The evolutionary consequences of epigenesis and neutral change: A conceptual approach at the organismal level.

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.

Can social behaviour drive accessory olfactory bulb asymmetries? Sister species of caviomorph rodents as a case in point.

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.

Anatomical Specializations Related to Foraging in the Visual System of a Nocturnal Insectivorous Bird, the Band-Winged Nightjar (Aves: Caprimulgiformes).

Nocturnal animals that rely on their visual system for foraging, mating, and navigation usually exhibit specific traits associated with living in scotopic conditions. Most nocturnal birds have several visual specializations, such as enlarged eyes and an increased orbital convergence. However, the actual role of binocular vision in nocturnal foraging is still debated. Nightjars (Aves: Caprimulgidae) are predators that actively pursue and capture flying insects in crepuscular and nocturnal environments, mainly using a conspicuous "sit-and-wait" tactic on which pursuit begins with an insect flying over the bird that sits on the ground. In this study, we describe the visual system of the band-winged nightjar (Systellura longirostris), with emphasis on anatomical features previously described as relevant for nocturnal birds. Orbit convergence, determined by 3D scanning of the skull, was 73.28°. The visual field, determined by ophthalmoscopic reflex, exhibits an area of maximum binocular overlap of 42°, and it is dorsally oriented. The eyes showed a nocturnal-like normalized corneal aperture/axial length index. Retinal ganglion cells (RGCs) were relatively scant, and distributed in an unusual oblique-band pattern, with higher concentrations in the ventrotemporal quadrant. Together, these results indicate that the band-winged nightjar exhibits a retinal specialization associated with the binocular area of their dorsal visual field, a relevant area for pursuit triggering and prey attacks. The RGC distribution observed is unusual among birds, but similar to that of some visually dependent insectivorous bats, suggesting that those features might be convergent in relation to feeding strategies.

Effects of Habitat and Social Complexity on Brain Size, Brain Asymmetry and Dentate Gyrus Morphology in Two Octodontid Rodents.

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.

Extracellular recordings reveal absence of magneto sensitive units in the avian optic tectum.

There is a consensus that birds detect the earth's magnetic field and use some of its features for orientation and homing purposes. Since the late 1960s, when the first solid behavioral evidence of magnetoreception was obtained, much research has been devoted to describing the ethological aspects of this behavior. The neurophysiological basis of magnetoreception has been much less studied, although a frequently cited 1986 report described a high prevalence (70 %) of magneto-sensitive neurons in the pigeon optic tectum with high signal-to-noise ratios (Semm and Demaine, J Comp Physiol A 159:619-625, 1986). Here, we repeated these neurophysiological experiments using anesthetized as well as awake pigeons and new recording techniques. Our data indicate that magneto-sensitive units do not exist in the avian tectum.

Early Development of the Thalamo-Pallial Stage of the Tectofugal Visual Pathway in the Chicken (Gallus gallus).

The tectofugal pathway is a highly conserved visual pathway in all amniotes. In birds and mammals, retinorecipient neurons located in the midbrain roof (optic tectum/superior colliculus) are the source of ascending projections to thalamic relays (nucleus rotundus/caudal pulvinar), which in turn project to specific pallial regions (visual dorsal ventricular ridge [vDVR]/temporal cortex) organized according to a columnar recurrent arrangement of interlaminar circuits. Whether or to which extent these striking hodological correspondences arise from comparable developmental processes is at present an open question, mainly due to the scarcity of data about the ontogeny of the avian tectofugal system. Most of the previous developmental studies of this system in birds have focused on the establishment of the retino-tecto-thalamic connectivity, overlooking the development of the thalamo-pallial-intrapallial circuit. In this work, we studied the latter in chicken embryos by means of immunohistochemical assays and precise ex vivo crystalline injections of biocytin and DiI. We found that the layered organization of the vDVR as well as the system of homotopic reciprocal connections between vDVR layers were present as early as E8. A highly organized thalamo-vDVR projection was also present at this stage. Our immunohistochemical assays suggest that both systems of projections emerge simultaneously even earlier. Combined with previous findings, these results reveal that, in striking contrast with mammals, the peripheral and central stages of the avian tectofugal pathway develop along different timelines, with a tecto-thalamo-intrapallial organization arising before and possibly independently of the retino-isthmo-tectal circuit.

Attentional capture? Synchronized feedback signals from the isthmi boost retinal signals to higher visual areas.

When a salient object in the visual field captures attention, the neural representation of that object is enhanced at the expense of competing stimuli. How neural activity evoked by a salient stimulus evolves to take precedence over the neural activity evoked by other stimuli is a matter of intensive investigation. Here, we describe in pigeons (Columba livia) how retinal inputs to the optic tectum (TeO, superior colliculus in mammals), triggered by moving stimuli, are selectively relayed on to the rotundus (Rt, caudal pulvinar) in the thalamus, and to its pallial target, the entopallium (E, extrastriate cortex). We show that two satellite nuclei of the TeO, the nucleus isthmi parvocelullaris (Ipc) and isthmi semilunaris (SLu), send synchronized feedback signals across tectal layers. Preventing the feedback from Ipc but not from SLu to a tectal location suppresses visual responses to moving stimuli from the corresponding region of visual space in all Rt subdivisions. In addition, the bursting feedback from the Ipc imprints a bursting rhythm on the visual signals, such that the visual responses of the Rt and the E acquire a bursting modulation significantly synchronized to the feedback from Ipc. As the Ipc feedback signals are selected by competitive interactions, the visual responses within the receptive fields in the Rt tend to synchronize with the tectal location receiving the "winning" feedback from Ipc. We propose that this selective transmission of afferent activity combined with the cross-regional synchronization of the areas involved represents a bottom-up mechanism by which salient stimuli capture attention.

A blinking focal pattern of re-entrant activity in the avian tectum.

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.

Envelope Analysis of the Human Alpha Rhythm Reveals EEG Gaussianity.

OBJECTIVE: To assess the Gaussianity of the human alpha rhythm using the envelope signal and the coefficient of variation of the envelope (CVE). METHODS: Envelope analysis relies on the fact that the CVE for Gaussian noise is √{(4-π)/π} ≈ 0.523. CVE can thus be used as a hallmark to detect Gaussianity, and any significant deviation from Gaussianity can be linked to synchronous neural dynamics. We applied envelope analysis to EEG and iEEG public databases. RESULTS: The human alpha rhythm can be characterized either as a synchronous or as a Gaussian signal based on the value of its CVE. Furthermore, Fourier analysis showed the canonical spectral peak at ≈ 10[Hz] is present in both the synchronous and Gaussian cases, thus demonstrating this same peak can be produced by different underlying neural dynamics. CONCLUSION: Human EEG can be classified using envelope parameters. This study confirms the original interpretation of Adrian regarding the origin of the alpha rhythm but also opens the door for the study of Gaussianity in brain dynamics. SIGNIFICANCE: Envelope analysis constitutes a novel complement to Fourier-based methods for neural signal analysis relating amplitude modulations (CVE) to signal energy. These results suggest a broader interpretation for event-related synchronization/desynchronization (ERS/ERD) may be needed.

Change in the neurochemical signature and morphological development of the parvocellular isthmic projection to the avian tectum.

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.

Shared and differential traits in the accessory olfactory bulb of caviomorph rodents with particular reference to the semiaquatic capybara.

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.

A canonical interlaminar circuit in the sensory dorsal ventricular ridge of birds: The anatomical organization of the trigeminal pallium.

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.

Intratelencephalic projections of the avian visual dorsal ventricular ridge: Laminarly segregated, reciprocally and topographically organized.

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.

A specialized reciprocal connectivity suggests a link between the mechanisms by which the superior colliculus and parabigeminal nucleus produce defensive behaviors in rodents.

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.

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia).

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.

The nucleus pretectalis principalis: A pretectal structure hidden in the mammalian thalamus.

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.

A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon.

We describe the operation of a midbrain neural circuit in pigeons that may participate in selecting and attending to one visual stimulus from the myriad displayed in their visual environment. This mechanism is based on a topographically organized cholinergic signal reentering the optic tectum (TeO). We have shown previously that, whenever a visual stimulus activates neurons in a given tectal location, this location receives a strong bursting feedback from cholinergic neurons of the nucleus isthmi pars parvocellularis (Ipc), situated underneath the tectum. Here we show that, if a second visual stimulus is presented, even far from the first, the feedback signal to the first tectal location is diminished or suppressed, and feedback to the second tectal location is initiated. We found that this long-range suppressive interaction is mostly mediated by the nucleus isthmi pars magnocellularis, which sends a wide-field GABAergic projection to Ipc and TeO. In addition, two sets of findings indicate that the feedback from the Ipc modulates the ascending output from the TeO. First, visually evoked extracellular responses recorded in the dorsal anterior subdivision of the thalamic nucleus rotundus (RtDa), receiving the ascending tectal output, are closely synchronized to this feedback signal. Second, local inactivation of the Ipc prevents visual responses in RtDa to visual targets moving in the corresponding region of visual space. These results suggest that the ascending transmission of visual activity through the tectofugal pathway is gated by this cholinergic re-entrant signal, whose location within the tectal visual map is dynamically defined by competitive interactions.

Oscillatory bursts in the optic tectum of birds represent re-entrant signals from the nucleus isthmi pars parvocellularis.

Fast oscillatory bursts (OBs; 500-600 Hz) are the most prominent response to visual stimulation in the optic tectum of birds. To investigate the neural mechanisms generating tectal OBs, we compared local recordings of OBs with simultaneous intracellular and extracellular single-unit recordings in the tectum of anesthetized pigeons. We found a specific population of units that responded with burst discharges that mirrored the burst pattern of OBs. Intracellular filling with biocytin of some of these bursting units demonstrated that they corresponded to the paintbrush axon terminals from the nucleus isthmi pars parvocellularis (Ipc). Direct recordings in the Ipc confirmed the high correlation between Ipc cell firing and tectal OBs. After injecting micro-drops of lidocaine in the Ipc, the OBs of the corresponding tectal locus disappeared completely. These results identify the paintbrush terminals as the neural elements generating tectal OBs. These terminals are presumably cholinergic and ramify across tectal layers in a columnar manner. Because the optic tectum and the Ipc are reciprocally connected such that each Ipc neuron sends a paintbrush axon to the part of the optic tectum from which its visual inputs come, tectal OBs represent re-entrant signals from the Ipc, and the spatial-temporal pattern of OBs across the tectum is the mirror representation of the spatial-temporal pattern of bursting neurons in the Ipc. We propose that an active location in the Ipc may act, via bursting paintbrushes in the tectum, as a focal "beam of attention" across tectal layers, enhancing the saliency of stimuli in the corresponding location in visual space.

Axon terminals from the nucleus isthmi pars parvocellularis control the ascending retinotectofugal output through direct synaptic contact with tectal ganglion cell dendrites.

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.

Microconnectomics of the pretectum and ventral thalamus in the chicken (Gallus gallus).

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.