Ursula Dicke

Extremely high-power tongue projection in plethodontid salamanders.

SUMMARY Many plethodontid salamanders project their tongues ballistically at high speed and for relatively great distances. Capturing evasive prey relies on the tongue reaching the target in minimum time, therefore it is expected that power production, or the rate of energy release, is maximized during tongue launch. We examined the dynamics of tongue projection in three genera of plethodontids (Bolitoglossa, Hydromantes and Eurycea), representing three independent evolutionary transitions to ballistic tongue projection, by using a combination of high speed imaging, kinematic and inverse dynamics analyses and electromyographic recordings from the tongue projector muscle. All three taxa require high-power output of the paired tongue projector muscles to produce the observed kinematics. Required power output peaks in Bolitoglossa at values that exceed the greatest maximum instantaneous power output of vertebrate muscle that has been reported by more than an order of magnitude. The high-power requirements are likely produced through the elastic storage and recovery of muscular kinetic energy. Tongue projector muscle activity precedes the departure of the tongue from the mouth by an average of 117 ms in Bolitoglossa, sufficient time to load the collagenous aponeuroses within the projector muscle with potential energy that is subsequently released at a faster rate during tongue launch.

Dorsal striatopallidal system in anurans

The dorsal striatopallidal system of tetrapods consists of the dorsal striatum (caudate‐putamen in mammals) and the dorsal pallidum. Although the existence of striatal and pallidal structures has been well documented in anuran amphibians, the exact boundaries of these structures have so far been a matter of debate. To delineate precisely the dorsal striatopallidal system of anurans, we used quantitative analysis of leucine‐enkephalin immunohistochemistry (in Bombina orientalis, Discoglossus pictus, Xenopus laevis, and Hyla versicolor), retrograde neurobiotin tracing studies (injections in the central and ventromedial thalamic nuclei in H. versicolor), and double‐labeling tracing studies (injections in the lateral forebrain bundle and the caudal striatum in B. orientalis). Immunohistochemistry revealed that enkephalin‐positive neurons are located mainly in the rostral and intermediate striatum. Neurobiotin tracing studies demonstrated that neurons projecting to the central and ventromedial thalamic nuclei are found in the intermediate and caudal striatum. Double‐labeling studies revealed that the population of neurons in the rostral and intermediate striatum innervating the caudal striatum is separated from neurons projecting into the lateral forebrain bundle. Neurons that project to both the caudal striatum and the lateral forebrain bundle are found only in the dorsal part of the intermediate striatum. Taken together, our results suggest that the rostral striatum of anurans is homologous to the striatum proper of mammals, whereas the caudal striatum is comparable to the dorsal pallidum. The intermediate striatum represents a transition area between the two structures. J. Comp. Neurol. 468:299–310, 2004.

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. J. Comp. Neurol. 461:91–110, 2003.

How do Ontogeny, Morphology, and Physiology of Sensory Systems Constrain and Direct the Evolution of Amphibians?

The evolutionary success of extant amphibians is accompanied by secondary simplification of sense organs and of the nervous system. Strong morphological reduction is found in the lateral line system and in the auditory and visual systems. Canal neuromasts are absent; additional loss of epidermal neuromasts and ampullary organs generally corresponds to terrestrial life. Reduction of the auditory system of some anurans and of many salamanders and caecilians affects middle and inner ear structures as well as central auditory structures. The visual system of caecilians and salamanders is strongly reduced with respect to the number and morphology of retinal ganglion cells and the morphological differentiation of central visual areas, particularly the tectum opticum. The extremes of secondary simplification are found in the salamanders of the plethodontid tribe Bolitoglossini. At the same time, these salamanders are one of the most successful groups of amphibians, and they possess the most derived feeding system and a variety of specializations of the visual system. In amphibians, there is a close correspondence between the degree of secondary simplification on the one hand and genome size (DNA content) and cell size on the other. We hypothesize that this process is the major cause of the observed secondary simplification.

Neuronal factors determining high intelligence.

Many attempts have been made to correlate degrees of both animal and human intelligence with brain properties. With respect to mammals, a much-discussed trait concerns absolute and relative brain size, either uncorrected or corrected for body size. However, the correlation of both with degrees of intelligence yields large inconsistencies, because although they are regarded as the most intelligent mammals, monkeys and apes, including humans, have neither the absolutely nor the relatively largest brains. The best fit between brain traits and degrees of intelligence among mammals is reached by a combination of the number of cortical neurons, neuron packing density, interneuronal distance and axonal conduction velocity—factors that determine general information processing capacity (IPC), as reflected by general intelligence. The highest IPC is found in humans, followed by the great apes, Old World and New World monkeys. The IPC of cetaceans and elephants is much lower because of a thin cortex, low neuron packing density and low axonal conduction velocity. By contrast, corvid and psittacid birds have very small and densely packed pallial neurons and relatively many neurons, which, despite very small brain volumes, might explain their high intelligence. The evolution of a syntactical and grammatical language in humans most probably has served as an additional intelligence amplifier, which may have happened in songbirds and psittacids in a convergent manner.

Morphology, axonal projection pattern, and response types of tectal neurons in plethodontid salamanders. II: Intracellular recording and labeling experiments

In the plethodontid salamanders Plethodon jordani and P. glutinosus, the morphology and axonal projections of 140 tectal neurons and their responses to electrical optic nerve stimulation were determined by intracellular recording and biocytin labeling. Six types of neurons are distinguished morphologically. TO1 neurons have wide dendritic trees that arborize mainly in tectal layers 1 and 3; they project bilaterally to the tegmentum and contralaterally to the medulla oblongata. TO2 neurons have very wide dendritic trees that arborize mainly in layers 2 and 3; axons project bilaterally or unilaterally to the pretectum and thalamus and ipsilaterally to the medulla oblongata. TO3 neurons have very wide and flat dendritic trees confined to layers 3–5; some have the same axonal projection as TO2 neurons, whereas others have descending axons that reach only the level of the cerebellum. TO4 neurons have narrower dendritic trees that arborize in layers 2 and 3; they project to the ipsilateral pretectum, thalamus, and medulla oblongata. TO5 neurons have dendritic trees that arborize in layers 1 and 2 or 1–3 and project bilaterally or unilaterally to the pretectum and thalamus. TO‐IN are interneurons, with a number of subtypes with respect to variations in dendritic arborization pattern. TO1–TO5 neurons generally have short latencies of 2–16 ms (average = 8.4 ms) at electrical optic nerve stimulation; first responses are always excitatory, often followed by inhibition. They are likely to be mono‐ or oligosynaptically driven by retinal afferents. TO‐IN interneurons have long latencies of 20–80 ms (average = 38.6 ms) and appear to receive no direct retinal input. With their specific dendritic arborization, consequent dominant retinal input, specific axonal projections, the different types of tectal projection neurons constitute separate ascending and descending visual pathways. Hypotheses are presented regarding the nature of the information processed by these pathways. J. Comp. Neurol. 404:489–504, 1999.

5-HT-like immunoreactivity in the brains of plethodontid and salamandrid salamanders (Hydromantes italicus, Hydromantes genei, Plethodon jordani, Desmognathus ochrophaeus, Pleurodeles waltl): an immunohistochemical and biocytin double-labelling study

Abstract.The distribution of 5-HT-like-immunoreactive cell bodies and fibres was studied in the brains of the salamanders Hydromantes italicus, H. genei, Plethodon jordani, Desmognathus ochrophaeus (family Plethodontidae), and Pleurodeles waltl (family Salamandridae). In addition, double-labelling experiments with biocytin were carried out to identify the relationship between serotonergic fibres and neurons involved in the processing of sensory and sensorimotor information. In all species, 5-HT-immunopositive somata are found in the ventral thalamus close to the ventricle forming the paraventricular organ. In the hypothalamus, cells are labelled in the ependymal layer around the infundibular recess and at the lateral edge of the periventricular grey. In the pretectum, a few immunoreactive cells are situated dorsolaterally in the grey matter. In the tegmentum and medulla oblongata, cells of the raphe nuclei are regularly distributed along the midline; labelled perikarya are occasionally found in the cervical spinal cord. 5-HT-like-immunoreactive fibres are widely distributed throughout the nervous system. Densely arborizing fibres are found in the olfactory bulb, striatum and amygdala. Distinct fibre projections extend in the ventral thalamus and tectum. Biocytin tracing of striatal and tectal projection neurons and ascending reticular neurons combined with the demonstration of 5-HT suggest that the striatum, the tectum and the ascending activating system are strongly influenced by 5-HT.

Morphology, axonal projection pattern, and response types of tectal neurons in plethodontid salamanders. I: Tracer study of projection neurons and their pathways

In three salamander species (Hydromantes italicus, H. genei, Plethodon jordani), the tectobulbospinal and tectothalamic pathways and their cells of origin were studied by means of anterograde and retrograde biocytin and tetramethylrhodamine tracing. In plethodontid salamanders, five types of tectal projection neurons were identified. TO1 neurons have widefield dendritic trees that arborize in the layers of retinal afferents and form a neuropil in the superficial layer; axons constitute the crossed tectospinal tract. Dendrites of TO2 cells have the largest dendritic trees that arborize in the intermediate and deep layers of retinal afferents; axons constitute a lateral uncrossed tectospinal tract. TO3 cells have widefield dendritic trees that arborize in the deep layer of retinal afferents and in the layer of tectal efferents; axons constitute a superficial uncrossed tectospinal tract. TO4 cells have slender primary dendrites and small‐field dendritic trees that arborize in the intermediate layers of retinal afferents; axons constitute another lateral uncrossed tectospinal tract. TO2, TO3, and TO4 cells also have ascending axons that run to the ventral and dorsal thalamus. TO5 cells have slender primary dendrites and small‐field dendritic trees that extend into the superficial layers of retinal afferents; their fine axons constitute the bulk of the pathways ascending to the ipsilateral and contralateral thalamus. These morphological types of projection neurons and their ascending and descending axonal pathways closely resemble those found in frogs, reptiles, and birds. Their role in visual and visuomotor functions is discussed. J. Comp. Neurol. 404:473–488, 1999. 

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. J. Comp. Neurol. 508:806–823, 2008.

Activation patterns of the tongue-projector muscle during feeding in the imperial cave salamander Hydromantes imperialis.

SUMMARY Salamanders of the genus Hydromantes project their tongues the greatest distance of any amphibian to capture prey, up to 80% of body length or approximately 6 cm in an adult individual. During tongue projection on distant prey, the tongue is shot ballistically and the tongue skeleton leaves the body of the salamander entirely. We investigated an aspect of the motor control of this remarkable behavior by examining electromyographic patterns within different regions of the tongue-projector muscle, the subarcualis rectus (SAR). SAR activation is strongly modulated, and features of this modulation can be predicted by tongue-projection distance (i.e. prey distance). The strap-like buccal portion of the SAR is always activated first and for the longest duration, compared to any other region. It is in a position to transmit force generated by the posterior SAR to the floor of the mouth, where it originates. The posterior SAR encompasses and applies force to the epibranchial of the tongue skeleton, and its activation pattern gradually changes from a posterior-to-anterior wave of activation onset during short-distance projection to an all-at-once pattern during the most extreme long-distance (ballistic) projection. The duration of activity and EMG area of each recorded region of the SAR increase with increasing prey distance, showing greater muscle recruitment during long-distance projection. No effect of prey-capture success was observed in the EMG patterns, indicating that SAR activation is controlled in a feed-forward manner.