Efferent and afferent connections of the olfactory bulb and prepiriform cortex in the pigeon (Columba livia)

Although olfaction in birds is known to be involved in a variety of behaviors, there is comparatively little detailed information on the olfactory brain. In the pigeon brain, the olfactory bulb (OB) is known to project to the prepiriform cortex (CPP), piriform cortex (CPi), and dorsolateral corticoid area (CDL), which together are called the olfactory pallium, but centrifugal pathways to the OB have not been fully explored. Fiber connections of CPi and CDL have been reported, but those of other olfactory pallial nuclei remain unknown. The present study examines the fiber connections of OB and CPP in pigeons to provide a more detailed picture of their connections using tract‐tracing methods. When anterograde and retrograde tracers were injected in OB, projections to a more extensive olfactory pallium were revealed, including the anterior olfactory nucleus, CPP, densocellular part of the hyperpallium, tenia tecta, hippocampal continuation, CPi, and CDL. OB projected commissural fibers to the contralateral OB but did not receive afferents from the contralateral olfactory pallium. When tracers were injected in CPP, reciprocal ipsilateral connections with OB and nuclei of the olfactory pallium were observed, and CPP projected to the caudolateral nidopallium and the limbic system, including the hippocampal formation, septum, lateral hypothalamic nucleus, and lateral mammillary nucleus. These results show that the connections of OB have a wider distribution throughout the olfactory pallium than previously thought and that CPP provides a centrifugal projection to the OB and acts as a relay station to the limbic system. J. Comp. Neurol. 522:1728–1752, 2014. © 2013 Wiley Periodicals, Inc.     

Fiber connections of the compact division of the posterior pallial amygdala and lateral part of the bed nucleus of the stria terminalis in the pigeon (Columba livia)

The compact division of the posterior pallial amygdala (PoAc) and lateral part of the bed nucleus of the stria terminalis (BSTL) are components of the limbic system in the pigeon brain. In this study, we examined the position and fiber connections of these two nuclei by using Nissl staining and tract-tracing methods. PoAc occupies a central division in the posterior pallial amygdala. BSTL faces the ventral horn of the lateral ventricle and extends between A 7.25 and A 10.50. PoAc and BSTL connect bidirectionally by the stria terminalis. PoAc connects reciprocally with two nuclear groups in the cerebrum: 1) a continuum consisting of the caudoventral nidopallium, lateral part of the caudoventral nidopallium (NCVl), subnidopallium beneath NCVl, and piriform cortex and 2) rostral areas of the hemisphere, including the frontolateral and frontomedial nidopallium and the densocellular part of the hyperpallium. Extratelencephalic projections of PoAc terminate in the dorsomedial thalamic nuclei and reach the lateral hypothalamic area via the hypothalamic part of the occipito-mesencephalic tract. BSTL also connects reciprocally with two main regions: 1) the same continuum as for PoAc projections, except the piriform cortex and 2) rostral areas of the hemisphere, including the olfactory tubercle and nucleus accumbens. Extratelencephalic reciprocal connections are with the substantia nigra, nucleus subceruleus dorsalis, parabrachial nucleus, locus coeruleus, and nucleus of the solitary tract. The dorsomedial subdivision of the hippocampal formation projects massively to PoAc and BSTL. These findings indicate that PoAc and BSTL are important components of an interconnected neural circuit involving widespread regions of the neuraxis and mediating limbic-visceral functions.     

Intratelencephalic connections of the hippocampus in pigeons (Columba livia)

Behavioral experiments using ablation of the hippocampus are increasingly being used to address the hypothesis that the avian hippocampus plays a role in memory, as in mammals. However, the morphological basis of the avian hippocampus has been poorly understood. In the present study, the afferent and efferent connections of the hippocampus in the pigeon telencephalon were defined by injections, at various rostrocaudal sites, of neuronal tracers mainly into the triangular part located between its V-shaped layer of densely packed neurons. The major results obtained in the present study were as follows. 1) A topographical organization of the commissural projections was confirmed. These projections had two courses that projected to the contralateral side, one traveling through the fiber wall of the ventromedial telencephalon, which was the main path from neurons in the caudal hippocampus, and the other running down through the septohippocampal junction, which was the main path from neurons in the middle to rostral hippocampus. Both courses passed through the pallial commissure. 2) The hippocampus projected bilaterally to the septum, parahippocampal area (APH), and dorsolateral cortical area (CDL). These projections were also distributed topographically, with contralateral efferents crossing through the pallial commissure. 3) The hippocampus had ipsilateral reciprocal connections with APH, CDL, and the dorsal hyperstriatum. Septal afferents to the ipsilateral hippocampus were very small. 4) Intrinsic connections were found between the triangular part of the hippocampus and the lateral limb of the V-shaped layer of neurons. 5) The hippocampus projected ipsilaterally to the ventral basal ganglia and the fasciculus diagonalis Brocae. In sum, these connections of the hippocampus may form a neuronal circuit for the processing of spatial memory in pigeons.     

Calcium-binding proteins, neuronal nitric oxide synthase, and GABA help to distinguish different pallial areas in the developing and adult chicken. I. Hippocampal formation and hyperpallium

To better understand the formation and adult organization of the avian pallium, we studied the expression patterns of gamma-aminobutyric acid (GABA), calbindin (CB), calretinin (CR), and neuronal nitric oxide synthase (nNOS) in the hippocampal formation and hyperpallium of developing and adult chicks. Each marker showed a specific spatiotemporal expression pattern and was expressed in a region (area)-specific but dynamic manner during development. The combinatorial expression of these markers was very useful for identifying and following the development of subdivisions of the chicken hippocampal formation and hyperpallium. In the hyperpallium, three separate radially arranged subdivisions were present since early development showing distinct expression patterns: the apical hyperpallium (CB-rich); the intercalated hyperpallium (nNOS-rich, CB-poor); the dorsal hyperpallium (nNOS-poor, CB-moderate). Furthermore, a novel division was identified (CB-rich, CR-rich), interposed between hyper- and mesopallium and related to the lamina separating both, termed laminar pallial nucleus. This gave rise at its surface to part of the lateral hyperpallium. Later in development, the interstitial nucleus of the apical hyperpallium became visible as a partition of the apical hyperpallium. In the hippocampal formation, at least five radial divisions were observed, and these were compared with the divisions proposed recently in adult pigeons. Of note, the corticoid dorsolateral area (sometimes referred as caudolateral part of the parahippocampal area) contained CB immunoreactivity patches coinciding with Nissl-stained cell aggregates, partially resembling the patches described in the mammalian entorhinal cortex. Each neurochemical marker was present in specific neuronal subpopulations and axonal networks, providing insights into the functional maturation of the chicken pallium.     

Afferent and efferent projections of the mesopallium in the pigeon (Columba livia)

The mesopallium is a thick cell plate occupying a substantial portion of the avian dorsal pallium, but its hodology is incompletely known. In pigeons we examined fiber connections of the frontodorsal (MFD) and frontoventral mesopallium (MFV), the ventrolateral mesopallium (MVL), the lateral (MIVl) and medial (MIVm) parts of the intermediate ventral mesopallium, and the caudal mesopallium (MC). MFV, MIVl, and MC connect reciprocally with secondary centers of the trigeminal, tectofugal, and auditory systems, respectively. MVL forms reciprocal connections with both the entopallial core and belt. MFV, MIVl, MVL, and MC receive thalamic inputs different from those of primary sensory pallial regions and have reciprocal connections with the caudolateral nidopallium (NCL) or arcopallium. MIVm has a strong reciprocal connection with the intermediate medial nidopallium. It receives afferents from the visual Wulst, rostral MC, posterior dorsointermediate thalamic nucleus, and caudal part of the posterior dorsolateral thalamic nucleus, is connected reciprocally with the arcopallium, and projects to NCL. MFD has reciprocal connections with the medial frontal nidopallium, arcopallium, posterior pallial amygdala, dorsolateral corticoid area, and projects to the medial part of medial striatum and hypothalamus. These results indicate that six subdivisions of the mesopallium have strong connections with corresponding portions of the nidopallium. In particular, the sensory mesopallial components of MFV, MIVl, MVL, and MC form parallel pathways to the one-way sensory streams in the nidopallium and make either feedback or feedforward circuits to the secondary centers of the nidopallium.     

Telencephalic connections in the pacific hagfish (Eptatretus stouti), with special reference to the thalamopallial system

The pallium of hagfishes (myxinoids) is unique: It consists of a superficial “cortical” mantle of gray matter which is subdivided into several layers and fields, but it is not clear whether or how these subdivisions can be compared to those of other craniates, i.e., lampreys and gnathostomes. The pallium of hagfishes receives extensive secondary olfactory projections (Wicht and Northcutt [1993] J. Comp. Neurol. 337:529–542), but there are no experimental data on its nonolfactory connections. We therefore investigated the pallial and dorsal thalamic connections of the Pacific hagfish. Injections of tracers into the pallium labeled many cells bilaterally in the olfactory bulbs. Other pallial afferents arise from the contralateral pallium, the dorsal thalamic nuclei, the preoptic region, and the posterior tubercular nuclei. Descending pallial efferents reach the preoptic region, the dorsal thalamus, and the mesencephalic tectum but not the motor or premotor centers of the brainstem. Injections of tracers into the dorsal thalamus confirmed the presence of reciprocal thalamopallial connections. In addition, these injections revealed that there is no “preferred” pallial target for the ascending thalamic fibers; instead, ascending thalamic and secondary olfactory projections overlap throughout the pallium. The mesencephalic tectum and tegmentum, which receive afferents from a variety of sensory sources, are interconnected with the dorsal thalamus; thus, ascending nonolfactory sensory information may reach myxinoid pallia via a tectal-thalamic-telencephalic route. A comparative analysis of pallial organization reveals that the subdivisions of the pallium in gnathostomes (i.e., medial, dorsal, and lateral pallia) cannot be recognized with certainty in hagfishes. J. Comp. Neurol. 395:245–260, 1998. © 1998 Wiley-Liss, Inc.     

Afferent connections of septal nuclei of the domestic chick (Gallus domesticus): a retrograde pathway tracing study

The afferents to the septum of the domestic chicken were studied using retrograde tracers, rhodamine conjugated latex bead or Fast Blue, placed in different septal subregions. The results were verified by anterograde tracer injections deposited to selected areas. The main telencephalic afferents to the septum arise ipsilaterally from the hippocampal formation, dorsolateral corticoid area, piriform cortex, amygdaloid pallium, and the ventral pallidum. Contralateral afferents originate from the lateral septum and the amygdaloid pallium. A massive bilateral projection arises from the lateral hypothalamus. Other hypothalamic afferents arise from the periventricular, paraventricular and anterior medial nuclei, and the premammillary and mammillary areas. The dorsal thalamic nuclei (dorsal medial anterior and posterior) and the reticular dorsal nuclei also contribute septal afferents. Brainstem afferents arise bilaterally from the ventral tegmental area, substantia nigra, central gray, A8, locus coeruleus, ventral subcoeruleus nucleus, and raphe nuclei. The main terminal fields for septal afferents lie in the lateral septal nucleus and the belt of medial septal nucleus. The core of the latter is invaded mainly by fibers from the brainstem, presumably belonging to the ascending activating system. The septal afferents of the chicken are largely similar to those of other avian and nonavian species. The most prominent differences with previous pigeon data were found in the subregional selectivity of the hippocampal formation, dorsolateral corticoid area, mammillary nuclei, some dorsal thalamic nuclei, substantia nigra, and subcoeruleus nuclei in their projections to defined septal nuclei.     

Expression of regulatory genes in the embryonic brain of a lizard and implications for understanding pallial organization and evolution

The comparison of gene expression patterns in the embryonic brain of mouse and chicken is being essential for understanding pallial organization. However, the scarcity of gene expression data in reptiles, crucial for understanding evolution, makes it difficult to identify homologues of pallial divisions in different amniotes. We cloned and analyzed the expression of the genes Emx1, Lhx2, Lhx9, and Tbr1 in the embryonic telencephalon of the lacertid lizard Psammodromus algirus. The comparative expression patterns of these genes, critical for pallial development, are better understood when using a recently proposed six‐part model of pallial divisions. The lizard medial pallium, expressing all genes, includes the medial and dorsomedial cortices, and the majority of the dorsal cortex, except the region of the lateral cortical superposition. The latter is rich in Lhx9 expression, being excluded as a candidate of dorsal or lateral pallia, and may belong to a distinct dorsolateral pallium, which extends from rostral to caudal levels. Thus, the neocortex homolog cannot be found in the classical reptilian dorsal cortex, but perhaps in a small Emx1‐expressing/Lhx9‐negative area at the front of the telencephalon, resembling the avian hyperpallium. The ventral pallium, expressing Lhx9, but not Emx1, gives rise to the dorsal ventricular ridge and appears comparable to the avian nidopallium. We also identified a distinct ventrocaudal pallial sector comparable to the avian arcopallium and to part of the mammalian pallial amygdala. These data open new venues for understanding the organization and evolution of the pallium.     

Distribution of the limbic system-associated membrane protein (LAMP) in pigeon forebrain and midbrain

The limbic system-associated membrane protein (LAMP) is an adhesion molecule involved in specifying regional identity during development, and it is enriched in the neuropil of limbic brain regions in mammals but also found in some somatic structures. Although originally identified in rat, LAMP is present in diverse species, including avians. In this study, we used immunolabeling with a monoclonal antibody against rat LAMP to examine the distribution of LAMP in pigeon forebrain and midbrain. LAMP immunolabeling was prominent in many telencephalic regions previously noted as limbic in birds. These regions include the hippocampal complex, the medial nidopallium, and the ventromedial arcopallium. Subpallial targets of these pallial regions were also enriched in LAMP, such as the medial-most medial striatum. Whereas some telencephalic areas that have not been regarded as limbic were also LAMP-rich (e.g., the hyperpallium intercalatum and densocellulare of the Wulst, the mesopallium, and the intrapeduncular nucleus), most nonlimbic telencephalic areas were LAMP-poor (e.g., field L, the lateral nidopallium, and somatic basal ganglia). Similarly, in the diencephalon and midbrain, prominent LAMP labeling was observed in such limbic areas as the dorsomedial thalamus, the hypothalamus, the ventral tegmental area, and the central midbrain gray, as well as in a few nonlimbic areas such as nucleus rotundus, the shell of the nucleus pretectalis, the superficial tectum, and the parvocellular isthmic nucleus. Thus, as in mammals, LAMP in birds appears to be enriched in most known forebrain and midbrain limbic structures but is present as well in some somatic structures.     

Efferent connections of the dorsomedial thalamic nuclei of the domestic chick (Gallus domesticus)

Small iontophoretic injections of the anterograde tracer Phaseolus vulgaris leucoagglutinin were placed in the thalamic anterior dorsomedial nucleus (DMA) of domestic chicks. The projections of the DMA covered the rostrobasal forebrain, ventral paleostriatum, nucleus accumbens, septal nuclei, Wulst, hyperstriatum ventrale, neostriatal areas, archistriatal subdivisions, dorsolateral corticoid area, numerous hypothalamic nuclei, and dorsal thalamic nuclei. The rostral DMA projects preferentially on the hypothalamus, whereas the caudal part is connected mainly to the dorsal thalamus. The DMA is also connected to the periaqueductal gray, deep tectum opticum, intercollicular nucleus, ventral tegmental area, substantia nigra, locus coeruleus, dorsal lateral mesencephalic nucleus, lateral reticular formation, nucleus papillioformis, and vestibular and cranial nerve nuclei. This pattern of connectivity is likely to reflect an important role of the avian DMA in the regulation of attention and arousal, memory formation, fear responses, affective components of pain, and hormonally mediated behaviors.     

Thalamo-telencephalic connections: new insights on the cortical organization in reptiles

Tracer injections into the dorsal tier of the lacertilian dorsal thalamus revealed an extensive innervation of the cerebral cortex. The medial cortex, the dorsomedial cortex, and the medial part of the dorsal cortex received a bilateral projection, whereas the lateral part of dorsal cortex and the dorsal part of the lateral cortex received only an ipsilateral thalamic projection. Thalamocortical fibers were found superficially in all cortical regions, but in the dorsal part of the lateral cortex, varicose axons within the cellular layer were also observed. The bilateral thalamocortical projection originates from a cell population located throughout the dorsolateral anterior nucleus, whereas the ipsilateral input originates mainly from a rostral neuronal subpopulation of the nucleus. This feature suggests that the dorsolateral anterior nucleus consists of various parts with different projections. The dorsal subdivision of the lateral cortex displayed hodological and topological (radial glia processes) features of a dorsal pallium derivative. After tracer injections into the dorsal cortex of lizards, we found long descending projections that reached the striatum, the diencephalic basal plate, and the mesencephalic tegmentum, which suggests that it may represent a sensorimotor cortex.     

Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions

The organization of the pigeon hippocampal formation was examined by tract tracing by using biotinylated dextran amine (BDA) and cholera toxin B subunit (CTB) and by injections of kainic acid to produce excitotoxic lesions. The hippocampal formation was divided into seven subdivisions based on Nissl staining and intrinsic and septal connections: dorsomedial (DM), dorsolateral (DL), triangular (Tr), V-shaped layer, magnocellular (Ma), parvocellular, and cell-poor regions. DL was composed of dorsal and ventral portions and sent associational fibers to DM, the V-shaped layer, and Tr. DL had strong reciprocal connections with the densocellular part of the hyperpallium (HD) and projected to the dorsolateral corticoid area. DM had reciprocal fiber connections with the V-shaped layer, Ma, and DL as well as with several subdivisions of the arcopallium. DL and DM, but not the V-shaped layer, projected fibers to the septum where those from DM exceeded in number those from DL. These projections further extended to the hypothalamus, particularly the lateral hypothalamic area. The lateral and medial septal nuclei projected back a very small number of ascending fibers to the hippocampal formation. Intraventricular injections of kainic acid induced neuronal loss widely in the hippocampal formation and subsequently produced gliosis in DM. These results indicate that DL receives its main afferents from HD and in turn sends inputs to an intrinsic circuit composed of hippocampal subdivisions DM, Ma, Tr, and the V-shaped layer; and also that DM is the main exit to the septum and hypothalamus. It is suggested that neurons in the V-shaped layer are intrinsic. Together, the results suggest that the V-shaped layer is comparable to the dentate gyrus of the mammalian hippocampal formation and that DM incorporates components comparable to both Ammon's horn and the subiculum.     

Afferent and efferent projections of the central caudal nidopallium in the pigeon (Columba livia)

The central caudal nidopallium (NCC) is a large subdivision of the nidopallium in the pigeon brain, but its connectional anatomy is unknown. Here, we examined the connections of NCC by using tract‐tracing methods. Injections of cholera toxin B‐chain (CTB) in NCC labeled many neurons within NCC. Outside NCC, many labeled neurons were found in the dorsal intermediate mesopallium and medialmost part of the medial intermediate nidopallium, with a few in the intermediate (AI) and medial (AM) arcopallium. In the thalamus, labeled neurons were located in the subrotundal nucleus, the shell region of nucleus ovoidalis, and the caudal part of the dorsolateral posterior thalamic nucleus. Injections of biotinylated dextran amine (BDA) in NCC labeled many fibers running rostrocaudally within NCC. Some of these terminated in the dorsal intermediate mesopallium, but the size of the terminal field was smaller than the region of the dorsal intermediate mesopallium that provided the projection to NCC. NCC sent numerous efferents to AI and AM but few to the thalamus. In contrast, after CTB injections in the dorsal intermediate mesopallium, a few neurons were labeled in NCC, but, after BDA injections in the dorsal intermediate mesopallium, large numbers of labeled fibers were seen to project widely throughout NCC. These findings indicate that the flow of information is predominantly from the dorsal intermediate mesopallium to NCC and from there to the arcopallium (AI and AM). The arcopallial outflow to the medial hypothalamus could imply that NCC is involved in neuroendocrine and autonomic functions and is limbic in nature. J. Comp. Neurol. 517:350–370, 2009. © 2009 Wiley‐Liss, Inc.     

Calcium-binding protein distributions and fiber connections of the nucleus accumbens in the pigeon (Columba livia)

Until recently, the exact location of the avian nucleus accumbens within the basal forebrain had not been well established (Reiner et al. [2004] J Comp Neurol 473:377-414). While a number of previous studies have shown afferents and efferents of the presumptive "nucleus accumbens," detailed and accurate connection patterns of this newly recognized area are still lacking. We set out to clarify these connections using small, localized injections of cholera toxin subunit B and biotinylated dextran amine directly into the nucleus. In order to increase the accuracy of tracer injections into target sites, we first conducted a systematic comparison of three calcium-binding proteins, namely, parvalbumin, calretinin, and calbindin, to characterize the nucleus accumbens and ascertain its boundaries. The results showed that the avian and mammalian nucleus accumbens had remarkable hodological similarities, including the connections with the hippocampus, amygdala, ventral pallidum, lateral hypothalamus, and ventral tegmental area. However, the most significant aspect of the present study is that the avian nucleus accumbens had extensive reciprocal connections with medial pallial structures, the mammalian counterparts of which are unclear. Three implications of this finding are discussed. First, the avian medial pallium may correspond to part of the mammalian prefrontal cortex based on the connections with the nucleus accumbens. Second, the avian brain has a "limbic loop" involving the medial pallium, which also receives input from the avian equivalent of the mediodorsal thalamus. Third, the extensive connections between the accumbens and medial pallium just dorsal to it suggest a column-like organization of limbic-associated areas in the avian telencephalon.     

Afferent and efferent connections of the bullfrog medial pallium.

Horseradish peroxidase or tritiated proline was unilaterally injected into the medial pallium in bullfrogs in order to determine the sources of afferent projections to the medial pallium and the targets of pallial efferent projections. Some cells in all telencephalic centers, except the corpus striatum and the pars lateralis of the amygdala, project to the ipsilateral medial pallium. The medial pallium receives projections from fewer centers in the contralateral hemisphere, which include the medial septal nucleus, the pars medialis of the amygdala, the bed nucleus of the pallial commissure and the medial pallium. The raphe nucleus and the anterior thalamic nuclei appear to be the only sources of afferents to the medial pallium from outside the telencephalon. Efferents of the medial pallium are far more extensive than reported in earlier studies. The medial pallium projects ipsilaterally to all telencephalic nuclei, with the exception of a large part of the corpus striatum, and contralaterally to the medial septal nucleus, the olfactory tubercle, amygdala, medial pallium and bed nucleus of the pallial commissure. Extensive efferent projections also terminate in preoptic and hypothalamic regions, as well as in most thalamic relay nuclei, the pretectum and, possibly, the optic tectum. Similarities to the medial pallium in other tetrapods and to that in mammals suggest that the medial pallium in anurans is homologous to the subicular and CA fields and, possibly, the dentate gyrus in mammals. However, the extensive projections of the medial pallium to the dorsal thalamus and pretectum in anurans may be primitive features of the medial pallium retained in anurans, or uniquely derived features in anurans.     

Septal complex of the telencephalon of lizards: III. Efferent connections and general discussion

The projections of the septum of the lizard Podarcis hispanica (Lacertidae) were studied by combining retrograde and anterograde neuroanatomical tracing. The results confirm the classification of septal nuclei into three main divisions. The nuclei composing the central septal division (anterior, lateral, medial, dorsolateral, and ventrolateral nuclei) displayed differential projections to the basal telencephalon, preoptic and anterior hypothalamus, lateral hypothalamic area, dorsal hypothalamus, mammillary complex, dorsomedial anterior thalamus, ventral tegmental area, interpeduncular nucleus, raphe nucleus, torus semicircularis pars laminaris, reptilian A8 nucleus/ substantia nigra and central gray. For instance, only the medial septal nucleus projected substantially to the thalamus whereas the anterior septum was the only nucleus projecting to the caudal midbrain including the central gray. The anterior and lateral septal nuclei also differ in the way in which their projection to the preoptic hypothalamus terminated. The midline septal division is composed of the dorsal septal nucleus, nucleus septalis impar and nucleus of the posterior pallial commissure. The latter two nuclei projected to the lateral habenula and, at least the nucleus of the posterior pallial commissure, to the mammillary complex. The dorsal septal nucleus projected to the preoptic and periventricular hypothalamus and the anterior thalamus, but its central part seemed to project to the caudal midbrain (up to the midbrain central gray). Finally, the ventromedial septal division (ventromedial septal nucleus) showed a massive projection to the anterior and the lateral tuberomammillary hypothalamus. Data on the connections of the septum of P. hispanica and Gecko gekko are discussed from a comparative point of view and used for better understanding of the functional anatomy of the tetrapodian septum. J. Comp. Neurol. 401:525–548, 1998. © 1998 Wiley-Liss, Inc.     

Anatomy of the avian hippocampal formation

Increasing knowledge of the avian hippocampal formation (hippocampus and parahippocampal area) suggests that it plays a role in a variety of behaviors, such as homing, cache retrieving, visual discrimination, imprinting, and sexual behavior. Knowledge of the neural circuits in the hippocampal formation and its related areas or nuclei is important for the understanding of these functions. This review therefore describes the functional neuroanatomy of the avian hippocampal formations, i.e., its subdivisions, cytoarchitecture, and afferent and efferent connections. Evidence obtained by a combination of Nissl staining and tract-tracing shows that the pigeon hippocampal formation can be divided into seven subdivisions: dorsolateral (DL), dorsomedial (DM), triangular (Tr), V-shaped (V), magnocellular (Ma), parvocellular, and cell-poor regions. DL and DM can be further divided into dorsal and ventral, and lateral and medial portions, respectively. In the hippocampal formation, reciprocal connections are found between DL-DM, DL-Tr, DL-Ma, DM-Ma, DM-V, and Tr-V. Neurons in the V-shaped layer appear to be intrinsic neurons. Sensory inputs from higher order visual and olfactory stations enter DL and DM, are modified or integrated by intrinsic hippocampal circuitry, and the outputs are sent, via DL and DM, to various telencephalic nuclei, septum, and hypothalamus. The neural pathways indicate that the hippocampal formation plays a central role in the limbic system, which also includes the dorsolateral corticoid area, nucleus taeniae of the amygdala, posterior pallial amygdala, septum, medial part of the anterior dorsolateral nucleus of the thalamus, and the lateral mammillary nucleus. Connectional and comparative studies, including the use of kainic acid excitotoxicity, suggest that the V-shaped layer is comparable to the dentate gyrus of the mammalian hippocampal formation and DM to Ammon's horn and subiculum.     

Revised nomenclature for avian telencephalon and some related brainstem nuclei

The standard nomenclature that has been used for many telencephalic and related brainstem structures in birds is based on flawed assumptions of homology to mammals. In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is neurochemically, hodologically, and functionally comparable to the mammalian neocortex, claustrum, and pallial amygdala (all of which derive from the pallial sector of the developing telencephalon). Recognizing that this promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains, avian brain specialists began discussions to rectify this problem, culminating in the Avian Brain Nomenclature Forum held at Duke University in July 2002, which approved a new terminology for avian telencephalon and some allied brainstem cell groups. Details of this new terminology are presented here, as is a rationale for each name change and evidence for any homologies implied by the new names. Revisions for the brainstem focused on vocal control, catecholaminergic, cholinergic, and basal ganglia-related nuclei. For example, the Forum recognized that the hypoglossal nucleus had been incorrectly identified as the nucleus intermedius in the Karten and Hodos (1967) pigeon brain atlas, and what was identified as the hypoglossal nucleus in that atlas should instead be called the supraspinal nucleus. The locus ceruleus of this and other avian atlases was noted to consist of a caudal noradrenergic part homologous to the mammalian locus coeruleus and a rostral region corresponding to the mammalian A8 dopaminergic cell group. The midbrain dopaminergic cell group in birds known as the nucleus tegmenti pedunculopontinus pars compacta was recognized as homologous to the mammalian substantia nigra pars compacta and was renamed accordingly; a group of gamma-aminobutyric acid (GABA)ergic neurons at the lateral edge of this region was identified as homologous to the mammalian substantia nigra pars reticulata and was also renamed accordingly. A field of cholinergic neurons in the rostral avian hindbrain was named the nucleus pedunculopontinus tegmenti, whereas the anterior nucleus of the ansa lenticularis in the avian diencephalon was renamed the subthalamic nucleus, both for their evident mammalian homologues. For the basal (i.e., subpallial) telencephalon, the actual parts of the basal ganglia were given names reflecting their now evident homologues. For example, the lobus parolfactorius and paleostriatum augmentatum were acknowledged to make up the dorsal subdivision of the striatal part of the basal ganglia and were renamed as the medial and lateral striatum. The paleostriatum primitivum was recognized as homologous to the mammalian globus pallidus and renamed as such. Additionally, the rostroventral part of what was called the lobus parolfactorius was acknowledged as comparable to the mammalian nucleus accumbens, which, together with the olfactory tubercle, was noted to be part of the ventral striatum in birds. A ventral pallidum, a basal cholinergic cell group, and medial and lateral bed nuclei of the stria terminalis were also recognized. The dorsal (i.e., pallial) telencephalic regions that had been erroneously named to reflect presumed homology to striatal parts of mammalian basal ganglia were renamed as part of the pallium, using prefixes that retain most established abbreviations, to maintain continuity with the outdated nomenclature. We concluded, however, that one-to-one (i.e., discrete) homologies with mammals are still uncertain for most of the telencephalic pallium in birds and thus the new pallial terminology is largely devoid of assumptions of one-to-one homologies with mammals. The sectors of the hyperstriatum composing the Wulst (i.e., the hyperstriatum accessorium intermedium, and dorsale), the hyperstriatum ventrale, the neostriatum, and the archistriatum have been renamed (respectively) the hyperpallium (hypertrophied pallium), the mesopallium (middle pallium), the nidopallium (nest pallium), and the arcopallium (arched pallium). The posterior part of the archistriatum has been renamed the posterior pallial amygdala, the nucleus taeniae recognized as part of the avian amygdala, and a region inferior to the posterior paleostriatum primitivum included as a subpallial part of the avian amygdala. The names of some of the laminae and fiber tracts were also changed to reflect current understanding of the location of pallial and subpallial sectors of the avian telencephalon. Notably, the lamina medularis dorsalis has been renamed the pallial-subpallial lamina. We urge all to use this new terminology, because we believe it will promote better communication among neuroscientists. Further information is available at http://avianbrain.org     

Organization of the pallium in the fire-bellied toad Bombina orientalis. I: Morphology and axonal projection pattern of neurons revealed by intracellular biocytin labeling

The cytoarchitecture and axonal projection pattern of pallial areas was studied in the fire-bellied toad Bombina orientalis by intracellular injection of biocytin into a total of 326 neurons forming 204 clusters. Five pallial regions were identified, differing in morphology and projection pattern of neurons. The rostral pallium receiving the bulk of dorsal thalamic afferents has reciprocal connections with all other pallial areas and projects to the septum, nucleus accumbens, and anterior dorsal striatum. The medial pallium projects bilaterally to the medial pallium, septum, nucleus accumbens, mediocentral amygdala, and hypothalamus and ipsilaterally to the rostral, dorsal, and lateral pallium. The ventral part of the medial pallium is distinguished by efferents to the eminentia thalami and the absence of contralateral projections. The dorsal pallium has only ipsilateral projections running to the rostral, medial, and lateral pallium; septum; nucleus accumbens; and eminentia thalami. The lateral pallium has ipsilateral projections to the olfactory bulbs and to the rostral, medial, dorsal, and ventral pallium. The ventral pallium including the striatopallial transition area (SPTA) has ipsilateral projections to the olfactory bulbs, rostral and lateral pallium, dorsal striatopallidum, vomeronasal amygdala, and hypothalamus. The medial pallium can be tentatively homologized with the mammalian hippocampal formation, the dorsal pallium with allocortical areas, the lateral pallium rostrally with the piriform and caudally with the entorhinal cortex, the ventral pallium with the accessory olfactory amygdala. The rostral pallium, with its projections to the dorsal and ventral striatopallidum, resembles the mammalian frontal cortex.     

Olfactory and amygdalar structures of the chicken ventral pallium based on the combinatorial expression patterns of LIM and other developmental regulatory genes

We compared the combinatorial expression patterns of several LIM domain‐containing regulatory genes in the ventrolateral pallium of mouse and chicken, in order to identify the homologues of the ventral pallial amygdala and other olfactory structures in birds. Lmo3, Lmo4, Lhx2, and Lhx9 showed comparable expression patterns in the telencephalon of mouse and chicken, which allowed distinction of the ventrolateral pallium and, particularly, the ventral pallial amygdala and entorhinal cortex. Lmo3 was expressed in most of the ventrolateral pallium in both species, including, in chicken, the piriform cortex and dorsal ventricular ridge (mesopallium, nidopallium, and arcopallium) and, in mouse, the piriform cortex, most of the claustral complex, and the pallial amygdala. Lhx9 was differentially expressed in the ventral pallium, where it was restricted to its rostral (olfactory bulb) and caudal (amygdalar and entorhinal) poles. In the caudal pole, expression of Lhx9 overlapped that of its paralog Lhx2. According to these expression patterns, the chicken ventral pallial amygdala appears to include the caudal dorsolateral pallium, the caudal nidopallium, and the whole arcopallium, and each one relates to a distinct ventricular sector. Finally, the combinatorial expression patterns of Lmo3, Lhx9, and Lmo4 distinguished four distinct subdivisions in the superficial, olfactorecipient area of the chicken ventral pallium, which appear comparable to the piriform, entorhinal, amygdalopiriform, and amygdalar cortices of mammals. The results are discussed in the context of the two existing, opposite views on the homology of the dorsal ventricular ridge of sauropsids and in terms of the evolution of pallial derivatives. J. Comp. Neurol. 516:166–186, 2009. © 2009 Wiley‐Liss, Inc.