András Csillag

Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei

The standard nomenclature that has been used for many telencephalic and related brainstem structures in birds is based on flawed assumptions of homology to mammals. In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is neurochemically, hodologically, and functionally comparable to the mammalian neocortex, claustrum, and pallial amygdala (all of which derive from the pallial sector of the developing telencephalon). Recognizing that this promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains, avian brain specialists began discussions to rectify this problem, culminating in the Avian Brain Nomenclature Forum held at Duke University in July 2002, which approved a new terminology for avian telencephalon and some allied brainstem cell groups. Details of this new terminology are presented here, as is a rationale for each name change and evidence for any homologies implied by the new names.

Avian brains and a new understanding of vertebrate brain evolution

We believe that names have a powerful influence on the experiments we do and the way in which we think. For this reason, and in the light of new evidence about the function and evolution of the vertebrate brain, an international consortium of neuroscientists has reconsidered the traditional, 100-year-old terminology that is used to describe the avian cerebrum. Our current understanding of the avian brain — in particular the neocortex-like cognitive functions of the avian pallium — requires a new terminology that better reflects these functions and the homologies between avian and mammalian brains.

Passive avoidance training results in lasting changes in deoxyglucose metabolism in left hemisphere regions of chick brain.

Day-old chicks peck when offered a bright bead; if the bead is coated with the bitter-tasting methylanthranilate (M) they avoid it thereafter. 2-[14C] Deoxyglucose injected 1 min prior to training shows increased uptake into the hyperstriatum ventrale (HV) and lobus parolfactorius (LPO) 30 min later compared with control birds which have pecked a water-coated bead (W). To distinguish effects of training from those of consolidation, and to study lateralization of the increased uptake, 2-[14C]deoxyglucose (4 muCi) was injected ip either 5 min before, or 10 or 30 min after training. Thirty minutes after injection, bilateral samples of medial hyperstriatum ventrale (MHV), LPO and palaeostriatum augmentatum (PA)-enriched regions were dissected. Specific radioactivity (dmp/mg X prot) in left and right MHV and left and right LPO was standardized on the mean PA-specific radioactivity for each bird. When 2-DG was injected 5 min prior to training, standardized radioactivity in the left LPO was 26% greater, and in the left MHV 13% greater in M than W birds. There were no differences in the right hemisphere. With injection 10 min after training, there was an increase of 22% in the left LPO of M birds over W, of 29% in the left MHV and 22% in the right MHV. If injection was delayed to 30 min after training, there was no increase in the LPO, but a 13% increase persisted in the left MHV. Enhanced 2DG metabolism following passive avoidance training is thus persistent, lateralized, and, in the MHV at least may represent an aspect of cellular reorganization consequent on experience but independent of the immediate concomitants of training--perhaps part of the process of memory consolidation.

Evidence for a role of GABA interneurones in the cortical modulation of midbrain 5-hydroxytryptamine neurones

Recent electrophysiological studies demonstrate that the ventral medial prefrontal cortex has a powerful inhibitory influence on 5-hydroxytryptamine (5-HT) neurones in the dorsal raphe nucleus. Here we utilised a combination of anatomical and electrophysiological methods to characterise the cellular substrate underlying this effect.Anterograde tracing (Phaseolus vulgaris leucoagglutinin) using electron microscopy demonstrated a pathway from the ventral medial prefrontal cortex that makes neuronal contacts throughout the dorsal raphe nucleus. These contacts were predominantly asymmetrical synapses adjoining GABA immunoreactive dendrites and spines. In vivo extracellular recordings were made in the dorsal raphe nucleus of the anaesthetised rat from a subpopulation of non-5-HT neurones. These neurones were fast-firing, irregular and with short spike width, properties strongly reminiscent of immunochemically identified GABA interneurones in other brain regions. Recordings of classical 5-HT neurones were also included. Electrical stimulation of the ventral medial prefrontal cortex elicited a rapid onset (16 ms latency), orthodromic excitation of the non-5-HT neurones (13/25 neurones). This stimulation also caused a pronounced inhibition of most 5-HT neurones tested, with a longer latency (30 ms), and this was partially blocked by locally applied bicuculline. These data provide the first evidence that the ventral medial prefrontal cortex influences the activity of large numbers of raphe 5-HT neurones by targeting a local network of GABA neurones. This circuitry predicts that physiological and pathological changes in the ventral medial prefrontal cortex will impact on significant parts of the forebrain 5-HT system.

Efferent connections of the domestic chick archistriatum: A phaseolus lectin anterograde tracing study

The archistriatum of the domestic chick has been implicated in both fear behaviour and learning. However, relatively little is known about its organisation. The efferent connections of discrete anatomical regions of the chick archistriatum were therefore investigated by iontophoresis of the anterograde tracer Phaseolus vulgaris leucoagglutinin into its anterior, dorsal intermediate, ventral intermediate, medial, and posterior parts. The results of this study suggest that the chick archistriatum can be divided into two basic divisions according to whether they project to the following limbic structures: the hippocampal formation, septal areas, lobus parolfactorius, nucleus accumbens, ventral paleostriatum, and dorsomedial thalamus. The limbic archistriatum includes the posterior archistriatum and extends rostrally through the ventral intermediate archistriatum into the anterior archistriatum. The non‐limbic archistriatum comprises the dorsal intermediate and medial archistriatum and largely gives rise to specific sensory, somatosensory, and motor telencephalofugal efferents. There may not be distinct borders between these two divisions of the chick archistriatum. J. Comp. Neurol. 389:679–693, 1997.

Striato-telencephalic and striato-tegmental circuits: relevance to learning in domestic chicks.

Memory formation for a passive avoidance task in the domestic chick is likely to involve a hyperstriatum ventrale (IMHV)-archistriatum-lobus parolfactorius (LPO) arc. The present study summarises previous findings, relevant to this neural system, and is also supplemented with some recent data from our laboratory. Projections from the IMHV on the archistriatum, as well as from the archistriatum on the LPO, have been characterised using a combination of anterograde pathway tracing (Phaseolus lectin), and post-embedding GABA and glutamate immunocytochemistry. The majority of IMHV efferents have been found to synapse with dendritic spine heads and necks of densely spiny projection neurons of the ventral archistriatum, and the ultrastructure of synapses suggested a potent excitatory input. Similar synaptic connections of the excitatory type were ultrastructurally verified between ventral archistriatal afferent terminals and dendrites or spines of the LPO, suggesting an involvement of the medium sized spiny neurons, which are typical of the striatum. Although some of the IMHV boutons terminating in the archistriatum were immunoreactive to glutamate, this was not observed in the archistriatal-LPO pathway. Tegmental connections of the basal ganglia, in particular LPO, are also likely to play a role in processing of the avoidance response. We have demonstrated reciprocal connections between the LPO and dopaminergic (TH-positive) neurons of the substantia nigra and ventral tegmentum. Dopamine D1 receptors were upregulated bilaterally in the LPO following avoidance learning and this response was not accompanied by significant changes in the level of dopamine or its metabolites (HVA, DOPAC), as revealed by HPLC chromatography of brain samples dissected from the LPO of control and trained chicks. The dopamine receptor-related phosphoprotein DARPP-32 was localised in dendritic elements of the LPO, often forming asymmetric synapses with glutamate immunoreactive axon terminals. The findings are consistent with a scenario in which the striatum acts as a suppressor of natural pecking behaviour. Learned visual association with the target (bead) occurs in the IMHV and is relayed to the basal ganglia via the limbic archistriatum (amygdala equivalent), the latter introducing a motivational element (aversion, fear). Suppression of a brainstem pecking centre is likely to involve activation of the nigrostriatal (tegmentostriatal) dopaminergic circuit.

Radial glia in the developing mouse cerebral cortex and hippocampus.

SummaryThe regional distribution of radial glia in the developing cerebral cortex and the hippocampus of the mouse was studied using silver impregnation and immunocytochemical staining for glial fibrillary acidic protein (GFAP). Whilst the former technique revealed radial fibres at a slightly earlier age, immunocytochemistry gave a better picture of their general distribution and enabled systematic study of the appearance and disappearance of GFAP-positive radial glia throughout the cortex. Although a clear association between migrating neurones and radial glia was evident in the later stages of cortical plate formation, this relationship was not apparent in all cortical regions nor at the very early stages of the formation of the cortical plate. Even after allowing for a delayed appearance of GFAP immunoreactivity in relatively mature radial glia, the uneven distribution of these cells, their appearance after the cortical plate has already been formed, and their regional development in a pattern dissynchronous with that of the cortical plate argue against a general role of these structures in neuronal migration in the mouse, although there are notable phylogenetic differences.

The involvement of dopamine in the striatum in passive avoidance training in the chick

Quantitative receptor autoradiography was used to investigate the distribution of binding of [3H]SCH 23390 to dopamine (D1) and [3H]spiroperone to D2 receptors in regions of the forebrain of the one-day-old domestic chick (Gallus domesticus). High levels of specific binding of the D1 and D2 ligands were found in the striatal regions (paleostriatum augmentatum and lobus parolfactorius) of the one-day-old chick, as reported previously in the pigeon, turtle and rat, whilst binding levels were considerably lower in the pallidum (paleostriatum primitivum), hippocampus and hyperstriatum ventrale. The proportions of D1 and D2 receptor binding in the chick were relatively similar in the striatum and pallidum, apart from the paleostriatum augmentatum, where D2 receptors outnumber those of D1 by a factor of two. Binding of the D1 and D2 ligands to forebrain regions was also investigated 30 min after one-trial passive avoidance training of one-day-old chicks in which the aversive stimulus was a bead coated with a bitter tasting substance, methyl anthranilate. These experiments demonstrated a large and highly significant bilateral increase (compared to control birds) in binding to D1 (but not D2) receptors in the lobus parolfactorius. In this striatal region, equivalent to the caudate-putamen of mammals, previous studies have shown that synaptic and dendritic alterations occur following avoidance training. It is concluded that alterations in dopamine binding may be involved in processes that result in modification of the pecking response in chicks after avoidance training.

Selective striatal connections of midbrain dopaminergic nuclei in the chick (Gallus domesticus)

Abstract. The avian medial striatum (lobus parolfactorius, LPO) has been considered an anatomically homogeneous region. However, recent findings have indicated that somatomotor and limbic functions may be linked to anatomically distinct units. The tracer fast blue was injected into the ventral tegmental area (AVT) or substantia nigra (SN) of 1-week-old domestic chicks, and the position of retrogradely labelled neurons was mapped in striatal subregions. In another set of experiments, fast blue and red microspheres were injected into the SN and AVT, and the number and position of single- and double-labelled neurons were established. Conversely, the anterograde tracer biotinylated dextran amine was injected into different subregions of the striatum, and the position of labelled fibres and terminal fields was charted in the mesencephalic tegmentum. The neurons projecting to the SN or AVT considerably overlap in the viscerolimbic parts of the striatum, namely the medial and dorsal LPO, nucleus accumbens (Ac), tuberculum olfactorium, bed nucleus of the stria terminalis and ventral paleostriatum. Exclusive striatonigral afferents arise from the paleostriatum augmentatum and paleostriatum primitivum. Of all labelled striatal neurons, 0.22% were double-labelled from both the AVT and the SN. Thus, the AVT and SN are innervated from distinct and partially overlapping subregions of the striatum. At the cellular level, however, striatonigral and striatoventrotegmental neurons represent separate neuronal populations, even in overlapping regions. Given the arrangement of striatoventrotegmental neurons, the Ac probably does not have a distinct boundary with the LPO but extends into the anatomically defined LPO, colocalizing with medial striatal neurons.

Alterations in synaptic structure in the paleostriatal complex of the domestic chick,Gallus domesticus, following passive avoidance training

A morphometric study was made of synapses in both left and right hemispheres of two regions of the chick paleostriatal complex, the paleostriatum augmentatum (PA) and the lobus parolfactorius (LPO), 24 h after passive avoidance training (methyl anthranilate, M-chicks), and in water-trained controls (W-chicks). The synaptic features examined were D, the mean length of the postsynaptic thickening; Nv.syn, the numerical density of synapses; Vv.syn, the volume density of the presynaptic bouton; V, the mean volume of the presynaptic bouton; Nv.ves, the numerical density of synaptic vesicles per bouton volume; ves.syn, the number of synaptic vesicles per presynaptic bouton; and K, the curvature of the synaptic contact zone. In the LPO there is a significant increase in the numerical density of synapses (Nv.syn) in both left and right hemispheres of M-compared with W-chicks (up to 59%, depending on the method of calculation used). A hemispheric asymmetry of postsynaptic thickening length (D) which is present in W-chicks (R greater than L by 10%) is reversed in M-chicks. There is no difference in the volume density of the presynaptic bouton (Vv.syn) or the mean bouton volume (V) either between W- and M-chicks, or between left and right hemispheres. Significant changes are found after avoidance training in both of the synaptic vesicle parameters measured. There is an increase of approximately 50%, both in the numerical density of synaptic vesicles (Nv.ves) and the number of vesicles per synaptic bouton (ves.syn), in the left hemisphere of M-chicks. No changes in the mean synaptic contact curvature (K) were observed after training, either of presynaptically concave, or presynaptically convex synapses, in either left or right hemispheres, nor did the percentage distribution of these different curvature classes vary greatly. In the PA there were no significant changes in D, Nv.syn or Vv.syn, either between M- and W-chicks, or between left and right hemispheres, 24 h after passive avoidance training. However, when the differences between the mean bouton volume (V) are examined, there is a significant increase in size of the boutons in the left hemisphere of M- compared to W-chicks. There is also a hemispheric asymmetry in both Nv.ves and ves.syn in W-chicks (R greater than L by approximately 15%) and this disappears on M-training. No changes in the mean synaptic contact curvature were observed after training, either of presynaptically concave, or presynaptically convex synapses, in either left or right hemispheres. However, the percentage distribution of these different curvature classes showed some variation.(ABSTRACT TRUNCATED AT 400 WORDS)