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Neurons can change their classical neurotransmitters during ontogeny, sometimes going through stages of dual release. Here, we explored the development of the neurotransmitter identity of neurons of the avian nucleus isthmi parvocellularis (Ipc), whose axon terminals are retinotopically arranged in the optic tectum (TeO) and exert a focal gating effect upon the ascending transmission of retinal inputs. Although cholinergic and glutamatergic markers are both found in Ipc neurons and terminals of adult pigeons and chicks, the mRNA expression of the vesicular acetylcholine transporter, VAChT, is weak or absent. To explore how the Ipc neurotransmitter identity is established during ontogeny, we analyzed the expression of mRNAs coding for cholinergic (ChAT, VAChT, and CHT) and glutamatergic (VGluT2 and VGluT3) markers in chick embryos at different developmental stages. We found that between E12 and E18, Ipc neurons expressed all cholinergic mRNAs and also VGluT2 mRNA; however, from E16 through posthatch stages, VAChT mRNA expression was specifically diminished. Our ex vivo deposits of tracer crystals and intracellular filling experiments revealed that Ipc axons exhibit a mature paintbrush morphology late in development, experiencing marked morphological transformations during the period of presumptive dual vesicular transmitter release. Additionally, although ChAT protein immunoassays increasingly label the growing Ipc axon, this labeling was consistently restricted to sparse portions of the terminal branches. Combined, these results suggest that the synthesis of glutamate and acetylcholine, and their vesicular release, is complexly linked to the developmental processes of branching, growing and remodeling of these unique axons.

The dorsal ventricular ridge (DVR), which is the largest component of the avian pallium, contains discrete partitions receiving tectovisual, auditory, and trigeminal ascending projections. Recent studies have shown that the auditory and the tectovisual regions can be regarded as complexes composed of three highly interconnected layers: an internal senso-recipient one, an intermediate afferent/efferent one, and a more external re-entrant one. Cells located in homotopic positions in each of these layers are reciprocally linked by an interlaminar loop of axonal processes, forming columnar-like local circuits. Whether this type of organization also extends to the trigemino-recipient DVR is, at present, not known. This question is of interest, since afferents forming this sensory pathway, exceptional among amniotes, are not thalamic but rhombencephalic in origin. We investigated this question by placing minute injections of neural tracers into selected locations of vital slices of the chicken telencephalon. We found that neurons of the trigemino-recipient nucleus basorostralis pallii (Bas) establish reciprocal, columnar and homotopical projections with cells located in the overlying ventral mesopallium (MV). "Column-forming" axons originated in B and MV terminate also in the intermediate strip, the fronto-trigeminal nidopallium (NFT), in a restricted manner. We also found that the NFT and an internal partition of B originate substantial, coarse-topographic projections to the underlying portion of the lateral striatum. We conclude that all sensory areas of the DVR are organized according to a common neuroarchitectonic motif, which bears a striking resemblance to that of the radial/laminar intrinsic circuits of the sensory cortices of mammals.

Re-entrant connections are inherent to nervous system organization; however, a comprehensive understanding of their operation is still lacking. In birds, topographically organized re-entrant signals, carried by axons from the nucleus-isthmi-parvocellularis (Ipc), are distinctly recorded as bursting discharges across the optic tectum (TeO). Here, we used up to 48 microelectrodes regularly spaced on the superficial tectal layers of anesthetized pigeons to characterize the spatial-temporal pattern of this axonal re-entrant activity in response to different visual stimulation. We found that a brief luminous spot triggered repetitive waves of bursting discharges that, appearing from initial sources, propagated horizontally to areas representing up to 28° of visual space, widely exceeding the area activated by the retinal fibers. In response to visual motion, successive burst waves started along and around the stimulated tectal path, tracking the stimulus in discontinuous steps. When two stimuli were presented, the burst-wave sources alternated between the activated tectal loci, as if only one source could be active at any given time. Because these re-entrant signals boost the retinal input to higher visual areas, their peculiar dynamics mimic a blinking "spotlight," similar to the internal searching mechanism classically used to explain spatial attention. Tectal re-entry from Ipc is thus highly structured and intrinsically discontinuous, and higher tectofugal areas, which lack retinotopic organization, will thus receive incoming visual activity in a sequential and piecemeal fashion. We anticipate that analogous re-entrant patterns, perhaps hidden in less bi-dimensionally organized topographies, may organize the flow of neural activity in other parts of the brain as well.

Recent reports have shown that the avian visual dorsal ventricular ridge (DVR) is organized as a trilayered complex, in which the forming layers-the thalamo-recipient entopallium (E), an overlaying nidopallial stripe called intermediate nidopallium (NI), and the dorsally adjacent mesopallium ventrale-appear to be extensively interconnected by topographically organized columns of reciprocal axonal processes running perpendicular to the layers, an arrangement highly reminiscent to that of the sensory cortices of mammals. In the present report, we implemented in vivo anterograde and retrograde tracing techniques aiming to elucidate the organization of the connections of this complex with other pallial areas. Previous studies have shown that the efferent projections of the visual DVR originate mainly from the NI and E, reaching several distinct associative and premotor nidopallial areas. We found that the efferents from the visual DVR originated solely from the NI, and confirmed that the targets of these projections were the pallial areas described by previous studies. We also found novel projections from the NI to the visual hyperpallium, and to the lateral striatum. Moreover, we found that these projections were reciprocal, topographically organized, and originated from different cell populations within the NI. We conclude that the NI constitutes a specialized layer of the visual DVR that form the core of a dense network of highly specific connections between this region and other higher order areas of the avian pallium. Finally, we discuss to what extent these hodological properties resemble those of the mammalian cortical layers II/III.

The origin of the human alpha rhythm has been a matter of debate since Lord Adrian attributed it to synchronous neural populations in the occipital cortex. While some authors have pointed out the Gaussian characteristics of the alpha rhythm, their results have been repeatedly disregarded in favor of Adrian's interpretation; even though the first EEG Gaussianity reports can be traced back to the origins of EEG. Here we revisit this problem using the envelope analysis -- a method that relies on the fact that the coefficient of variation of the envelope (CVE) for continuous-time zero-mean Gaussian white noise (as well as for any filteredsub-band) is equal to {surd}(4-{pi})/{pi}{approx}0.523, thus making the CVE a fingerprint for Gaussianity. As a consequence, any significant deviation from Gaussianity is linked to synchronous neural dynamics. Low-CVE signals come from phase-locking dynamics, while mid-CVE signals constitute Gaussian noise. High-CVE signals have been linked to unsteady dynamics in populations of nonlinear oscillators. We analyzed occipital EEG and iEEG data from massive public databases and the order parameter of a population of weakly coupled oscillators using the envelope analysis. Our results showed that the human alpha rhythm can be characterized as a rhythmic, Gaussian, or pulsating signal due to intra- and inter-subject variability. Furthermore, Fourier analysis showed that the canonical spectral peak at{approx}10[Hz] is present in all three CVE classes, thus demonstrating that this same peak can be produced by rhythms, Gaussian noise, and pulsating ripples. Alpha-like signals obtained from a population of non-linear oscillators showed a different CVE depending only on the coupling constant, suggesting that the same neural population can produce the amplitude modulation patterns observed in experimental data. iEEG data, however, was found to be mostly Gaussian, specially the signals recorded from the calcarine cortex. These results suggest that a new interpretation for EEG event-related synchronization/desynchronization (ERS/ERD) may be needed. Envelope analysis constitutes a novel complement to traditional Fourier-based methods for neural signal analysis relating amplitude modulations (CVE) to signal energy.

Living beings are autopoietic systems with highly context-dependent structural dynamics and interactions, that determine whether a disturbance in the genotype or environment will lead or not to phenotypic change. The concept of epigenesis entails how a change in the phenotype may not correspond to a change in the structure of an earlier developmental stage, including the genome. Disturbances of embryonic structure may fail to change the phenotype, as in regulated development, or when different genotypes are associated to a single phenotype. Likewise, the same genotype or early embryonic structure may develop different phenotypes, as in phenotypic plasticity. Disturbances that fail to trigger phenotypic change are considered neutral, but even so, they can alter unexpressed developmental potential. Here, we present conceptual diagrams of the "epigenic field": similar to Waddington's epigenetic landscapes, but including the ontogenic niche (organism/environment interactional dynamics during ontogeny) as a factor in defining epigenic fields, rather than just selecting among possible pathways. Our diagrams illustrate transgenerational changes of genotype, ontogenic niche, and their correspondence (or lack thereof) with changes of phenotype. Epigenic fields provide a simple way to understand developmental constraints on evolution, for instance: how constraints evolve as a result of developmental system drift; how neutral changes can be involved in genetic assimilation and de-assimilation; and how constraints can evolve as a result of neutral changes in the ontogenic niche (not only the genotype). We argue that evolutionary thinking can benefit from a framework for evolution with conceptual foundations at the organismal level.

The parabigeminal nucleus (PBG) is the mammalian homologue to the isthmic complex of other vertebrates. Optogenetic stimulation of the PBG induces freezing and escape in mice, a result thought to be caused by a PBG projection to the central nucleus of the amygdala. However, the isthmic complex, including the PBG, has been classically considered satellite nuclei of the Superior Colliculus (SC), which upon stimulation of its medial part also triggers fear and avoidance reactions. As the PBG-SC connectivity is not well characterized, we investigated whether the topology of the PBG projection to the SC could be related to the behavioral consequences of PBG stimulation. To that end, we performed immunohistochemistry, in situ hybridization and neural tracer injections in the SC and PBG in a diurnal rodent, the Octodon degus. We found that all PBG neurons expressed both glutamatergic and cholinergic markers and were distributed in clearly defined anterior (aPBG) and posterior (pPBG) subdivisions. The pPBG is connected reciprocally and topographically to the ipsilateral SC, whereas the aPBG receives afferent axons from the ipsilateral SC and projected exclusively to the contralateral SC. This contralateral projection forms a dense field of terminals that is restricted to the medial SC, in correspondence with the SC representation of the aerial binocular field which, we also found, in O. degus prompted escape reactions upon looming stimulation. Therefore, this specialized topography allows binocular interactions in the SC region controlling responses to aerial predators, suggesting a link between the mechanisms by which the SC and PBG produce defensive behaviors.

A defining feature of the amniote tecto-fugal visual pathway is a massive bilateral projection to the thalamus originating from a distinct neuronal population, tectal ganglion cells (TGCs), of the optic tectum/superior colliculus (TeO/SC). In sauropsids, the thalamic target of the tecto-fugal pathway is the nucleus rotundus thalami (Rt). TGCs axons collateralize en route to Rt to target the nucleus pretectalis principalis (PT), which in turn gives rise to bilateral projection to the TeO. In rodents, the thalamic target of these TGCs afferents is the caudal division of the pulvinar complex (PulC). No pretectal structures in receipt of TGC collaterals have been described in this group. However, Baldwin et al. (Journal of Comparative Neurology, 2011;519(6):1071-1094) reported in the squirrel a feedback projection from the PulC to the SC. Pulvino-tectal (Pul-T) cells lie at the caudal pole of the PulC, intermingled with the axonal terminals of TGCs. Here, by performing a combination of neuronal tracing, immunohistochemistry, immunofluorescence, and in situ hybridization, we characterized the pattern of projections, neurochemical profile, and genoarchitecture of Pul-T cells in the diurnal Chilean rodent Octodon degus. We found that Pul-T neurons exhibit pretectal, but not thalamic, genoarchitectonical markers, as well as hodological and neurochemical properties that match specifically those of the avian nucleus PT. Thus, we propose that Pul-T cells constitute a pretectal cell population hidden within the dorsal thalamus of mammals. Our results solve the oddity entailed by the apparent existence of a noncanonic descending sensory thalamic projection and further stress the conservative character of the tectofugal pathway.

In mammals, the accessory olfactory or vomeronasal system exhibits a wide variety of anatomical arrangements. In caviomorph rodents, the accessory olfactory bulb (AOB) exhibits a dichotomic conformation, in which two subdomains, the anterior (aAOB) and the posterior (pAOB), can be readily distinguished. Interestingly, different species of this group exhibit bias of different sign between the AOB subdomains (aAOB larger than pAOB or vice versa). Such species-specific biases have been related with contrasting differences in the habitat of the different species (e.g. arid vs. humid environments). Aiming to deepen these observations, we performed a morphometric comparison of the AOB subdomains between two sister species of octodontid rodents, Octodon lunatus and Octodon degus. These species are interesting for comparative purposes, as they inhabit similar landscapes but exhibit contrasting social habits. Previous reports have shown that O. degus, a highly social species, exhibits a greatly asymmetric AOB, in which the aAOB has twice the size of the pAOB and features more and larger glomeruli in its glomerular layer (GL). We found that the same as in O. degus, the far less social O. lunatus also exhibits a bias, albeit less pronounced, to a larger aAOB. In both species, this bias was also evident for the mitral/tufted cells number. But unlike in O. degus, in O. lunatus this bias was not present at the GL. In comparison with O. degus, in O. lunatus the aAOB GL was significantly reduced in volume, while the pAOB GL displayed a similar volume. We conclude that these sister species exhibit a very sharp difference in the anatomical conformation of the AOB, namely, the relative size of the GL of the aAOB subdomain, which is larger in O. degus than in O. lunatus. We discuss these results in the context of the differences in the lifestyle of these species, highlighting the differences in social behaviour as a possible factor driving to distinct AOB morphometries.

The sensory-motor division of the avian arcopallium receives parallel inputs from primary and high-order pallial areas of sensory and vocal control pathways, and sends a prominent descending projection to ascending and premotor, subpallial stages of these pathways. While this organization is well established for the auditory and trigeminal systems, the arcopallial subdivision related to the tectofugal visual system and its descending projection to the optic tectum (TeO) has been less investigated. In this study, we charted the arcopallial area displaying tectofugal visual responses and by injecting neural tracers, we traced its connectional anatomy. We found visual motion-sensitive responses in a central region of the dorsal (AD) and intermediate (AI) arcopallium, in between previously described auditory and trigeminal zones. Blocking the ascending tectofugal sensory output, canceled these visual responses in the arcopallium, verifying their tectofugal origin. Injecting PHA-L into the visual, but not into the auditory AI, revealed a massive projection to tectal layer 13 and other tectal related areas, sparing auditory, and trigeminal ones. Conversely, CTB injections restricted to TeO retrogradely labeled neurons confined to the visual AI. These results show that the AI zone receiving tectofugal inputs sends top-down modulations specifically directed to tectal targets, just like the auditory and trigeminal AI zones project back to their respective subpallial sensory and premotor areas, as found by previous studies. Therefore, the arcopallium seems to be organized in a parallel fashion, such that in spite of expected cross-modal integration, the different sensory-motor loops run through separate subdivisions of this structure.

Navigational and social challenges due to habitat conditions and sociality are known to influence dentate gyrus (DG) morphology, yet the relative importance of these factors remains unclear. Thus, we studied three natural populations of O. lunatus (Los Molles) and Octodon degus (El Salitre and Rinconada), two caviomorph species that differ in the extent of sociality and with contrasting vegetation cover of habitat used. The brains and DG of male and female breeding degus with simultaneous information on their physical and social environments were examined. The extent of sociality was quantified from total group size and range area overlap. O. degus at El Salitre was more social than at Rinconada and than O. lunatus from Los Molles. The use of transects to quantify cover of vegetation (and other physical objects in the habitat) and measures of the spatial behavior of animals indicated animal navigation based on unique cues or global landmarks is more cognitively challenging to O. lunatus. During lactation, female O. lunatus had larger brains than males. Relative DG volume was similar across sexes and populations. The right hemisphere of male and female O. lunatus had more cells than the left hemisphere, with DG directional asymmetry not found in O. degus. Degu population differences in brain size and DG cell number seemed more responsive to differences in habitat than to differences in sociality. Yet, large-sized O. degus (but not O. lunatus) that ranged over larger areas and were members of larger social groups had more DG cells per hemisphere. Thus, within-population variation in DG cell number by hemisphere was consistent with a joint influence of habitat and sociality in O. degus at El Salitre. Fil: Sobrero, Raul Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Ciencias Veterinarias del Litoral. Universidad Nacional del Litoral. Facultad de Ciencias Veterinarias. Instituto de Ciencias Veterinarias del Litoral; Argentina. Universidad de Chile; Chile Fil: Fernández Aburto, Pedro. Universidad de Chile; Chile Fil: Ly Prieto, Álvaro. Pontificia Universidad Católica de Chile; Chile Fil: Delgado, Scarlett E.. Universidad de Chile; Chile Fil: Mpodozis, Jorge. Universidad de Chile; Chile Fil: Ebensperger, Luis A.. Pontificia Universidad Católica de Chile; Chile

The avian pretectal and ventrothalamic nuclei, encompassing the griseum tectale (GT), n. lentiformis mesencephali (LM), and n. geniculatus lateralis pars ventralis (GLv), are prominent retinorecipient structures related to optic flow operations and visuomotor control. Hence, a close coordination of these neural circuits is to be expected. Yet the connectivity among these nuclei is poorly known. Here, using intracellular labeling and in situ hybridization, we investigated the detailed morphology, connectivity, and neurochemical identity of neurons in these nuclei. Two different cell types exist in the GT: one that generates an axonal projection to the optic tectum (TeO), LM, GLv, and n. intercalatus thalami (ICT), and a second population that only projects to the LM and GLv. In situ hybridization revealed that most neurons in the GT express the vesicular glutamate transporter (VGluT2) mRNA, indicating a glutamatergic identity. In the LM, three morphological cell types were defined, two of which project axons towards dorsal targets. The LM neurons showed strong VGluT2 expression. Finally, the cells located in the GLv project to the TeO, LM, GT, n. principalis precommisuralis (PPC), and ICT. All neurons in the GLv showed strong expression of the vesicular inhibitory amino acid transporter (VIAAT) mRNA, suggesting a GABAergic identity. Our results show that the pretectal and ventrothalamic nuclei are highly interconnected, especially by glutamatergic and GABAergic neurons from the GT and GLv, respectively. This complex morphology and connectivity might be required to organize orienting visuomotor behaviors and coordinate the specific optic flow patterns that they induce. J. Comp. Neurol. 524:2208-2229, 2016. © 2015 Wiley Periodicals, Inc.

The optic tectum in birds and its homologue the superior colliculus in mammals both send major bilateral, nontopographic projections to the nucleus rotundus and caudal pulvinar, respectively. These projections originate from widefield tectal ganglion cells (TGCs) located in layer 13 in the avian tectum and in the lower superficial layers in the mammalian colliculus. The TGCs characteristically have monostratified arrays of brush-like dendritic terminations and respond mostly to bidimensional motion or looming features. In birds, this TGC-mediated tectofugal output is controlled by feedback signals from the nucleus isthmi pars parvocellularis (Ipc). The Ipc neurons display topographically organized axons that densely ramify in restricted columnar terminal fields overlapping various neural elements that could mediate this tectofugal control, including the retinal terminals and the TGC dendrites themselves. Whether the Ipc axons make synaptic contact with these or other tectal neural elements remains undetermined. We double labeled Ipc axons and their presumptive postsynaptic targets in the tectum of chickens (Gallus gallus) with neural tracers and performed an ultrastructural analysis. We found that the Ipc terminal boutons form glomerulus-like structures in the superficial and intermediate tectal layers, establishing asymmetric synapses with several dendritic profiles. In these glomeruli, at least two of the postsynaptic dendrites originated from TGCs. We also found synaptic contacts between retinal terminals and TGC dendrites. These findings suggest that, in birds, Ipc axons control the ascending tectal outflow of retinal signals through direct synaptic contacts with the TGCs.

The dorsal ventricular ridge (DVR) is one of the main components of the sauropsid pallium. In birds, the DVR is formed by an inner region, the nidopallium, and a more dorsal region, the mesopallium. The nidopallium contains discrete areas that receive auditory, visual, and multisensory collothalamic projections. These nidopallial nuclei are known to sustain reciprocal, short-range projections with their overlying mesopallial areas. Recent findings on the anatomical organization of the auditory DVR have shown that these short-range projections have a columnar organization that closely resembles that of the mammalian neocortex. However, it is unclear whether this columnar organization generalizes to other areas within the DVR. Here we examine in detail the organization of the visual DVR, performing small, circumscribed deposits of neuronal tracers as well as intracellular fillings in brain slices. We show that the visual DVR is organized in three main laminae, the thalamorecipient nucleus entopallium; a dorsally adjacent nidopallial lamina, the intermediate nidopallium; and a contiguous portion of the ventral mesopallium, the mesopallium ventrale. As in the case of the auditory DVR, we found a highly topographically organized system of reciprocal interconnections among these layers, which was formed by dorsoventrally oriented, discrete columnar bundles of axons. We conclude that the columnar organization previously demonstrated in the auditory DVR is not a unique feature but a general characteristic of the avian sensory pallium. We discuss these results in the context of a comparison between sauropsid and mammalian pallial organization.

To what extent can the mammalian visual system be shaped by visual behavior? Here we analyze the shape of the visual fields, the densities and distribution of cells in the retinal ganglion-cell layer and the organization of the visual projections in two species of facultative non-strictly subterranean rodents, Spalacopus cyanus and Ctenomys talarum, aiming to compare these traits with those of phylogenetically closely related species possessing contrasting diurnal/nocturnal visual habits. S. cyanus shows a definite zone of frontal binocular overlap and a corresponding area centralis, but a highly reduced amount of ipsilateral retinal projections. The situation in C. talarum is more extreme as it lacks of a fronto-ventral area of binocular superposition, has no recognizable area centralis and shows no ipsilateral retinal projections except to the suprachiasmatic nucleus. In both species, the extension of the monocular visual field and of the dorsal region of binocular overlap as well as the whole set of contralateral visual projections, appear well-developed. We conclude that these subterranean rodents exhibit, paradoxically, diurnal instead of nocturnal visual specializations, but at the same time suffer a specific regression of the anatomical substrate for stereopsis. We discuss these findings in light of the visual ecology of subterranean lifestyles Fil: Vega Zuniga, Tomas. Universidad de Chile; Chile Fil: Medina, Felipe. Universidad de Chile; Chile Fil: Marin, Gonzalo. Universidad de Chile; Chile Fil: Letelier, Juán Carlos. Universidad de Chile; Chile Fil: Palacios, Adrián G.. Universidad de Valparaíso; Chile Fil: Němec, Pavel. Charles University in Prague; República Checa Fil: Schleich, Cristian. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones Marinas y Costeras. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Marinas y Costeras; Argentina Fil: Mpodozis, Jorge. Universidad de Chile; Chile

The isthmic complex is part of a visual midbrain circuit thought to be involved in stimulus selection and spatial attention. In birds, this circuit is composed of the nuclei isthmi pars magnocellularis (Imc), pars parvocellularis (Ipc), and pars semilunaris (SLu), all of them reciprocally connected to the ipsilateral optic tectum (TeO). The Imc conveys heterotopic inhibition to the TeO, Ipc, and SLu via widespread γ-aminobutyric acid (GABA)ergic axons that allow global competitive interactions among simultaneous sensory inputs. Anatomical studies in the chick have described a cytoarchitectonically uniform Imc nucleus containing two intermingled cell types: one projecting to the Ipc and SLu and the other to the TeO. Here we report that in passerine species, the Imc is segregated into an internal division displaying larger, sparsely distributed cells, and an external division displaying smaller, more densely packed cells. In vivo and in vitro injections of neural tracers in the TeO and the Ipc of the zebra finch demonstrated that neurons from the external and internal subdivisions project to the Ipc and the TeO, respectively, indicating that each Imc subdivision contains one of the two cell types hodologically defined in the chick. In an extensive survey across avian orders, we found that, in addition to passerines, only species of Piciformes and Rallidae exhibited a segregated Imc, whereas all other groups exhibited a uniform Imc. These results offer a comparative basis to investigate the functional role played by each Imc neural type in the competitive interactions mediated by this nucleus.

O surgimento do sistema imune na filogênese dos vertebrados mandibulados com sua vasta coleção de receptoreslinfocitários expressos de forma clonal é usualmente visto como um processo otimizado para a defesa do organismo.Há uma clara associação entre o neodarwinismo, a visão dominante na Biologia atual e a descrição usual da atividadeimunológica, conhecida como imunidade adaptativa. Neste texto, sugerimos que toda uma nova abordagem à origem dossistemas vivos, denominada por Maturana e Mpodozis deriva filogênica natural, aplicada à imunologia, pode substituir aexplicação neodarwinista sobre a origem da atividade imunológica. Além disso, pelo emprego dos conceitos de tímpanos (spandrels) e de exaptação, criados por Gould e colaboradores, revemos dados da imunologia comparada e afirmamos que o sistema imune não se formou como um sistema otimizado para a defesa do organismo, mas pode ser visto como um tímpano (spandrel), uma consequência de processos que originalmente não estavam relacionados a interações do organismo com materiais estranhos. Afirmamos também que a inserção de linfócitos na dinâmica do organismo era necessária para contornar o potencial imunopatogênico de expansões clonais.

The mammalian pulvinar complex is a collection of dorsal thalamic nuclei related to several visual and integrative processes. Previous studies have shown that the superficial layers of the superior colliculus project to multiple divisions of the pulvinar complex. Although most of these works agree about the existence of an ipsilateral tectopulvinar projection arising from the stratum griseum superficialis, some others report a bilateral projection originating from this same tectal layer. We investigated the organization of the tectopulvinar projections in the Californian ground squirrel using cholera toxin B (CTb). We confirmed previous studies showing that the caudal pulvinar of the squirrel receives a massive bilateral projection originating from a specific cell population located in the superficial collicular layers (SGS3, also called the "lower SGS" or "SGSL"). We found that this projection shares striking structural similarities with the tectorotundal pathway of birds and reptiles. Morphology of the collicular cells originating this projection closely corresponds to that of the bottlebrush tectal cells described previously for chickens and squirrels. In addition, we found that the rostral pulvinar receives an exclusively ipsilateral projection from a spatially separate population of collicular cells located at the base of the stratum opticum, deeper than the cells projecting to the caudal pulvinar. These results strongly support, at a structural level, the homology of the pathway originating in the SGS3 collicular cells upon the caudal pulvinar with the tectorotundal pathway of nonmammalian amniotes and contribute to clarifying the general organization of the tectopulvinar pathways in mammals.

The vomeronasal system is crucial for social and sexual communication in mammals. Two populations of vomeronasal sensory neurons, each expressing Gαi2 or Gαo proteins, send projections to glomeruli of the rostral or caudal accessory olfactory bulb, rAOB and cAOB, respectively. In rodents, the Gαi2- and Gαo-expressing vomeronasal pathways have shown differential responses to small/volatile vs. large/non-volatile semiochemicals, respectively. Moreover, early gene expression suggests predominant activation of rAOB and cAOB neurons in sexual vs. aggressive contexts, respectively. We recently described the AOB of Octodon degus, a semiarid-inhabiting diurnal caviomorph. Their AOB has a cell indentation between subdomains and the rAOB is twice the size of the cAOB. Moreover, their AOB receives innervation from the lateral aspect, contrasting with the medial innervation of all other mammals examined to date. Aiming to relate AOB anatomy with lifestyle, we performed a morphometric study on the AOB of the capybara, a semiaquatic caviomorph whose lifestyle differs remarkably from that of O. degus. Capybaras mate in water and scent-mark their surroundings with oily deposits, mostly for male-male communication. We found that, similar to O. degus, the AOB of capybaras shows a lateral innervation of the vomeronasal nerve, a cell indentation between subdomains and heterogeneous subdomains, but in contrast to O. degus the caudal portion is larger than the rostral one. We also observed that four other caviomorph species present a lateral AOB innervation and a cell indentation between AOB subdomains, suggesting that those traits could represent apomorphies of the group. We propose that although some AOB traits may be phylogenetically conserved in caviomorphs, ecological specializations may play an important role in shaping the AOB.

The vomeronasal system (VNS) of rodents participates in the regulation of a variety of social and sexual behaviours related to semiochemical communication. All rodents studied so far possess two parallel pathways from the vomeronasal organ (VNO) to the accessory olfactory bulb (AOB). These segregated afferences express either Gi2 or Go protein alpha-subunits and innervate the rostral or caudal half of the AOB, respectively. In muroid rodents, such as rats and mice, both subdivisions of the AOB are of similar proportions; as there is no anatomical feature indicative of the segregation, histochemical detection has been required to portray its boundary. We studied the AOB of Octodon degus, a diurnal caviomorph rodent endemic to central Chile, and found several distinctive traits not reported in a rodent before: (i) the vomeronasal nerve innervates the AOB from its lateral aspect, in opposition to the medial innervation described in rabbits and muroids, (ii) an indentation that spans all layers delimits the boundary between the rostral and caudal AOB subdivisions (rAOB and cAOB, respectively), (iii) the rAOB is twice the size of the cAOB and features more and larger glomeruli, and (iv) the rAOB, but not the cAOB, shows male-biased sexual dimorphisms in size and number of glomeruli, while the cAOB, but not the rAOB, shows a male-biased dimorphism in mitral cell density. The heterogeneities we describe here within AOB subdomains suggest that these segregated regions may engage in distinct operationalities. We discuss our results in relation to conspecific semiochemical communication in O. degus, and present it as a new animal model for the study of VNS neurobiology and evolution.

The avian pretectal and ventrothalamic nuclei, encompassing the griseum tectale (GT), n. lentiformis mesencephali (LM), and n. geniculatus lateralis pars ventralis (GLv), are prominent retinorecipient structures related to optic flow operations and visuomotor control. Hence, a close coordination of these neural circuits is to be expected. Yet the connectivity among these nuclei is poorly known. Here, using intracellular labeling and in situ hybridization, we investigated the detailed morphology, connectivity, and neurochemical identity of neurons in these nuclei. Two different cell types exist in the GT: one that generates an axonal projection to the optic tectum (TeO), LM, GLv, and n. intercalatus thalami (ICT), and a second population that only projects to the LM and GLv. In situ hybridization revealed that most neurons in the GT express the vesicular glutamate transporter (VGluT2) mRNA, indicating a glutamatergic identity. In the LM, three morphological cell types were defined, two of which project axons towards dorsal targets. The LM neurons showed strong VGluT2 expression. Finally, the cells located in the GLv project to the TeO, LM, GT, n. principalis precommisuralis (PPC), and ICT. All neurons in the GLv showed strong expression of the vesicular inhibitory amino acid transporter (VIAAT) mRNA, suggesting a GABAergic identity. Our results show that the pretectal and ventrothalamic nuclei are highly interconnected, especially by glutamatergic and GABAergic neurons from the GT and GLv, respectively. This complex morphology and connectivity might be required to organize orienting visuomotor behaviors and coordinate the specific optic flow patterns that they induce. J. Comp. Neurol. 524:2208-2229, 2016. © 2015 Wiley Periodicals, Inc.

Owen’s pre-evolutionary definition of a homologue as “the same organ in different animals under every variety of form and function” and its redefinition after Darwin as “the same trait in different lineages due to common ancestry” entail the same heuristic problem: how to establish “sameness”. Although different criteria for homology often conflict, there is currently a generalized acceptance of gene expression as the best criterion. This gene-centered view of homology results from a reductionist and preformationist concept of living beings. Here, we adopt an alternative organismic-epigenetic viewpoint, and conceive living beings as systems whose identity is given by the dynamic interactions between their components at their multiple levels of composition. We posit that there cannot be an absolute homology criterion, and instead, homology should be inferred from comparisons at the levels and developmental stages where the delimitation of the compared trait lies. In this line, we argue that neural connectivity, i.e., the hodological criterion, should prevail in the determination of homologies between brain supra-cellular structures, such as the vertebrate pallium.

The optic tectum in birds and its homologue the superior colliculus in mammals both send major bilateral, nontopographic projections to the nucleus rotundus and caudal pulvinar, respectively. These projections originate from widefield tectal ganglion cells (TGCs) located in layer 13 in the avian tectum and in the lower superficial layers in the mammalian colliculus. The TGCs characteristically have monostratified arrays of brush-like dendritic terminations and respond mostly to bidimensional motion or looming features. In birds, this TGC-mediated tectofugal output is controlled by feedback signals from the nucleus isthmi pars parvocellularis (Ipc). The Ipc neurons display topographically organized axons that densely ramify in restricted columnar terminal fields overlapping various neural elements that could mediate this tectofugal control, including the retinal terminals and the TGC dendrites themselves. Whether the Ipc axons make synaptic contact with these or other tectal neural elements remains undetermined. We double labeled Ipc axons and their presumptive postsynaptic targets in the tectum of chickens (Gallus gallus) with neural tracers and performed an ultrastructural analysis. We found that the Ipc terminal boutons form glomerulus-like structures in the superficial and intermediate tectal layers, establishing asymmetric synapses with several dendritic profiles. In these glomeruli, at least two of the postsynaptic dendrites originated from TGCs. We also found synaptic contacts between retinal terminals and TGC dendrites. These findings suggest that, in birds, Ipc axons control the ascending tectal outflow of retinal signals through direct synaptic contacts with the TGCs.

Most birds have an opposable digit 1 (hallux) allowing the foot to grasp, which evolved from the non-opposable hallux of early theropod dinosaurs. An important morphological difference with early theropods is the twisting of the long axis of its metatarsal. Here, we show how embryonic musculature and the onset of its activity are required for twisting of metatarsal 1 (Mt1) and retroversion of the hallux. Pharmacologically paralyzed embryos do not fully retrovert the hallux and have a straight Mt1 shaft, phenocopying the morphology of early tetanuran dinosaurs. Molecular markers of cartilage maturation and ossification show that differentiation of Mt1 is significantly delayed compared to Mt2-4. We hypothesize on how delayed maturation may have increased plasticity, facilitating muscular twisting. Our experimental results emphasize the importance of embryonic muscular activity in the evolutionary origin of a crucial adaptation.

The dorsal ventricular ridge (DVR) is one of the main components of the sauropsid pallium. In birds, the DVR is formed by an inner region, the nidopallium, and a more dorsal region, the mesopallium. The nidopallium contains discrete areas that receive auditory, visual, and multisensory collothalamic projections. These nidopallial nuclei are known to sustain reciprocal, short-range projections with their overlying mesopallial areas. Recent findings on the anatomical organization of the auditory DVR have shown that these short-range projections have a columnar organization that closely resembles that of the mammalian neocortex. However, it is unclear whether this columnar organization generalizes to other areas within the DVR. Here we examine in detail the organization of the visual DVR, performing small, circumscribed deposits of neuronal tracers as well as intracellular fillings in brain slices. We show that the visual DVR is organized in three main laminae, the thalamorecipient nucleus entopallium; a dorsally adjacent nidopallial lamina, the intermediate nidopallium; and a contiguous portion of the ventral mesopallium, the mesopallium ventrale. As in the case of the auditory DVR, we found a highly topographically organized system of reciprocal interconnections among these layers, which was formed by dorsoventrally oriented, discrete columnar bundles of axons. We conclude that the columnar organization previously demonstrated in the auditory DVR is not a unique feature but a general characteristic of the avian sensory pallium. We discuss these results in the context of a comparison between sauropsid and mammalian pallial organization.

We evaluated the extent to which manipulation of early olfactory environment can influence social behaviours in the South American Hystricognath rodent Octodon degus. The early olfactory environment of newborn degus was manipulated by scenting all litter members with eucalyptol during the first month of life. The social behaviour of sexually mature animals (5-7 months old) towards conspecifics was then assessed using a y-maze to compare the response of control (naïve) and treated animals to two different olfactory configurations (experiment 1): (i) a non-familiarized conspecific impregnated with eucalyptol (eucalyptol arm) presented against (ii) a non-familiarized unscented conspecific (control arm). In addition, in dyadic encounters, we assessed the behaviour of control and eucalyptol treated animals towards a non-familiarized conspecific scented with eucalyptol (experiment 2). We found that control subjects explored and spent significantly less time in the eucalyptol arm, indicating neophobic behaviours towards the artificially scented conspecific. Treated subjects explored and spent similar time in both arms of the maze, showing the same interest for both olfactory stimuli presented. During dyadic encounters in experiment 2, an interaction effect between early experience and sex was observed. Control males escaped and avoided their scented partner more frequently than eucalyptol treated male subjects and than females. Both groups did not differ in the exploration of their scented partners, suggesting that avoidance within agonistic context does not relate to neophobic behaviours. Our results suggest that the exposure to eucalyptol during early ontogeny decreases evasive behaviours within an agonistic context as a result of olfactory learning. Altogether, these results indicate that olfactory cues learned in early ontogeny can influence olfactory-guided behaviours in adult degus.

The anklebone (astragalus) of dinosaurs presents a characteristic upward projection, the ‘ascending process' (ASC). The ASC is present in modern birds, but develops a separate ossification centre, and projects from the calcaneum in most species. These differences have been argued to make it non-comparable to dinosaurs. We studied ASC development in six different orders of birds using traditional techniques and spin–disc microscopy for whole-mount immunofluorescence. Unexpectedly, we found the ASC derives from the embryonic intermedium, an ancient element of the tetrapod ankle. In some birds it comes in contact with the astragalus, and, in others, with the calcaneum. The fact that the intermedium fails to fuse early with the tibiale and develops an ossification centre is unlike any other amniotes, yet resembles basal, amphibian-grade tetrapods. The ASC originated in early dinosaurs along changes to upright posture and locomotion, revealing an intriguing combination of functional innovation and reversion in its evolution., The anklebone of dinosaurs presents the ‘ascending process' (ASC), a projection also found in modern birds, yet the ASC in birds has unique developmental characteristics. Here, the authors show that the ASC in six birds develops from an ancient element of the tetrapod ankle in a way that resembles basal tetrapods.

Most of the physiological studies of the pigeon retino-tectal visual pathway have investigated the accessible tectum, a small dorso-lateral tectal section that can be easily accessed by a simple craniotomy. However, at present we lack a detailed study of the topographical arrangement between the visual field, the retina and the accessible tectum. In particular, it is not known which section of the visual field is mapped onto the accessible tectum, and which of the specialized retinal areas mediates this projection. Here we determined, using local field potential (LFP) recordings and reverse retinoscopy, the shape, size and position in the visual space of the portion of the visual field mapped onto the accessible tectum (called here the accessible visual field, or AVF). Using this data and the mapping of Nalbach et al. [Vis. Res. 30 (4) (1990) 529], the retinal area corresponding to the AVF was determined. Such retinal area was also directly delimited by means of retrograde transport of DiI. The results indicate that the AVF is a triangular perifoveal zone encompassing only 15% of total visual field. The retinal region corresponding to the AVF has the shape of an elongated triangle that runs parallel to the visual equator and contains the fovea, the tip of the pecten, a perifoveal region of the yellow field and a small crescent of the red field. In agreement with this anatomical heterogeneity, visual evoked potentials measured in different parts of the accessible tectum present steep variations in shape and size. These results are helpful to better design and interpret anatomical and physiological experiments involving the pigeon's visual system.

The retinotectofugal system is the main visual pathway projecting upon the telencephalon in birds and many other nonmammalian vertebrates. The ascending tectal projection arises exclusively from cells located in layer 13 of the optic tectum and is directed bilaterally toward the thalamic nucleus rotundus. Although previous studies provided evidence that different types of tectal layer 13 cells project to different subdivisions in Rt, apparently without maintaining a retinotopic organization, the detailed spatial organization of this projection remains obscure. We reexamined the pigeon tectorotundal projection using conventional tracing techniques plus a new method devised to perform small deep-brain microinjections of crystalline tracers. We found that discrete injections involving restricted zones within one subdivision retrogradely label a small fraction of layer 13 cells that are distributed throughout the layer, covering most of the tectal representation of the contralateral visual field. Double-tracer injections in one subdivision label distinct but intermingled sets of layer 13 neurons. These results, together with the tracing of tectal axonal terminal fields in the rotundus, lead us to propose a novel “interdigitating” topographic arrangement for the tectorotundal projection, in which intermingled sets of layer 13 cells, presumably of the same particular class and distributed in an organized fashion throughout the surface of the tectum, terminate in separate regions within one subdivision. This spatial organization has significant consequences for the understanding of the physiological and functional properties of the tectofugal pathway in birds. J. Comp. Neurol. 458:361‐380, 2003. © 2003 Wiley-Liss, Inc. Indexing terms: tectofugal pathway; nucleus rotundus; topography; visual system; birds

In scatter-hoarding species, several behavioral and neuroanatomical adaptations allow them to store and retrieve thousands of food items per year. Nectarivorous animals face a similar scenario having to remember quality, location and replenishment schedules of several nectar sources. In the green-backed firecrown hummingbird (Sephanoides sephanoides), males are territorial and have the ability to accurately keep track of nectar characteristics of their defended food sources. In contrast, females display an opportunistic strategy, performing rapid intrusions into males territories. In response, males behave aggressively during the non-reproductive season. In addition, females have higher energetic demands due to higher thermoregulatory costs and travel times. The natural scenario of this species led us to compared cognitive abilities and hippocampal size between males and females. Males were able to remember nectar location and renewal rates significantly better than females. However, the hippocampal formation was significantly larger in females than males. We discuss these findings in terms of sexually dimorphic use of spatial resources and variable patterns of brain dimorphisms in birds.

We have developed an instrument to perform microinjections of solid neural tracers into deep structures of the brain. The instrument consists of a thin hypodermic needle equipped with a movable internal rod, which is connected to a pressure chamber. When a pressure pulse is applied to the chamber, the rod moves forward and back inside the needle, pushing out a solid load previously packed inside the needle tip. By attaching a microelectrode to the instrument, it is also possible to have electrophysiological control of the injection placement. To test the instrument, we microinjected DiI and rhodamine crystals into selected structures of the visual system of pigeons. The results show small, well-defined injection sites, accurately located in the desired targets, together with well-developed anterogade and retrograde transport, selectively originated from the injection sites. This method extends the usage of solid tracers to most structures in the brain and may, in certain cases, be more advantageous than the conventional method of injecting tracer solutions.

Here we describe a method to fix gaze positions and to significantly reduce saccadic oscillations in pigeons. The procedure consists of a mechanical immobilization of the eye through the use of an electromagnet that exerts a radial force upon a small metal rectangle glued to the dorsal part of the eye. The method can be used in avian visual neurophysiology in order to hold the eye immobilized for periods of time, long enough to map the properties of visual receptive fields and investigate the possible functions of saccadic oscillations.

The tectofugal pathway is a massive ascending polysynaptic pathway from the tectum to the thalamus and then to the telencephalon. In birds, the initial component of this pathway is known as the tectorotundal pathway; in mammals, it is known as the tectopulvinar pathway. The avian tectorotundal pathway is highly developed; thus, it provides a particularly appropriate model for exploring the fundamental properties of this system in all amniotes. To further define the connectivity of the tectorotundal projections of the tectofugal pathway, we injected cholera toxin B fragment into various rotundal divisions, the tectobulbar projection, and the ventral supraoptic decussation of the pigeon. We found intense bilateral retrograde labeling of neurons that stratified within layer 13 and, in certain cases, granular staining in layer 5b of the optic tectum. Based on these results, we propose that there are two distinct types of layer 13 neurons that project to the rotundus: 1) type I neurons, which are found in the outer sublamina of layer 13 (closer to layer 12) and which project to the anterior and centralis rotundal divisions, and 2) type II neurons, which are found in the inner sublamina of layer 13 (closer to layer 14) and which project to the posterior and triangularis rotundal divisions. Only the labeling of type I neurons produced the granular dendritic staining in layer 5b. An additional type of tectal neuron was also found that projected to the tectobulbar system. We then injected Phaseolus vulgaris-leucoagglutinin in the optic tract and found that the retinal axons terminating within tectal layer 5b formed narrow radial arbors (7–10 μm in diameter) that were confined to layer 5b. Based on these results, we propose that these axons are derived from a population of small retinal ganglion cells (4.5–6.0 μm in diameter) that terminate on the distal dendrites of type I neurons. This study strongly indicated the presence of a major bilateral oligosynaptic retinotectorotundal pathway arising from small retinal ganglion cells projecting to the rotundus with only a single intervening tectal neuron, the proposed type I neuron. We suggest that a similar organization of retinotectopulvinar connections exist in reptiles and in many mammals. J. Comp. Neurol. 387:449–465, 1997. © 1997 Wiley-Liss, Inc.

The avian nucleus rotundus, a nucleus that appears to be homologous to the inferior/caudal pulvinar of mammals, is the major target of an ascending retino-tecto-thalamic pathway. Further clarification of the inputs to the rotundus and their functional properties will contribute to our understanding of the fundamental role of the ascending tectal inputs to the telencephalon in all vertebrates, including mammals. We found that the rotundus contains a massive plexus of glutamic acid decarboxylase (GAD)-immunoreactive axons using antibodies against GAD. The cells within the rotundus, however, were not immunoreactive for GAD. The retrograde tracer cholera toxin B fragment was injected into the rotundus to establish the location of the afferent neurons and determine the source of the gamma aminobutyric acid (GABA) inputs into the rotundus. In addition to the recognized bilateral inputs from layer 13 of the tectum, we found intense retrograde labeling of neurons within the ipsilateral nuclei subpretectalis (SP), subpretectalis-caudalis (SPcd), interstitio-pretecto-subpretectalis (IFS), posteroventralis thalami (PV), and reticularis superior thalami (RS). All the neurons of the SP, SPcd, IFS, and PV were intensely GAD-immunoreactive. The neurons of layer 13 of the tectum were not immunoreactive for GAD. Following the destruction of the ipsilateral SP/IPS complex, we found a major reduction in the intensity of the GAD axonal immunoreactivity within the ipsilateral rotundus, but this destruction did not diminish the intensity of the GAD-immunoreactivity within the contralateral rotundus. Our studies indicated that the source of the massive GAD-immunoreactive plexus within the rotundus was from the ipsilateral SP, SPcd, IFS, and PV nuclei. These nuclei, in turn, received ipsilateral tectal input via collaterals of the neurons of layer 13 in the course of their projections upon the rotundus. We suggest that the direct bilateral tecto-rotundal projections are excitatory, whereas the indirect ipsilateral projections from the SP/IPS and PV are mainly inhibitory, possibly acting via a GABA-A receptor. (C) 1996 Wiley-Liss, Inc.

The anatomical characteristics of the avian visual system are well known. However, there are wide gaps in our knowledge with respect to the physiological characteristics of their visual system. For example, we lack both an operational identification of the different ganglion cell types present in the retinae of birds, and a description of their presumptive differential central projections. The results presented here address this latter point by classifying the conduction velocity groups of fibers present in the optic tract of the pigeon. We report the existence of at least 5 groups of axons in the optic tract of the pigeon, with conduction velocities of 22-18 m/s, 12-10 m/s, 8 m/s, 6 m/s and less than 2.5 m/s. All five groups project to the tectum but only the four fastest groups project to the dorsal thalamic complex. The homologies with the populations of retinal axons found in cats are discussed.