Thalamo-telencephalic pathways in the fire-bellied toad Bombina orientalis

It was suggested that among extant vertebrates, anuran amphibians display a brain organization closest to the ancestral tetrapod condition, and recent research suggests that anuran brains share important similarities with the brains of amniotes. The thalamus is the major source of sensory input to the telencephalon in both amphibians and amniote vertebrates, and this sensory input is critical for higher brain functions. The present study investigated the thalamo-telencephalic pathways in the fire-bellied toad Bombina orientalis, a basal anuran, by using a combination of retrograde tract tracing and intracellular injections with the tracer biocytin. Intracellular labeling revealed that the majority of neurons in the anterior and central thalamic nuclei project to multiple brain targets involved in behavioral modulation either through axon collaterals or en passant varicosities. Single anterior thalamic neurons target multiple regions in the forebrain and midbrain. Of note, these neurons display abundant projections to the medial amygdala and a variety of pallial areas, predominantly the anterior medial pallium. In Bombina, telencephalic projections of central thalamic neurons are restricted to the dorsal striato-pallidum. The bed nucleus of the pallial commissure/thalamic eminence similarly targets multiple brain regions including the ventral medial pallium, but this is accomplished through a higher variety of distinct neuron types. We propose that the amphibian diencephalon exerts widespread influence in brain regions involved in behavioral modulation and that a single dorsal thalamic neuron is in a position to integrate different sensory channels and distribute the resulting information to multiple brain regions.     

Organization of the sensory input to the telencephalon in the fire-bellied toad, Bombina orientalis

The functional organization of sensory activity in the amphibian telencephalon is poorly understood. We used an in vitro brain preparation to compare the anatomy of afferent pathways with the localization of electrically evoked sensory potentials and single neuron intracellular responses in the telencephalon of the toad Bombina orientalis. Anatomical tracing showed that the anterior thalamic nucleus innervates the anterior parts of the medial, dorsal, and lateral pallia and the rostralmost part of the pallium in addition to the subpallial amygdala/ventral pallidum region. Additional afferents to the medial telencephalon originate from the thalamic eminence. Electrical stimulation of diverse sensory nerves and brain regions generated evoked potentials with distinct characteristics in the pallium, subpallial amygdala/ventral pallidum, and dorsal striatopallidum. In the pallium, this sensory activity is generated in the anterior medial region. In the case of olfaction, evoked potentials were recorded at all sites, but displayed different characteristics across telencephalic regions. Stimulation of the anterior dorsal thalamus generated a pattern of activity comparable to olfactory evoked potentials, but it became similar to stimulation of the optic nerve or brainstem after bilateral lesion of the lateral olfactory tract, which interrupted the antidromic activation of the olfactohabenular tract. Intracellular bimodal sensory responses were obtained in the anterior pallium, medial amygdala, ventral pallidum, and dorsal striatopallidum. Our results demonstrate that the amphibian anterior pallium, medial amygdala/ventral pallidum, and dorsal striatopallidum are multimodal sensory centers. The organization of the amphibian telencephalon displays striking similarities with the brain pathways recently implicated in mammalian goal-directed behavior.     

Morphology,axonal projection pattern,and responses to optic nerve stimulation of thalamic neurons in the fire-bellied toad Bombina orientalis

Intracellular recording and biocytin labeling were carried out in the fire-bellied toad Bombina orientalis to study the morphology and axonal projections of thalamic (TH) neurons and their responses to electrical optic nerve stimulation. Labeled neurons (n = 142) were divided into the following groups: TH1 neurons projecting to the dorsal striatum; TH2 neurons projecting to the amygdala, nucleus accumbens, and septal nuclei; TH3 neurons projecting to the medial or dorsal pallium; TH4 neurons with projections ascending to the dorsal striatum or ventral striatum/amygdala and descending to the optic tectum, tegmentum, and rostral medulla oblongata; TH5 neurons with projections to the tegmentum, rostral medulla oblongata, prectectum, or tectum; and TH6 neurons projecting to the hypothalamus. TH1 neurons are found in the central, TH2 neurons in the anterior and central, TH3 neurons in the anterior dorsal nucleus, and TH4 and TH5 neurons in the posterior dorsal or ventral nucleus. Neurons with descending projections arborize in restricted parts of retinal afferents; neurons with ascending projections do not substantially arborize within retinal afferents. At electrical optic nerve stimulation, neurons in the ventral thalamus respond with excitation at latencies of 10.8 msec; one-third of them follow repetitive stimulation and possibly are monosynaptically driven. Neurons in the dorsal thalamus respond mostly with inhibition at latencies of 42.3 msec and are polysynaptically driven. This corroborates the view that neurons in the dorsal thalamus projecting to the telencephalon receive no substantial direct retinal input and that the thalamopallial pathway of amphibians is not homologous to the mammalian retinogeniculocortical pathway.     

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

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

Morphology and axonal projection pattern of neurons in the telencephalon of the fire-bellied toad Bombina orientalis: an anterograde, retrograde, and intracellular biocytin labeling study

The connectivity and cytoarchitecture of telencephalic centers except dorsal and medial pallium were studied in the fire-bellied toad Bombina orientalis by anterograde and retrograde biocytin labeling and intracellular biocytin injection (total of 148 intracellularly labeled neurons or neuron clusters). Our findings suggest the following telencephalic divisions: (1) a central amygdala-bed nucleus of the stria terminalis in the caudal midventral telencephalon, connected to visceral-autonomic centers; (2) a vomeronasal amygdala in the caudolateral ventral telencephalon receiving input from the accessory olfactory bulb and projecting mainly to the preoptic region/hypothalamus; (3) an olfactory amygdala in the caudal pole of the telencephalon lateral to the vomeronasal amygdala receiving input from the main olfactory bulb and projecting to the hypothalamus; (4) a medial amygdala receiving input from the anterior dorsal thalamus and projecting to the medial pallium, septum, and hypothalamus; (5) a ventromedial column formed by a nucleus accumbens and a ventral pallidum projecting to the central amygdala, hypothalamus, and posterior tubercle; (6) a lateral column constituting the dorsal striatum proper rostrally and the dorsal pallidum caudally, and a ventrolateral column constituting the ventral striatum. We conclude that the caudal mediolateral complex consisting of the extended central, vomeronasal, and olfactory amygdala of anurans represents the ancestral condition of the amygdaloid complex. During the evolution of the mammalian telencephalon this complex was shifted medially and involuted. The mammalian basolateral amygdala apparently is an evolutionary new structure, but the medial portion of the amygdalar complex of anurans reveals similarities in input and output with this structure and may serve similar functions.     

Connectivity and cytoarchitecture of the ventral telencephalon in the salamander Plethodon shermani

The cytoarchitecture and axonal connection pattern of centers in the ventral telencephalon of the salamander Plethodon shermani were studied using biocytin for anterograde and retrograde labeling of cell groups, as well as by intracellular injections. Application of biocytin to the main and accessory olfactory bulbs identified the olfactory pallial regions and the vomeronasal portion of the amygdala, respectively. According to our results, the amygdala of Plethodon is divided into (1) a rostral part projecting to visceral and limbic centers and receiving afferents from the dorsal thalamus, and (2) a caudal part receiving accessory olfactory input. The striatopallial transition area (SPTA) lies rostrodorsally to the caudal (vomeronasal) amygdala and is similar in connections and possibly in function. The rostral striatum has few descending projections to the medulla, whereas the intermediate striatum sends strong projections to the tegmentum and medulla. The caudal striatum has strong ascending projections to the striatum and descending projections to the ventral hypothalamus. The dendritic trees of neurons labeled below the striatum and in the SPTA spread laterally from the soma, whereas dendrites of striatal neurons converge into the laterally situated striatal neuropil. In the caudal amygdala, three distinct types of neurons are found differing in dendritic arborization. It is concluded that, hodologically, the rostral part of the urodele amygdala corresponds to the central and basolateral amygdala and the caudal part to the cortical/medial amygdala of mammals. The urodele striatum is divided into a rostral striatum proper, an intermediate dorsal pallidum, and a caudal part, with distinct connections described here for the first time in a vertebrate.     

Evolution of air-borne vocalization: Insights from neural studies in the archeobatrachian species Bombina orientalis

Vocalization of tetrapods evolved as an air-driven mechanism. Thus, it is conceivable that the underlaying neural network might have evolved from more ancient respiratory circuits and be made up of homologous components that generate breathing rhythms across vertebrates. In this context, the extant species of stem anurans provide an opportunity to analyze the connection of the neural circuits of lung ventilation and vocalization. Here, we analyzed the fictive lung ventilation and vocalization behavior of isolated brains of the Chinese fire-bellied toad Bombina orientalis during their mating season by nerve root recordings. We discovered significant differences in durations of activation of male brains after stimulation of the statoacoustic nerve or vocalization-relevant forebrain structures in comparison to female brains. The increased durations of motor nerve activities in male brains can be interpreted as fictive calling, as male's advertisement calls in vivo had the same general pattern compared to lung ventilation, but longer duration periods. Female brains react to the corresponding stimulations with the same shorter activity pattern that occurred spontaneously in both female and male brains and thus can be interpreted as fictive lung ventilations. These results support the hypothesis that vocal circuits evolved from ancient respiration networks in the anuran caudal hindbrain. Moreover, we could show that the terrestrial stem archeobatrachian Bombina spec. is an appropriate model to study the function and evolution of the shared network of lung ventilation and vocal generation.     

Connections of the mesencephalic, thalamic and telencephalic auditory centers in turtles. Some structural bases for audiosomatic interrelations

The organization of auditory projections at the mesencephalic, thalamic and telencephalic brain levels was studied utilizing the method of horseradish peroxidase (HRP) transport in two species of the turtle--Emys orbicularis and Testudo horsfieldi. It was shown that the torus semicircularis receives bilateral afferents from the brain stem auditory centers. They arise predominantly from the contralateral cochlear nuclei, the ipsilateral superior olive, the dorsal and ventral nuclei of the lateral lemniscus and from the symmetrical torus semicircularis. These connections appear to be reciprocal. After the enzyme injections correspondingly into the torus semicircularis and n. reuniens anterograde and retrograde HRP transports show that the central nucleus of the torus semicircularis projects to n. reuniens throughout its rostro-caudal extent mainly ipsilaterally. In turn, n. reuniens projects to the medioventral part of the dorsal ventricular ridge. A following common principle of the organization of the auditory system was revealed at the three brain levels explored. Auditory relay centers occupy the most medial positions at every level (n. centralis of the torus semicircularis, n. reuniens, the medioventral part of the dorsal ventricular ridge). Immediately lateral to them are somatic centers (correspondingly, n. intercollicularis, n. ventralis, the central part of the dorsal ventricular ridge). These together with the auditory centers form united functional complexes at every level. In these complexes auditory and somatic projections overlap, thus constituting a basis for the interaction between auditory and somatic afferent inputs. Mesencephalic and thalamic auditory centers were shown to receive direct somatic (cervical spinal) projections and non-direct from the underlying somatic center as well as from the adjacent somatic center at the same level (n. intercollicularis in the mesencephalon, n. ventralis in the thalamus). Somatic centers in the complexes described get no direct auditory projections. Auditory impulses however can enter them via two pathways: along neuron axons from the neighbouring auditory center reaching the adjacent somatic center and along somatic neuron dendrites which pass into the adjacent auditory center. The morphological basis for the auditory-somatic interactions primarily in the auditory center and also in the somatic center was demonstrated in Golgi-like HRP labeled and Golgi-impregnated neurons of these centers. The organization of the auditory-somatic projections at the three brain levels in turtles in to a degree comparable to the auditory system in mammals which is structured according to the core-belt principle.(ABSTRACT TRUNCATED AT 400 WORDS)     

Neurotransmitters in the regulation of neuronal cytoarchitecture

Recent experiments in isolated neurons in cell culture have demonstrated that neurotransmitters and associated electrical activity can directly affect neurite outgrowth. The results indicate that neurotransmitters have considerable potential to control the development of the neuronal circuits in which they participate in information coding in the adult. Cellular mechanisms regulating growth cone motility have been found to be similar to those regulating neurotransmitter release at the synapse and involve electrical activity, calcium and other second messengers. These similarities suggest that the morphological changes in connections observed in adult plasticity may involve the transition of synaptic terminals back to a growth mode. Excitatory and inhibitory neurotransmitters can interact to yield a net effect on neuronal morphology. In the intact nervous system a balance between these neurotransmitter inputs is probably important in maintaining circuits. Studies of neurotransmitter involvement in learning and memory processes indicate that brain function can alter brain structure and that neurotransmitters may control these structural changes. The hippocampus is one brain region in which we are beginning to define roles for neurotransmitters as sculptors of neuronal cytoarchitecture. The neurotransmitter glutamate was found to specifically affect the cytoarchitecture of hippocampal pyramidal neuron dendrites in a graded manner which suggests that glutamate may be involved in: establishing hippocampal circuitry during brain development; maintaining and modifying circuitry in the adult; and inducing neurodegeneration in several disorders including epilepsy, Alzheimer's disease and stroke. Therapeutic approaches to disorders which affect brain cytoarchitecture may now be devised based upon knowledge of the neurotransmitters and their cellular mechanisms in the perinent brain region.     

Neurotransmitters in the regulation of neuronal cytoarchitecture

Recent experiments in isolated neurons in cell culture have demonstrated that neurotransmitters and associated electrical activity can directly affect neurite outgrowth. The results indicate that neurotransmitters have considerable potential to control the development of the neuronal circuits in which they participate in information coding in the adult. Cellular mechanisms regulating growth cone motility have been found to be similar to those regulating neurotransmitter release at the synapse and involve electrical activity, calcium and other second messengers. These similarities suggest that the morphological changes in connections observed in adult plasticity may involve the transition of synaptic terminals back to a growth mode. Excitatory and inhibitory neurotransmitters can interact to yield a net effect on neuronal morphology. In the intact nervous system a balance between these neurotransmitter inputs is probably important in maintaining circuits. Studies of neurotransmitter involvement in learning and memory processes indicate that brain function can alter brain structure and that neurotransmitters may control these structural changes. The hippocampus is one brain region in which we are beginning to define roles for neurotransmitters as sculptors of neuronal cytoarchitecture. The neurotransmitter glutamate was found to specifically affect the cytoarchitecture of hippocampal pyramidal neuron dendrites in a graded manner which suggests that glutamate may be involved in: establishing hippocampal circuitry during brain development; maintaining and modifying circuitry in the adult; and inducing neurodegeneration in several disorders including epilepsy, Alzheimer's disease, and stroke. Therapeutic approaches to disorders which affect brain cytoarchitecture may now be devised based upon knowledge of the neurotransmitters and their cellular mechanisms in the pertinent brain region.     

Topography and cytoarchitecture of the motor nuclei in the brainstem of salamanders

The organization of the motor nuclei of cranial nerves V (including mesencephalic nucleus), VI, VII, IX, and X is described from HRP-stained material (whole mounts and sections) for 25 species representing five families of salamanders, and the general topology of the brainstem is considered. Location and organization of the motor nuclei, cytoarchitecture of each nucleus, and target organs for nuclei and subnuclei are described. The trigeminal nucleus is separated distinctly from the facial and abducens nuclei and consists of two subnuclei. The abducens nucleus consists of two distinct subnuclei, one medial in location, the abducens proper, and the other lateral, the abducens accessorius. The facial nucleus has two subnuclei, and in all but one species it is posterior to the genu facialis. The facial nucleus completely overlaps the glossopharyngeal nucleus and partially overlaps that of the vagus. In bolitoglossine plethodontid salamanders, all of which have highly specialized projectile tongues, the glossopharyngeal and vagus nuclei have moved rostrally to overlap extensively and intermingle with the anterior and posterior subnuclei of the facial nerve. In the bolitoglossines there is less organization of the cells of the brainstem nuclei: dendritic trunks are less parallel and projection fields are wider than in other salamanders. Some aspects of function and development are discussed; comparisons are made to conditions in anurans; and phylogenetic implications are considered.     

Symptomatic cysts of the telencephalic choroid plexus

Symptomatic cysts of the telencephalic choroid plexus are rare. This is a paediatric problem, with the oldest patient being 10 years old. Pertinent cases from the literature are reviewed. The case of a 9 year old girl with suboccipital headaches made more severe by lying on her right side or on her abdomen is discussed. Physical examination was within normal limits except for evidence of early papilloedema. The cerebrospinal fluid pressure was normal, and the protein was not elevated (32 mg/100 ml.). The brain scan showed a left frontoparietal mass near the midline, and the electroencephalogram was abnormal. The pneumoencephalogram demonstrated a mobile, pedunculated mass in the left trigone which approached the foramen of Monro when the patient assumed the head-erect position. A transcallosal approach was used and the cyst was easily removed. Postoperatively the patient has done well and is currently asymptomatic and without headaches. The significance of the presenting symptoms, the cerebrospinal fluid and brain scan findings, as well as the surgical approach, are discussed.     

Morphometry of cytoarchitecture of the lateral hypothalamic area in the rat

The cytoarchitecture of the lateral hypothalamic area (LHA) in rats was studied with cresyl violet-stained coronal celloidin sections and with sections of the brain impregnated by a Golgi method. Unimodality was established in the frequency distribution histogram of both the somatic cross-sectional area of the LHA neurons and somatic shape (elongation and circularity). The predominant somatic orientation was in the dorsomedial-ventrolateral direction: bimodality of the frequency distribution of somatic orientation was denied. These findings suggest that the LHA neurons examined in the present study are not subdivisible on the basis of the somatic area, shape or orientation. Although the neurons were classified into eight types based upon the dendritic pattern, those in the LHA largely consisted of only three of them; Type III (dendrites extending in two directions along the long axis of soma), Type IV (three directions) and Type VIII (four directions) jointly accounted for 97.1 percent of the total neurons examined. This finding suggests that the parameter of dendritic pattern serves an important purpose in the typing of the rat LHA neurons. The orientation of intrinsic dendrites and intrinsic axons in the LHA has also been described.     

Neurogenesis of the magnocellular basal telencephalic nuclei in the rat

Neurogenesis in the magnocellular basal telencephalic nuclei of the rat was examined with [³H]thymidine autoradiography. The experimental animals were the offspring of pregnant females given two injections of [³H]thymidine on consecutive embryonic (E) days (E12–E13, E13–E14, … E21–E22). On postnatal day (P) 60, the percentage of labeled cells and the proportion of cells originating during 24 h periods were quantified at several anatomical levels throughout the magnocellular basal telencephalic nuclei. The neurons of the horizontal limb of the diagonal band originate mainly between E13 and E16 in a combined rostral-to-caudal and lateral-to-medial gradient. The neurogenetic gradients in the horizontal limb are continued by generation patterns of cells in the vertical limb of the diagonal band-medial septal complex, the large cells in the polymorph layer of the olfactory tubercle, and the large cells of the anterior amygdaloid area. The substantia innominata originates between E13 and E17 in combined caudal-to-rostral and lateral-to-medial gradients. The globus pallidus originates between E13 and E17 in combined caudal-to-rostral, ventral-to-dorsal and medial-to-lateral gradients. The entopeduncular nucleus originates between E12 and E14 in a ‘sandwich’ gradient where neurons in the core of the nucleus are older than those in either the anterior or posterior ends. There is an overall superficial (ventral) to deep (dorsal) neurogenetic gradient between the magnocellular basal nuclei present at any given rostrocaudal level. An important finding is that neurogenetic gradients in the individual components of the magnocellular basal nuclei are alike (with the possible exception of the entopeduncular nucleus) indicating they are part of a single system. Finally, evidence is presented that neurogenetic gradients in the magnocellular basal telencephalic neurons can be correlated with their anatomical projections to the cerebral cortex.     

3H-Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ

The birthdates of neuronal populations comprising the chick telencephalon were determined by ³H-thymidine labeling and were mapped with respect to their terminal positions in the 16-day embryo. Essentially all neurons were generated between four and nine days of embryonic development. Each telencephalic structure (based on terminology used by Karten and Hodos, '67) was characterized by a specific range of birthdates: some regions such as the core of the ectostriatum or the paleostriatum primitivum, were generated within a single day, while others, such as the hyperstriatum accessorium, required up to five days for generation of the complete population. Spatial-temporal gradients of neuronal birthdates, lateromedial and ventrodorsal, were seen in the telencephalon as a whole and within individual subcompartments as well. An “outside-in” pattern of histogenesis predominated throughout the entire telencephalon, including the dorsolateral cortex. However, notable exceptions pertaining to the paleostriatum augmentatum, hyperstriatum intercalatus and field “L” were observed. Glial cells, generated for the most part after day ten, were found to be distributed homogeneously throughout all areas of the telencephalon. These data provide the first birthdating data for an avian telencephalon and bring greater resolution to previous analyses of the histogenesis of this brain region. Further, the compartmentalization of the proliferative neuroepithelium is revealed by these data, and the possibility of a common time of origin in the neuroepithelium for neurons of related function is discussed.     

The cytoarchitecture of the human anteroventral cochlear nucleus

The cytoarchitecture of the anteroventral cochlear nucleus (Av) was studied in six human brain stems stained with cresyl violet. A compensating polar planimeter was used to measure the cross-sectional area of perikarya drawn with a camera lucida device. The majority of neurons are ovoid in shape with somewhat eccentric nuclei and moderately coarse Nissl granules which are uniformly distributed throughout the neuroplasm. On a dimensional basis, there is a single population of cells which vary in size according to a normal distribution. The average perikaryal size is 370 sq. μ (18 × 26 μ). Cellular density is greatest along the lateral margin of Av near the rostral end. Neurons of all sizes intermingle in every part of the nucleus and no circumscribed area can be characterized as containing exclusively or even predominantly neurons of any given size. The cytoarchitecture of the human anteroventral cochlear nucleus so closely resembles that of the rhesus monkey as to suggest similar fiber projections and physiological properties in both species.