0000000000242932
AUTHOR
Amparo Novejarque
Sexual pheromones and the evolution of the reward system of the brain: the chemosensory function of the amygdala.
The amygdala of all tetrapod vertebrates receives direct projections from the main and accessory olfactory bulbs, and the strong similarities in the organization of these projections suggest that they have undergone a very conservative evolution. However, current ideas about the function of the amygdala do not pay sufficient attention to its chemosensory role, but only view it as the core of the emotional brain. In this study, we propose that both roles of the amygdala are intimately linked since the amygdala is actually involved in mediating emotional responses to chemical signals. The amygdala is the only structure in the brain receiving pheromonal information directly from the accessory …
Amygdaloid projections to the ventral striatum in mice: direct and indirect chemosensory inputs to the brain reward system
Rodents constitute good models for studying the neural basis of socio-sexual behaviour. Recent findings in mice have revealed the molecular identity of the some pheromonal molecules triggering intersexual attraction. However, the neural pathways mediating this basic socio-sexual behaviour remain elusive. Since previous work indicates that the dopaminergic tegmento-striatal pathway is not involved in pheromone reward, the present report explores alternative pathways linking the vomeronasal system with the tegmento-striatal system (the limbic basal ganglia) by means of tract-tracing experiments studying direct and indirect projections from the chemosensory amygdala to the ventral striato-pall…
Distribution of CGRP-like immunoreactivity in the chick and quail brain
Calcitonin gene-related peptide (CGRP)-containing neurones have been implicated in the transmission of visceral sensory information to the cortex and in the control of arterial blood pressure in mammals. However, little is known about its function in other vertebrates. As a first step toward investigating the function of CGRP in birds, its distribution was studied in the domestic chick and quail brain by means of immunocytochemistry, by using antibodies against rat CGRP. The distribution of CGRP immunoreactivity in the chick and quail central nervous system was found to be similar. CGRP-immunoreactive (CGRPi) perikarya were not present in the telencephalon. In the diencephalon, CGRPi perika…
Vomeronasal inputs to the rodent ventral striatum.
Vertebrates sense chemical signals through the olfactory and vomeronasal systems. In squamate reptiles, which possess the largest vomeronasal system of all vertebrates, the accessory olfactory bulb projects to the nucleus sphericus, which in turn projects to a portion of the ventral striatum known as olfactostriatum. Characteristically, the olfactostriatum is innervated by neuropeptide Y, tyrosine hydroxylase and serotonin immunoreactive fibers. In this study, the possibility that a structure similar to the reptilian olfactostriatum might be present in the mammalian brain has been investigated. Injections of dextran-amines have been aimed at the posteromedial cortical amygdaloid nucleus (th…
Striato-amygdaloid transition area lesions reduce the duration of tonic immobility in the lizard Podarcis hispanica.
Neuroanatomical data suggest that the lizard striato-amygdaloid transition area is homologous with the mammalian central amygdala. In order to investigate possible functional similarities, tonic immobility was induced in adult lizards and its duration recorded. Each lizard was then randomly assigned to one of three treatments: (1) bilateral striato-amygdaloid transition area lesions, (2) bilateral dorsal cortex lesions or (3) untreated controls. Three days after trial 1, each lizard was subjected to a second trial and the tonic immobility duration recorded. The mean tonic immobility duration in lizards with striato-amygdaloid transition area lesions was significantly shorter (80.5%; p < 0.0…
Amygdalostriatal projections in reptiles: A tract-tracing study in the lizardPodarcis hispanica
Whereas the lacertilian anterior dorsal ventricular ridge contains unimodal sensory areas, its posterior part (PDVR) is an associative center that projects to the hypothalamus, thus being comparable to the amygdaloid formation. To further understand the organization of the reptilian cerebral hemispheres, we have used anterograde and retrograde tracing techniques to study the projections from the PDVR and adjoining areas (dorsolateral amygdala, DLA; deep lateral cortex, dLC; nucleus sphericus, NS) to the striatum in the lizard Podarcis hispanica. This information is complemented with a detailed description of the organization of the basal telencephalon of Podarcis. The caudal aspect of the d…
Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice
The medial amygdaloid nucleus (Me) is a key structure in the control of sociosexual behaviour in mice. It receives direct projections from the main and accessory olfactory bulbs, as well as an important hormonal input. To better understand its behavioural role, in this work we investigate the structures receiving information from the Me, by analysing the efferent projections from its anterior (MeA), posterodorsal (MePD) and posteroventral (MePV) subdivisions, using anterograde neuronal tracing with biotinylated and tetrametylrhodamine-conjugated dextranamines.The Me is strongly interconnected with the rest of the chemosensory amygdala, but shows only moderate projections to the central nucl…
Refining the dual olfactory hypothesis: Pheromone reward and odour experience
In rodents, sexual advertisement and gender recognition are mostly (if not exclusively) mediated by chemosignals. Specifically, there is ample evidence indicating that female mice are ‘innately’ attracted by male sexual pheromones that have critical non-volatile components and are detected by the vomeronasal organ. These pheromones can only get access to the vomeronasal organ by active pumping mechanisms that require close contact with the source of the stimulus (e.g. urine marks) during chemoinvestigation. We have hypothesised that male sexual pheromones are rewarding to female mice. Indeed, male-soiled bedding can be used as a reinforcer to induce conditioned place preference, provided co…
Projections from the posterolateral olfactory amygdala to the ventral striatum: neural basis for reinforcing properties of chemical stimuli
Abstract Background Vertebrates sense chemical stimuli through the olfactory receptor neurons whose axons project to the main olfactory bulb. The main projections of the olfactory bulb are directed to the olfactory cortex and olfactory amygdala (the anterior and posterolateral cortical amygdalae). The posterolateral cortical amygdaloid nucleus mainly projects to other amygdaloid nuclei; other seemingly minor outputs are directed to the ventral striatum, in particular to the olfactory tubercle and the islands of Calleja. Results Although the olfactory projections have been previously described in the literature, injection of dextran-amines into the rat main olfactory bulb was performed with …
Attraction to sexual pheromones and associated odorants in female mice involves activation of the reward system and basolateral amygdala
Adult female mice are innately attracted to non-volatile pheromones contained in male-soiled bedding. In contrast, male-derived volatiles become attractive if associated with non-volatile attractive pheromones, which act as unconditioned stimulus in a case of Pavlovian associative learning. In this work, we study the chemoinvestigatory behaviour of female mice towards volatile and non-volatile chemicals contained in male-soiled bedding, in combination with the analysis of c-fos expression induced by such a behaviour to clarify: (i) which chemosensory systems are involved in the detection of the primary attractive non-volatile pheromone and of the secondarily attractive volatiles; (ii) where…
Evolution of the Amygdala in Vertebrates
The main aim of this article is to identify the homologues of the different components of the mammalian amygdala in the cerebral hemispheres of non-mammals using, primarily, a topological/embryological perspective. Thus, we first consider two main divisions of the amygdala of mammals, namely the pallial and subpallial (striatopallidal) amygdala. The pallial amygdala includes derivatives of both the lateral and ventral embryonic pallium that in the adult conform layered, superficial areas usually called cortical amygdala, and deep nuclei that conform the basolateral division of the amygdala plus the amygdalohippocampal area (AHA). The components of the subpallial amygdala are usually grouped…
Attractive properties of sexual pheromones in mice
Abstract It is generally assumed that chemical signals (sexual pheromones) constitute the primary stimulus for sexual attraction in many mammals. However, it is unclear whether these pheromones are volatile or nonvolatile and which sensory systems are involved in their detection (vomeronasal and/or olfactory). Moreover, it has been demonstrated that experience influences the behavioral response to sexual pheromones and the sensory systems implicated. In order to clarify this issue, the attractive properties of volatile and nonvolatile components of the male-soiled bedding have been analyzed in female mice that had no previous experience with adult male-derived chemical signals (chemically n…
Distribution of calcitonin gene-related peptide-like immunoreactivity in the brain of the lizardPodarcis hispanica
The present work studies the distribution of calcitonin gene-related peptide-immunoreactive (CGRP-li) neurons and fibers in the brain of a reptile, the lizard Podarcis hispanica. CGRP-li perikarya were not present in the telencephalon. In the thalamus, CGRP-li perikarya were restricted to the posteromedial and posterolateral nuclei. In the hypothalamus, CGRP-li cells were found mainly in the supramammillary and mammillary nuclei. In the midbrain and brainstem, CGRP-li cells appeared in the ventral tegmental area, the parabrachial nucleus, and the motor nuclei of the III-VII, IX, X, and XII cranial nerves. Motoneurons of the ventral horn of the spinal cord were also immunoreactive for CGRP. …
Piriform Cortex and Amygdala
Publisher Summary A ventral view of the cerebral hemispheres of mammals shows an array of structures ultimately connected with the olfactory bulbs through the olfactory tracts. This is the basis for the old concept of rhinencephalon, a series of neural centers in the cerebral hemispheres, located ventral to the rhinal fissure, for which an olfactory role was assumed. Although mice lack a conspicuous rhinal fissure, their “rhinencephalon” is well developed. The concept of the rhinencephalon is difficult to sustain nowadays, as it includes neural centers of diverse origin, organization and nature. The rhinencephalon comprises several allocortical areas that constitute the olfactory cortex, de…
Two interconnected functional systems in the amygdala of amniote vertebrates.
The amygdala shows ventropallial and lateropallial derivatives that can be compared among vertebrates according to their topological position, either superficial (cortical amygdala) or deep (basolateral amygdala and amygdalo-hippocampal area), connections and histochemical features. On the other hand, the subpallial amygdala, also called extended amygdala, is composed of medial and central divisions. In mammals, both divisions consist of an intra-amygdaloid portion and a part of the bed nucleus of the stria terminalis. In non-mammals, the intratelencephalic trajectory of the stria terminalis is short and both poles of the extended amygdala are close together. Like its mammalian counterpart,…