, potrebbero favorire la miscelazione del fluido nel lumen del VNO in modo che il contatto tra le

molecole e le cellule recettoriali sia migliorato.

L’epitelio che riveste la porzione mediale, denominato Epitelio Sensoriale, è pseudo stratificato e contiene cellule basa-

li che sostengono le cellule più superficiali e quelle recettoriali. Questo tipo di epitelio si estende molto causalmente, a dif-

ferenza di quanto avviene nel ratto e nel criceto.

Sano e Okano suddividono il VNO del cane in quattro porzioni: vestibolare, rostrale, corpo e caudale. L’epitelio sen-

soriale sarebbe presente nella porzione del corpo che è compresa tra il canino e l’apice del terzo premolare.

La via neurale dal VNO al cervello è distinta da quelle delle mucosa olfattiva normale. Questa via proietta al bulbo ol-

fattivo accessorio attraverso due o tre branche nervose che emergono prima dell’osso etmoide.

Il sistema olfattivo presenta differenze notevoli tra i diversi mammiferi; in particolare nei roditori sono individuabili

quattro differenti aree nasali: l’epitelio olfattivo principale, l’organo settale, il ganglio di Grüneberg e il VNO. Il sistema

olfattivo del cane è privo dell’organo settale e del ganglio di Grüneberg. Tutti questi aspetti, oltre alla mancanza del gene

VR2 nel genoma canino, potrebbero essere il risultato di un processo di regressione del sistema olfattivo del cane, nono-

stante questo animale sia considerato un mammifero macrosmatico per il suo particolare olfatto. Tuttavia la maggior di-

mensione della cavità nasale del cane potrebbe comunque permettere una migliore discriminazione fisica degli odori ri-

spetto al topo.

Un’altra possibile spiegazione della regressione del VNO nel cane potrebbe essere la domesticazione a cui questo ani-

male è stato sottoposto da almeno 15 mila anni.

Recentemente alcuni studi hanno valutato il ruolo del VNO nella comunicazione animale, osservando le alterazioni

del comportamento quando tale organo sia lesionato, in modo spontaneo o sperimentale.

Nei roditori il VNO risulta indispensabile nel modulare il comportamento riproduttivo, permettendo la percezione

dei feromoni sessuali. Negli ovini, il riconoscimento dell’agnello da parte della madre non avviene se si rende non funzio-

nante il VNO attraverso la cauterizzazione del dotto naso-incisivo. Nel gatto, processi infiammatori del VNO sembrano

correlati a fenomeni di aggressività.

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Full-text available

Aug 2023

Pigs are widely acknowledged for their olfactory abilities. Research on pigs’ olfactory capacities has focused mainly on aspects of olfaction that directly impact production, such as palatability of feed and pheromones to stimulate reproduction. Several basic research questions remain unanswered, such as which odors do pigs like/dislike, and how may odors enrich their lives? This review aims to explore the currently available literature on pig olfaction to elucidate the current knowns and unknowns within the following topics: chemicals in a pig’s environment, the olfactory organs of pigs, olfactory detection and acuity, behavioral reactions to odors, aversive odors, reaction to novel odors, attractive odors, and odors as a management tool in commercial pig production. The review focuses on complex odors of non-social origin (e.g., ammonia), and when information on this topic is lacking we include information from research on other mammalian species. We found that the olfactory organs of pigs are already functional at birth and that piglets can recognize the smell of the sow within 12h postpartum. Compared with humans and several other mammalian species, the pig’s olfactory system is highly developed, and the use of their sense of smell is incorporated into their natural behavior. While sniffing is a well-known behavior in pigs’ exploratory behavioral repertoire, this review points to a lack of knowledge on pigs’ behavioral reactions specifically when exposed to odors. Some odors appear attractive to pigs, whereas others appear repellent. Depending on the properties of the odor, providing pigs access to odors may be a way to stimulate their sense of smell, and could possibly be used in commercial pig production to enrich their lives. The review lastly highlights potential risks for animal welfare caused from lacking knowledge about how pigs perceive odors in their environment, and proposes future research questions and ways to utilize pigs’ sense of smell in the daily management of these animals. Further research on the olfactory abilities of pigs could help to ensure a more sustainable pig production.

Plenary presentation: Pig olfaction – a well-known yet overlooked sensory modality

Presentation

Sep 2022

Pigs are widely acknowledged for their sense of smell, but how much do we know about this sensory modality in pigs? There are numerous basic questions that remain unanswered, such as: What odours are pigs able to smell? And what odours are they interested in? These questions need to be addressed to identify the odours best suited to enrich the life of our farmed pigs. This review aims to explore the currently available literature on olfaction and olfactory abilities of pigs to elucidate the current knowns and unknowns within the topic. We further want to highlight potential risks for animal welfare that the lacking knowledge poses and propose new promising research questions and ways to utilize pigs’ sense of smell in the daily management of the animals. Where we, as humans, direct our eyes (i.e. vision) towards the point of attention, pigs will direct their ears and/or snout. Studies suggest that the olfactory organ of pigs is functional already at birth and that piglets can recognize the smell of the sow within 12h postpartum. When compared to humans, and several other animal species, the pig’s olfactory system is more prominent, and their olfactory detection threshold is lower than for other mammalian species. Olfaction serves a variety of functions for pigs, for instance pigs use odours for the recognition of familiar individuals/group mates, social status, sexual receptivity, and to keep roaming bands together. Further, sniffing is a well-known part of pigs’ exploratory behaviour. Still, there is a lack of knowledge of pigs’ behaviour when exploring odours (other than sniffing and appetitive behaviour). Further research on the olfactory abilities of pigs is greatly needed and may ultimately ensure a more sustainable pig production in terms of improved animal welfare. With this review, we want to spark discussion of the challenges this research area may pose to the industry and potential ways to move forward.

The Value of Sniffing: A Scoping Review of Scent Activities for Canines

Article

Full-text available

Dec 2024
APPL ANIM BEHAV SCI

Establishing the volatile organic compound profile and detection capabilities of human remain detection dogs to human bones

Article

Full-text available

Dec 2024

The detection of skeletal remains using human remain detection dogs (HRD) is often reported anecdotally by handlers to be a challenge. Limited studies have been conducted to determine the volatile organic compounds (VOCs) emitted from bones, particularly when there is limited organic matter remaining. This study aimed to determine the VOCs emitted from dry, weathered bones and examine the detection performance of HRD dogs on these bones when used as training aids. The VOCs of four different bones (clavicle, rib, humerus, and vertebrae) from three cadavers were collected using sorbent tubes and analyzed using comprehensive two-dimensional gas chromatography‒time-of-flight mass spectrometry (GC × GC‒TOFMS). Subsequently, the responses of the HRD dogs to the bone samples were recorded over two separate two-day trials. A total of 296 VOCs were detected and classified into chemical classes, with aromatics and linear aliphatics being the most abundant classes. Several differences in the chemical class distribution were observed between the bone types, but the number and intensity of the VOCs were similar between the bone samples. During the HRD dog training, a higher false detection rate was observed on the first day of each trial; however, the detection rate improved to 100 % on the second day of each trial. Although the dogs are capable of detecting bones, they require exposure to and training with a diverse range of skeletal remains to enhance their efficiency. This is necessary due to the variations in the types and intensity of VOCs compared to earlier decomposition stages involving soft tissue.

Canine Smell Preferences—Do Dogs Have Their Favorite Scents?

Article

Full-text available

Jun 2022

Simple Summary There are many products that are targeted to pet owners. One category of these products is dog repellents—strongly aromatized solutions designed to stop dogs from approaching and investigating particular areas; the second are cosmetics which should be pleasant for dogs. Dogs have a particularly sensitive sense of smell; therefore, strong scents may be very intense, and not always pleasant, stimuli. It is truly interesting, then, that canine cosmetic products often have very strong fragrances designed mostly to appeal to the dog owners, rather than to the dogs themselves. Indeed, the scents that dogs choose to put on their fur differ strongly from those of common cosmetics. Dogs choose mostly intense, animal-derived smells, such as feces or carcasses, so there is a need to differentiate between canine and human smell preferences. As there is limited scientific data related to canine smell preferences, the purpose of this study was to verify dogs’ reactions to selected scents, which can also be appealing to humans. Our study shows that dogs were more likely to interact with the scents of blueberry, blackberry, mint, rose, lavender, and linalol. 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 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.

MRI Features of the Vomeronasal Organ in Dogs (Canis Familiaris)

Article

Full-text available

Mar 2020

According to current knowledge, the vomeronasal organ (VNO, Jacobson's organ) is the structure responsible for semiochemical signal detection. In dogs and other mammals, it is located close to the vomer and palatine processes of the incisive and maxillary bones. Although there are reports describing the anatomy and histology of this structure, there are limited available reports assessing this organ in live individuals and no direct visualization reports in dogs. The aim of this study was 2-fold: (1) preparation and optimization of a protocol for magnetic resonance imaging (MRI) examination of the VNO in a cadaver study with precise visualization and localization, and (2) characterization of the physiological VNO image features in MRI of live dogs. The first part of the study was performed on 10 beagle cadavers, the second on 8 live beagle dogs. For the VNO visualization, a 1.5T MRI (Philips® Ingenia) scanner and 20-channel digital head-neck spine coil were used (Philips®, Holland). The cadaver study allowed confirmation of the organ's location by the topical application of an MRI contrast agent (gadolinium) via the external entrance of the VNO canal. Accurate delineation of the VNO was obtained using a high resolution submillimeter three-dimensional T1-fast field echo (FFE) 3D sequence. Imaging of the VNO in 8 living dogs allowed the description of the morphological MRI features and direct evaluation of its shape and size. The results obtained demonstrate the ability to visualize the VNO in vivo and to evaluate its structure in dogs.

A review on the effects of sensory stimulation in shelter dogs

Article

Jan 2018

Giacomo Riggio

Millions of dogs enter public and private shelters every year. Shelters are often very stressful environments to dogs, which are kept in very limited space and are impeded to appease their social motivations. Furthermore, the environmental stimuli provided are generally quantitatively - hyper/hypo-stimulation - and qualitatively inadequate. In such conditions dogs are likely to develop abnormal behaviors as maladaptive coping strategies that are not only a symptom of low welfare, but they also drastically decrease their chances of being permanently adopted. Environmental enrichment, such as training sessions, additional cage furniture and food-filled toys have been shown to decrease levels of stress in confined dogs. However, many of these programs require a noticeable financial and time commitment. Unfortunately, many shelter running institutions lack necessary funds, personnel and time to provide their dogs with complex environmental enrichment programs. In this light, sensory stimulation may represent a scientifically valid, low-cost and no time-wasting instrument to enhance the average level of welfare of shelter dogs, limit the development of behavioral problems and increase dog adoptability.

A neuroscience-based approach to the assessment of sexual behavior in animals

Article

Full-text available

Apr 2023

Sexual behavior in animals is important in ensuring the continuity of the generation. These behaviors differ in animal species. Sexual behaviors are shaped under the control of the reproductive system. Physiological stimuli produced by the reproductive system find their counterparts in the organism as reproductive activity. Reproductive activity display a critical role by transferring on the genetic heritage of organisms to the next generations. This activity, which is built on delicate balances, is associated with many systems in the organism. Nervous system, hormonal system, and circulatory system are the main ones. The regular formation of the reproductive activity in species is due to the effect of various factors. In domestic mammals, the reproductive activity is regulated by hormones secreted from brain and endocrine glands. Many hormones have duties in terms of the sustainability of reproductive activity. GnRH is the main hormone responsible for initiating this reproductive activity. Gonadotropin-releasing hormone (GnRH), which is a small molecule peptide from certain nerve cells in the nucleus infundibularis region of the hypothalamus and consists of different amino acids, is secreted under the influence of smell, temperature, light, and physical stimulation. Besides, GnRH release is controlled by various neurotransmitters (adrenaline, noradrenaline, dopamine, acetylcholine, serotonin). On the other hand, various genetic factors in secretory glands, gonadal cells, reproductive tissues can lead to significant changes on reproductive activity through specific molecular pathways and mechanisms.

LXI. Jacobson's Organ (Organon Vomero-Nasale, Jacobsoni): Its Anatomy, Gross, Microscopic and Comparative, with Some Observations as Well on its function.

Article

Full-text available

Jun 2016
Ann Otol Rhinol Laryngol

Samuel J. Pearlman

Adaptive mechanisms in dogs adopted from shelters: A behavioral assessment of the use of a synthetic analogue of the canine appeasing pheromone

Article

Full-text available

May 2015

Adaptation to a new socio-environment might represent a very hard step for sheltered dogs, because of a higher level of difficulty in coping with unfamiliar conditions. The adaptation process can be logically and scientifically related to the concept of stress and welfare, limiting the success rate of rehoming. A synthetic analogue of the Dog Appeasing Pheromone (Dog Appeasing Pheromone, DAP) is reported to have a reassuring effect in puppies and adult dogs in a wide variety of stressful situations. The aim of the current study was to investigate the effects of DAP (Adaptil ® Ceva Vetem S.p.A.) in dogs re-homed from rescue shelters. The study was designed as a prospective open-label clinical trial. Significant decreases were observed in adult dogs for wandering in the house restlessly (p=0.022) and hiding fearfully in protected corners (p=0.033), whereas in puppies treatment with DAP significantly (p<0.05) improved the reaction towards unfamiliar dogs (p=0.048) and wandering in the house restlessly (p=0.022). In both adults and puppies a significant improvement in interaction with owners was observed. In particular, " looking continuously for the owners " and " following the owners everywhere like a shadow " were significantly improved (p=0.0012 and 0.0016 respectively) in adult dogs. Separation reactions revealed a significant decrease (p<0.05) and in puppies the tendency to vocalize in absence of the owner was also significantly reduced (p=0.0029). Both adults and puppies showed a decreased tendency to wake suddenly in the night (p=0.024 and p=0.026 respectively) and wander around the home (p=0.012 and p=0.026 respectively). In contrast, for house-training no significant difference was reported in adults, whereas for puppies there was a significant decrease (p<0.05) in the mean scores for urination and/or defecation wherever in the house and after coming home. Data regarding the overall assessment suggested a significant improvement in all the efficacy variables considered in the study. The analysis of owners' degree of satisfaction at the final visit showed that DAP treatment was considered successful by 84.4 % of owners. Results suggest that DAP might improve dogs' adaptability throughout the first weeks following adoption and can be considered a useful tool for reducing stress in re-homed dogs.

Pathology and behaviour in feline medicine: investigating the link between vomeronasalitis and aggression

Article

Full-text available

Aug 2015

The aim of the study was to investigate if the feline vomeronasal organ (VNO) can be affected by inflammatory lesions and if these changes are associated with behavioural alterations. VNOs from 20 cats were sampled during necropsy, submitted for routine tissue processing and stained with haematoxylin and eosin for histopathological evaluation. Of the 20 cats, data on the presence of aggressive behaviours towards cats or humans were collected by questionnaire survey at the point of death. Inflammatory lesions were classified depending on the duration of the process as acute or chronic, both in vomeronasal sensory epithelium (VNSE) and in non-sensory epithelium (NSE). Fisher’s exact test was used to compare VNO inflammation with behavioural data.The VNSE was inflamed in 11/20 VNOs (55%) while the NSE was inflamed in 13/20 (65%). Overall, the VNO was affected by inflammation in 14/20 (70%) cats, and all the lesions were classified as chronic. Five out of 20 cats (25%) had documented intraspecific aggressive behaviours and 8/20 (40%) had shown aggression towards humans. Fisher’s exact test showed a statistically significant correlation between inflammation of the VNSE and intraspecific aggression (P = 0.038). No statistically correlations were observed between VNSE inflammation and aggression towards humans and between NSE inflammation and aggression towards cats or humans. Conclusions and relevance Our results show, for the first time, the existence of vomeronasalitis in animals and its possible association with intraspecific aggressive behaviours. The inflammatory microenvironment could impair VNSE functionality, causing intraspecific communication alterations, probably through a reduction in chemical communication action and perception. Owing to the pivotal role of the VNO in the social life of cats and other species, this report provides a rationale to further investigate this disease in relation to a variety of behavioural disorders.

Dog and mouse: Toward a balanced view of the mammalian olfactory system

Article

Full-text available

Sep 2014

Although the most intensively studied mammalian olfactory system is that of the mouse, in which olfactory chemical cues of one kind or another are detected in four different nasal areas [the main olfactory epithelium (MOE), the septal organ (SO), Grüneberg's ganglion, and the sensory epithelium of the vomeronasal organ (VNO)], the extraordinarily sensitive olfactory system of the dog is also an important model that is increasingly used, for example in genomic studies of species evolution. Here we describe the topography and extent of the main olfactory and vomeronasal sensory epithelia of the dog, and we report finding no structures equivalent to the Grüneberg ganglion and SO of the mouse. Since we examined adults, newborns, and fetuses we conclude that these latter structures are absent in dogs, possibly as the result of regression or involution. The absence of a vomeronasal component based on VR2 receptors suggests that the VNO may be undergoing a similar involutionary process.

Olfactory Receptor Multigene Family in Vertebrates: From the Viewpoint of Evolutionary Genomics

Article

Full-text available

Apr 2012
CURR GENOMICS

Yoshihito Niimura

Olfaction is essential for the survival of animals. Diverse odor molecules in the environment are detected by the olfactory receptors (ORs) in the olfactory epithelium of the nasal cavity. There are ~400 and ~1,000 OR genes in the human and mouse genomes, respectively, forming the largest multigene family in mammals. The relationships between ORs and odorants are multiple-to-multiple, which allows for discriminating almost unlimited number of different odorants by a combination of ORs. However, the OR-ligand relationships are still largely unknown, and predicting the quality of odor from its molecular structure is unsuccessful. Extensive bioinformatic analyses using the whole genomes of various organisms revealed a great variation in number of OR genes among species, reflecting the diversity of their living environments. For example, higher primates equipped with a well-developed vision system and dolphins that are secondarily adapted to the aquatic life have considerably smaller numbers of OR genes than most of other mammals do. OR genes are characterized by extremely frequent gene duplications and losses. The OR gene repertories are also diverse among human individuals, explaining the diversity of odor perception such as the specific anosmia. OR genes are present in all vertebrates. The number of OR genes is smaller in teleost fishes than in mammals, while the diversity is higher in the former than the latter. Because the genome of amphioxus, the most basal chordate species, harbors vertebrate-like OR genes, the origin of OR genes can be traced back to the common ancestor of the phylum Chordata.

Structure and function of the vomeronasal organ

Article

Nov 1998

Many animals use their vomeronasal organs to gain direct and specific contact with chemical cues released by congeners and in biological fluids. These cues provide information about the physiological status of the emitter and facilitate or regulate social interactions such as sexual relationships. The present review gives a short description of the discovery of the vomeronasal organ and the pivotal findings of Jacobson. The distribution of the organ and its anatomy in some vertebrates are described. The mechanisms for stimulus entry and egress are discussed, and the findings that led to the appreciation of the vomeronasal organ in mammals as a main chemosensory organ for pheromones mediating reproductive status and inducing sexual behaviour are reported. The anatomical, biochemical and functional properties of the receptor neurones are described.

The Development of the Chondrocranium in Primates

Chapter

Jan 1975

Dietrich Starck

Because of its richness of characters the adult vertebrate skull has been a principal subject of taxonomic and phylogenetic investigations for a long time. Thus, it is logical that there should also have been many attempts to include the morphology of embryonic stages of the cranium for the elucidation of phylogenetic problems.

Miller's Anatomy of the Dog

Article

Jan 1993

H. E. Evans

Structural, morphometric, and immunohistological study of the accessory olfactory bulb in the dog

Article

Jan 2005
Anat Rec

Background: The study of the morphological, morphometric, and immunohistological characteristics of the accessory olfactory bulb (AOB) in the dog is the main goal of this work. Methods: Horizontal sections of the AOB where stained by four different methods (haematoxilin/eosin, Tolivia, Nissl, and Bielchowsky). The avidin-biotin-peroxidase complex (ABC) was used, whereas the monoclonal antibodies to neuron-specific enolase, neurofilaments, glial fibrillary acidic protein, and synaptophysin were selected for the immunohistological study. A computer-assisted image analysis was employed in order to define the morphometric characteristics of de AOB. Results: The general morphology of the AOB indicates that it comprises a thick glomerular layer and a thinner internal layer containing mitral/tufted, granular, and glial cells. The mitral/tufted cells have large pale-staining nuclei with intensely staining nucleoli. There does not appear to be a clearly defined granular layer. No reactivity with antibodies to neuron-specific enolase or to neurofilaments was observed in any part of the AOB, but there was some reactivity with an antibody to glial fibrillary acidic protein and widespread reactivity with an antibody to synaptophysin. Conclusions: The stratification of the AOB is simpler and less well defined than that of the main olfactory bulb (MOB), unlike in rodents in which the structure of the AOB corresponds closely to that of the MOB. According to the scale of Frahm and Bhatnagar (1980. J. Anat., 130: 349-365) the AOB of the adult dog has an intermediate position.

Immunohistochemical study on the accessory olfactory bulb of the dog

Article

Nov 1998
Anat Rec

The accessory olfactory bulb (AOB) is a primary center of the vomeronasal system. In the dog, the position and morphology of the AOB remained vague for a long time. Recently, the morphological characteristics of the dog AOB were demonstrated by means of lectin-histochemical, histological, and immunohistochemical staining, although the distribution of each kind of neuron, especially granule cells, remains controversial in the dog AOB. In the present study, we examined the distribution of neuronal elements in the dog AOB by means of immunohistochemical and enzyme-histochemical staining. Horizontal paraffin or frozen sections of the dog AOB were immunostained with antisera against protein gene product 9.5 (PGP 9.5), brain nitric oxide synthase (NOS), glutamic acid decarboxylase (GAD), tyrosine hydroxylase (TH), substance P (SP), and vasoactive intestinal polypeptide (VIP) by avidin-biotin peroxidase complex method. In addition, frozen sections were stained enzyme-histochemically for NADPH-diaphorase. In the dog AOB, vomeronasal nerve fibers, glomeruli, and mitral/ tufted cells were PGP 9.5-immunopositive. Mitral/ tufted cells were observed in the glomerular layer (GL) and the neuronal cell layer (NCL). In the NCL, a small number of NOS-, GAD-, and SP-immunopositive and NADPH-diaphorase positive granule cells were observed. In the GL, GAD-, TH-, and VIP-immunopositive periglomerular cells were observed. In the GL and the NCL, TH-, and VIP-immunopositive short axon cells were also observed. In addition to these neurons, TH- and SP-immunopositive afferent fibers were observed in the GL and the NCL. We could distinctly demonstrate the distribution of neuronal elements in the dog AOB. Since only a small number of granule cells were present in the dog AOB, the dog AOB did not display such a well-developed GCL as observed in the other mammals. Anat. Rec. 252:393–402, 1998. © 1998 Wiley-Liss, Inc.

The dog vomeronasal organ: A review

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