The olfactory system and in particular the olfactory bulbs are extremely conserved in vertebrate evolution in terms of embryological origin, neurochemistry, connectivity and function. In all tetrapods the olfactory bulbs are pallial structures that incorporate subpallial components (Puelles et al. 2000). In particular, the olfactory neurons projecting outside the bulbs are pallial cells, like all projection neurons in the cortex, whereas the interneurons originate in the subpallium. This situation has also been confirmed in anurans, in which the mitral neurons express pallial markers (Moreno et al. 2003), while the interneurons express subpallial markers and are thought to reach the bulbs probably following a migratory process similar to that of amniotes (Smeets & González, 2000; Boyd & Delaney, 2002; Brox et al. 2003) (Fig. 2).
A major part of the amygdala is an integral component of the olfactory and vomeronasal systems of the brain (Swanson & Petrovich, 1998; Halpern & Martínez-Marcos, 2003; Moreno & González, 2006), receiving large olfactory and vomeronasal projections in all tetrapods (Swanson & Petrovich, 1998; Moreno et al. 2005). In fact, the amygdala includes the main secondary vomeronasal and olfactory centres in the brain (Swanson & Petrovich, 1998). Thus, the organization of the main sensory inputs of the amygdala (vomeronasal and olfactory) is extremely conserved, at least in tetrapods, which is striking in view of the evolutionary distance between species. However, it should be noted that in the avian brain the absence of a vomeronasal system and the important reduction of the olfactory system hamper the identification of the pallial amygdala.
The vomeronasal amygdala
In mammals, the vomeronasal information passes via the accessory olfactory bulb (AOB) to the ‘vomeronasal amygdala’, i.e. the medial (MeA) and the cortical posteromedial amygdala (CoApm) (Swanson & Petrovich, 1998). The CoApm is a cortical amygdaloid area that displays important bidirectional connections with the AOB and a minor relationship with the lateral hypothalamic area (Canteras et al. 1992; Risold et al. 1997). In addition, it projects to other telencephalic centres, primarily to other amygdaloid subdivisions (Canteras et al. 1992; Swanson & Petrovich, 1998; Martínez-García et al. 2002). The MeA receives a massive unidirectional input from the AOB and a restricted input from the main olfactory bulb (MOB; Scalia & Winans, 1975; Lehman & Winans, 1982; Canteras et al. 1995) and projects massively to the hypothalamus, especially to the ventromedial nucleus to modulate reproductive and defensive behaviours (Canteras et al. 1994, 1995; Risold et al. 1997; Choi et al. 2005). In reptiles and anurans the existence of a well-developed ‘vomeronasal amygdala’ has been reported (Scalia et al. 1991; Lanuza & Halpern, 1998; Moreno & González, 2003). By contrast, this system in birds has not been described and therefore no vomeronasal amygdaloid nuclei have been reported in the pallial amygdala (Martínez-García et al. 2006). However, the subpallial nuclus taeniae (TnA) has been traditionally considered, based on its olfactory input, to be the avian counterpart of the mammalian MeA (Reiner & Karten, 1985; Martínez-García et al. 2006). In reptiles the vomeronasal information is relayed in the AOB and reaches pallial areas (the nucleus sphericus) and a subpallial nucleus (the medial amygdala) that have been compared with the amygdaloid parts of similar origin in the vomeronasal amygdala of mammals (Lanuza et al. 1998). Unlike the case in amniotes, in anurans the MeA constitutes the only secondary vomeronasal centre in the forebrain and projects heavily to the ventral hypothalamus (Moreno & González, 2003, 2005b; Moreno et al. 2005). Thus, in all tetrapods the main secondary vomeronasal brain areas belong to the AC, but in amniotes this information reaches cortical and subpallial structures, whereas in anurans the only vomeronasal area has a subpallial origin, although also possesses migrated cells from adjacent areas, such as the ventral pallium (Moreno & González, 2006, 2007) (Fig. 3). This is in line with the notion of the total lack of cortical structures in the brain of anamniotes (Bruce & Neary, 1995; Striedter, 1997).
Figure 3. Drawings over representative coronal sections through the amygdaloid complex and a diagram (lower right) illustrating its main connections in relation to olfactory vomeronasal and multimodal information. (Diagrams of amniotes modified from Martínez-García et al. 2006.)
The olfactory/multisensorial amygdala
In their review of the organization of the AC of mammals into functional systems, Swanson & Petrovich (1998) proposed the existence of two distinct multisensorial systems: the frontotemporal amygdaloid system and a main olfactory amygdaloid system. However, in other vertebrates such a subdivision has not been recognized and it seems more appropriate to consider only one ‘multisensorial amygdala’, which certainly receives major olfactory information but also thalamic and brainstem inputs (Moreno & González, 2006).
In mammals, taken together, the olfactory/multimodal amygdaloid system consists of distinct cortical and deep amygdaloid areas. The cortical areas include the anterior cortical amygdala (CoAa), the posterolateral cortical amygdala (CoApl) and the cortex–amygdala transition area (CxA). In turn, the deep pallial areas (named, as a whole, the basolateral amygdala) include the basolateral (BL), basomedial (BM) and lateral (LA) nuclei (Swanson & Petrovich, 1998). Notably, the lateral nucleus, included in the frontotemporal functional system (Swanson & Petrovich, 1998), is the major sensory receptive area (LeDoux et al. 1990; Savander et al. 1997) and conveys sensory information to other amygdaloid nuclei for further processing (Pitkänen et al. 1995) and, thus, it is a very important component of the multimodal amygdala strongly implicated in the emotional behaviour (LeDoux, 2000). In the avian amygdala, the important reduction of the olfactory system has hindered the identification of the amygdaloid olfactory components. However, recent studies have postulated that the avian amygdala includes lateropallial olfactory cortices, the CPi, comparable with the COApl. In turn, the lateropallial structures of the avian brain deep to the CPi would be the putative homologues of the BL amygdala. In the ventral pallium, birds would posses only deep ventropallial amygdaloid nuclei, probably to be the counterparts of the BM and LA (Martínez-García et al. 2006).
Studies conducted in several species of reptiles (Martínez-García et al. 1991; Lanuza & Halpern, 1998; Lanuza et al. 1998) have identified the presence of a multimodal association area comparable with the mammalian basolateral complex. Two cortical (superficial and layered) structures in the caudal telencephalon were seen to receive a massive projection from the MOB, whereas a deep area receives multiple inputs including non-chemosensory afferents from the thalamus and telencephalic sensory centres, highly processed sensory information from the dorsal cortex, olfactory information from the (ventrocaudal) lateral cortex, and vomeronasal inputs from the nucleus sphericus. In addition, all this information is relayed to the ventromedial hypothalamus through the stria terminalis (Hoogland & Vermeulen-Vanderzee, 1995; Lanuza & Halper, 1997; Lanuza et al. 1997, 1998; Martínez-Marcos et al. 1999).
The anuran counterpart of the mammalian olfactory/multimodal amygdala, with a ventropallial origin, is the lateral amygdala (LA; Moreno & González, 2004; Moreno et al. 2004), which receives, directly or indirectly, olfactory, visual, auditory, somatosensory, vomeronasal and gustatory information. Therefore, in the anuran LA convergence of chemical (odours) and non-chemical (multisensory information) stimuli would occur (Moreno & González, 2003, 2004; Moreno et al. 2005). Convergence of projections from the vomeronasal and olfactory systems would account for an association of pheromones with odours, thus resulting in an emotional labelling of odours, conferring a predictive value to odours and allowing the animal to anticipate its reaction to the pheromone (Halpern & Martínez-Marcos, 2003). In addition, afferents from the thalamus would associate chemical (pheromones and odours) with non-chemical stimuli, as well as different non-chemical stimuli among them. All this suggests that the anuran amygdala plays an important role in the emotional labelling of any kind of novel stimuli as either attractive or aversive, in the ‘emotive memory’, thus conditioning the animal behavioural response based on its previous experiences (LeDoux, 1995, 2000).
Concerning the possible existence of a lateropallial component of the amygdala in anurans, this structure should have, in addition to the olfactory input, an important bidirectional connection with the striatum and important cholinergic and dopaminergic innervation (Martínez-García et al. 2002, 2006), both lacking in the anuran lateral pallium (Marín et al. 1998a; Moreno et al. 2004).
The multimodal integration that occurs in the AC is the basis for the acquisition of the ‘emotional memory’ and it has as its final response the ‘emotional behaviour’, i.e. responses that occur to warrant the survival of individuals and their species as, for instance, in defence against danger, in the interaction with sexual partners or in fighting with an enemy (LeDoux, 2000; Paré, 2003). It allows the association of different stimuli that are important in terms of survival, reproduction, etc., with emotions occurring at the same time. This results in an emotional labelling of odours and pheromones with important somatosensory and autonomic components (LeDoux, 1995, 1996) (Fig. 3).