The sea lamprey has a primordial accessory olfactory system
© Chang et al.; licensee BioMed Central Ltd. 2013
Received: 24 October 2012
Accepted: 1 August 2013
Published: 17 August 2013
A dual olfactory system, represented by two anatomically distinct but spatially proximate chemosensory epithelia that project to separate areas of the forebrain, is known in several classes of tetrapods. Lungfish are the earliest evolving vertebrates known to have this dual system, comprising a main olfactory and a vomeronasal system (VNO). Lampreys, a group of jawless vertebrates, have a single nasal capsule containing two anatomically distinct epithelia, the main (MOE) and the accessory olfactory epithelia (AOE). We speculated that lamprey AOE projects to specific telencephalic regions as a precursor to the tetrapod vomeronasal system.
To test this hypothesis, we characterized the neural circuits and molecular profiles of the accessory olfactory epithelium in the sea lamprey (Petromyzon marinus). Neural tract-tracing revealed direct and reciprocal connections with the dorsomedial telencephalic neuropil (DTN) which in turn projects directly to the dorsal pallium and the rostral hypothalamus. High-throughput sequencing demonstrated that the main and the accessory olfactory epithelia have virtually identical profiles of expressed genes. Real time quantitative PCR confirmed expression of representatives of all 3 chemoreceptor gene families identified in the sea lamprey genome.
Anatomical and molecular evidence shows that the sea lamprey has a primordial accessory olfactory system that may serve a chemosensory function.
A dual olfactory system is thought to be unique to tetrapods. The two distinct sensory epithelia of this system, the main and the vomeronasal olfactory epithelia, heterogeneously express families of chemoreceptor genes, with some overlap . These epithelia have anatomically distinct projections to different parts of the forebrain. These dichotomous molecular and anatomical profiles led to the hypothesis that the VNO is specialized to detect pheromones [2–6] whereas other research has suggested overlapping functions for the main olfactory system and VNO [7–11]. Amphibians were thought to be the earliest evolving animals with a complete VNO [12, 13], however recent work has shown that lungfish have a vomeronasal system . It should be noted that although they do not possess a canonically recognized VNO system, molecular components of a VNO system exist in elephant shark  and teleost fish [16, 17]. Therefore, the vomeronasal system is presumed to have evolved after the main olfactory system in the vertebrate lineage .
Although a distinct vomeronasal system has not been identified in fish [19, 20], a recent study has found a vomeronasal system in a sister group to tetrapods, the lungfish [14, 21]. Moreover, molecular components of a vomeronasal system have been identified in a basal vertebrate, the sea lamprey (Petromyzon marinus) [15, 22]. Although fish have only one recognized olfactory epithelium, Dulka (1993)  suggested a functional division of the primary olfactory pathway in goldfish that may be analagous to the output neurons from the MOE and VOE in tetrapods. Interestingly, the sea lamprey, like tetrapods, has two separate and distinct olfactory epithelia. The AOE was discovered by in 1887 by Scott , but its function had eluded description. In 2009, Ren et al. showed that lamprey AOE is lined with a simple cuboidal ciliated epithelium and projects to the medial olfactory bulb . In addition, another structure with elusive function in the sea lamprey brain, the dorsomedial telencephalic neuropil (DTN) , is located in a similar position to the tetrapod AOB. The sea lamprey DTN is dorsomedially situated, immediately caudal to the olfactory bulb, receives input from the olfactory bulb and projects to the hypothalamus [26, 27].
We hypothesized that the AOE coupled with the DTN comprise a primitive form of the vomeronasal system in the vertebrate lineage. We reasoned that if the AOE was chemosensory, it should express at least some of the chemoreceptor (CR) genes encoded in the lamprey genome . We further reasoned that the AOE projects to a separate telencephalic region, possibly the DTN. Here we present evidence that AOE expresses all known families of lamprey CR genes and projects to the DTN. We conclude that the AOE-DTN-hypothalamic pathway in lamprey is a partial segregation of the olfactory pathway, which suggests that the components of a vomeronasal system may have been in place in this basal vertebrate.
AOE projects to the DTN and other telencephalic areas
DTN connects to the AOE and the hypothalamus
MOE and AOE have virtually identical gene expression profiles
Expression of chemoreceptor genes is sexually dimorphic
Comparison of main and accessory olfactory system components in rodent, frog, zebrafish and lamprey *note – teleost fish do not have a recognized vomeronasal organ nor an accessory olfactory bulb
Pseudostratified Ciliated Columnar 
Pseudostratified Ciliated Columnar and Microvillous 
Pseudostratified Ciliated Columnar 
OR, TAAR 
OR, TAAR, V1R 
OR, V1R, V2R 
To MOB 
To MOB and DTN
To MOB 
To AOB 
To MOB and DTN
Mitral cells 
Mitral cells 
Yes, loosely defined 
Yes, loosely defined 
To olfactory cortex 
To olfactory amygdala 
To habenula/limbic system output pathway 
To amygdala (limbic area) and hypothalamus 
To piriform cortex 
To pallial areas and hypothalamus
Our neural tract-tracing results show direct projections from the AOE to the DTN. Injections of biocytin to the AOE revealed connections to the medial olfactory bulb similar to the results of Derjean et al., 2010 , the pallial areas of the telencephalon and the DTN. Labeling of cells in the MOE after injection to the AOE was unexpected as the MOE and AOE are anatomically separate, however, this may be due to piercing of olfactory nerve fascicles during injection, which are in close proximity to the AOE vesicles [23, 24]. Alternatively, some AOE vesicles have been observed to be connected to the MOE by ducts at the ventrolateral aspect of the nasal capsule, though this assertion could be an artifact of the plane of sectioning . Moreover, dye could have been transported anterogradely to the MOE from the AOE via the olfactory nerve axons that are in close proximity to the AOE. Injections of biocytin to the DTN revealed reciprocal connections with the AOE and the MOE. While the primary projections of the AOE to the DTN in lamprey are very similar to the primary projections of the VNO to the AOB in tetrapods, a difference is that in lamprey, the AOE has direct projections to the MOB . In tetrapods, the MOE and VNO have segregated outputs to the MOB and AOB, respectively . Therefore, the lamprey pathway is less segregated than those in adult tetrapods.
Interestingly, the lamprey system shares similarities with the system in developing tetrapods. Previous studies have already demonstrated anatomical evidence that MOE and AOE both project to the medial olfactory bulb and functional evidence that the medial olfactory bulb activates locomotor brain regions . Our work builds on these findings via anterograde and retrograde tracings from the AOE and the DTN of lamprey to show partial segregation at the peripheral level. The vomeronasal system recently discovered in lungfish is also a less segregated system , as molecular markers for a VNO are expressed in the MOE. The question of the ancestral vertebrate condition with respect to olfactory projections (mixed or segregated outputs) requires further investigations.
Another similarity seen between the lamprey and tetrapod pathways is in their projections to higher centers. The lamprey DTN has direct projections to a putative amygdala homolog as well as the hypothalamus and thalamus. Dye injections to the DTN revealed labeling in the dorsal pallium, the hypothalamus and the thalamus. This confirms previous discoveries by Northcutt and Puzdrowski  who demonstrated DTN connectivity to the hypothalamus. Polenova and Vesselkin  also demonstrated connectivity of the DTN to the pallial areas of the telencephalon. Our work provides further information on the telencephalic pathways with respect to the main and accessory olfactory epithelia. The bi-directional connectivity between the medial pallium and striatum has been demonstrated in silver lamprey by Northcutt and Wicht . Furthermore, the pallial areas are likely homologs of the tetrapod amygdala because of GABA-ergic projections from the medial pallium to the striatum . Consequently, the pattern of projection of AOE to DTN to pallial areas and hypothalamus likely parallels the tetrapod vomeronasal pathway.
The pathway seen in our study flows from the AOE to the DTN to the pallial areas and the hypothalamus. In tetrapods, the MOE and VNO have anatomically distinct primary projections. The MOE projects primarily to the main olfactory bulb and the VNO projects to the accessory olfactory bulb. In mice, there is a further segregation of output from the VNO. Specifically, sensory neurons in the anterior and posterior VNO express V1R and V2R receptors, respectively, and project to the anterior and posterior AOB, repeating the anatomical division seen at the periphery [1, 43]. Output neurons from the AOB in turn project to limbic areas of the brain including the amygdala and also to the hypothalamus and thalamus . From the AOB, there are two distinct populations of output neurons that project to the rostral and caudal regions of the amygdala, which in turn project to rostral and caudal regions of the hypothalamus which mirrors the segregated inputs from the vomeronasal organ [57, 62]. In sea lamprey, there is a convergence of output from the MOE and the AOE. Both the MOE and AOE have connections to the OB and the DTN, and so there is not a clear division of output from the MOE and AOE to their respective olfactory integration centers.
The sea lamprey AOE has cellular and molecular characteristics of an olfactory sensory epithelium. Since its discovery in Petromyzon by Scott in 1887 , AOE has been suggested to function as Jacobsen’s organ , nasal sac rudiments , part of the pituitary  and Bowman’s glands . Recently, Ren et al.  demonstrated retrograde connectivity from the medial olfactory bulb to the AOE and concluded that the AOE and its projections are a distinct division within the olfactory pathway. Our data complements this conclusion by demonstrating anterograde connectivity from the AOE to the medial OB. In addition, we have shown reciprocal connectivity between the AOE and the DTN. Morphologically, the retrogradely labeled sensory neurons from both MOE and AOE in lamprey are ciliated. Molecular level analysis revealed further evidence that the lamprey AOE is a sensory epithelium. As expected, the overall gene categories expressed in MOE and AOE are virtually identical, furthering the case of the AOE as a chemosensory structure. Expression of chemoreceptor genes from all three of the families of chemoreceptor genes (ORs, TAARs and V1Rs) identified in the lamprey genome was confirmed . In tetrapods, the VNO expresses V1Rs, V2Rs and ORs [4, 8, 10, 66, 67] while the MOE expresses ORs, TAARs and V1Rs . While the MOE and VNO are anatomically separate in tetrapods, there is overlap with respect to chemoreceptor gene expression, secondary projection pathways and neural connectivity [8, 11, 40, 68]. The similarities in chemoreceptor gene families expressed in lamprey MOE and AOE may be explained by the status of the lamprey as a basal vertebrate [69, 70]. Moreover, during embryological development, the MOE and AOE of vertebrates both arise from the olfactory placode [71, 72]. At the neural circuit level, as well as the molecular level, it appears that the lamprey dual system is not as segregated as the tetrapod dual olfactory system.
Chemoreceptor genes were found to have a sexually dimorphic pattern of expression in lamprey MOE and AOE. In vertebrates, sexually dimorphic gene expression is usually linked to sex determination. For example, in rainbow trout, sox9a1 is expressed in male gonads and cyp19a1 is expressed in female gonads . In the sea lamprey, the gene expression pattern observed in this study may be related to its sexually dimorphic behavior. While both males and females can detect the pheromone 3-keto petromyzonol sulfate (3 kPZS), only females show a strong locomotor response . However, this speculation requires further examinations.
Anatomical and molecular evidence shows that the sea lamprey has a primordial accessory olfactory system that may serve a chemosensory function.
Migrating adults (n = 93) were obtained from the St. Mary’s River in Sault Ste. Marie, Michigan from the Hammond Bay Biological Station with mean length ± s.d. (48.3 cm ± 0.4 cm) and mean weight ± s.d. (237.4 g ± 5.0 g). Animals were handled according to guidelines provided by the Institutional Animal Care and Use Committee at Michigan State University.
Neural tract tracing
Animals were euthanized in tricaine methanesulfonate (MS-222, 100 mg/L, Sigma). The olfactory epithelium and brain were rapidly exposed by dorsal dissection, removing any surrounding muscle or cartilage. The tissue was rinsed in aerated cold Ringer’s solution (pH 7.4) with the following composition: 130 mM NaCl, 2.1 mM KCl, 2.6 mM CaCl2, 1.8 mM MgCl2, 4 mM HEPES, 4 mM dextrose and 1 mM NaHCO3. Glass capillaries with a diameter of 50 μm were filled with 2 μl of 2% biocytin [in 0.1M phosphate buffer saline (PBS), pH7.2] and inserted into either multiple accessory olfactory vesicles or the DTN (see Additional file 2), and the tracer was applied to the lesion. Tissue was rinsed and incubated in lamprey Ringer’s for 10 minutes before being placed in a flow-through chamber held at 7°C. The tissue was continuously perfused with cold aerated Ringer’s solution during the entire incubation period. After 4 hours, the tissue was fixed in 4% paraformaldehyde in 0.1 M PBS (pH 7.4). Tissue was then immersed in Sakura Tissue-Tek O.C.T. compound (VWR) and frozen with a combination of liquid nitrogen and dry ice. Thin sections (20 μm) were collected on Superfrost Plus slides (VWR) and stored at −20°C. Slides were washed in 0.1 M PBS (pH 7.4) and biocytin signal was visualized by addition of Alexa 488 Streptavidin (1:100, Invitrogen). Slides were examined on an upright Zeiss Axioskop 2, equipped with fluorescence and a CCD camera. Images were captured using Axiovision software (Zeiss). Samples with clear leakage from the intended injection site were rejected.
Laser Capture Microdissection (LCM) and mRNA-Seq preparation
Olfactory organs from mature males and females were dissected out, embedded in O.C.T. compound and frozen with a combination of dry ice and liquid nitrogen. Seven-μm frontal sections were collected on non-charged glass slides (VWR) and stored at −80°C. Slides were then passed through an ascending alcohol series and rinsed with xylene to dehydrate the tissue and remove the alcohol. Slides were then viewed under an inverted Nikon Eclipse microscope outfitted with the Arcturus Pixcell II/e Laser Capture Microdissection System and Arcview software (Arcturus). The MOE and the AOE are not distinguishable with the naked eye, but are easily distinguished when viewed under a microscope (data not shown). Cells from the MOE and AOE were lifted under the following conditions (duration: 20.0 ms, repeat: 0.4 s, spot size: 7.5 μm, power: 100 mW). Because of the anatomical separation of the MOE and AOE, we were absolutely sure that we were lifting cells from the appropriate epithelium. RNA was extracted using TRIZOL reagent (Invitrogen) and stored at −80°C. Quality of samples was verified using an Agilent 2100 Bioanalyzer before submission for high-throughput sequencing.
MOE and AOE RNA samples were sequenced at the Michigan State University Research Technology Support Facility, using the Illumina DGE kit according to manufacturer’s instructions. 64,141,260 reads were obtained and 58% (37,785,187) passed a quality filter. The filtered reads were aligned, using Bowtie software , to our assembly of the sea lamprey transcriptome to obtain transcript expression count information for each lane, which were then quantile-normalized. The transcriptome assembly was, in turn, aligned to mouse RefSeq protein sequences, providing a putative orthology with which mouse protein annotations were assigned to corresponding lamprey transcripts, and these annotations were combined with transcript expression counts to infer expression information for putative lamprey-mouse orthologs. This information was used to infer putative ortholog differential expression between MOE and AOE. Using inferred expression ratios, significantly enriched or depleted gene ontology categories were identified, with the help of GoMiner software .
SYBR green real-time quantitative PCR
Primers used for SYBR green qPCR
We thank the staff at USGS Hammond Bay Biological Station (Millersburg, MI). We also thank Dr. Rejean Dubuc and Mr. Francois Auclair for providing images for Figure one. This work was supported by US NIGMS grant 5R24GM83982 (to WL), NSF grant IOB0517491 (to WL), Great Lakes Fishery Commission Grants (to WL), and USDA NIFA AFRI Competitive Grant no. 2010-65205-20361 (to CTB).
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