The crocodylian skull and osteoderms: A functional exaptation to ectothermy?

The crocodylians are ectothermic semi-aquatic vertebrates which are assessed to have evolved from endothermic terrestrial forms during the Mesozoic. Such a physiological transition should have involved modifications in their cardio-vascular system allowing to increase the heat transfers with the surrounding environment by growing a peripheral vascularization which would be mainly located in the dermal skeleton: the dermatocranium and the osteoderms. In order to assess the implication of these anatomical regions in thermal exchanges, we have recorded the temperature above a set of representative skin areas in order to draw comparisons between the skull, the osteoderms, and the rest of the body parts which present either none or residual dermal ossification. We computed the data after the specimens were successively laid in different stereotyped environmental conditions which involved significant variations in the environmental temperature. Our results show that the osteoderms collect the external heat during the basking periods as they become significantly warmer than the surrounding skin; they further release the heat into the core of the organism as they turn out to be colder than the surrounding skin after a significant cooling period. In disregard of the environmental temperature variations, the skull table (which encloses the braincase) remains warmer than the rest of the cranial regions and shows less temperature variations than the osteoderms; a result which has lead us to think that the braincase temperature is monitored and controlled by a thermoregulatory system. Therefore, as hypothesized by previous authors regarding the ectothermic diapsids, we assume that the crocodylian skull possesses shunting blood pathways which tend to maintain both the braincase and the main sensory organs at the nearest to the optimal physiological temperature depending on the external temperature variations. Concerning the skin vascularization, the study of an albino Alligator mississippiensis specimen permitted to observe the repartition of the superficial blood vessels by transparency through the skin. We thus testify that the skin which covers either the skull or the osteoderms is more vascularized than the skin which does not present any subjacent dermal ossification. We consequently deduce that the significant contrast in the thermal behavior between the dermal skeleton and the rest of the body is indeed correlated with a difference in the relative degree of skin vascularization. This last assessment confirms that the development of the dermal skeleton should have played a functional role in the crocodylian transition from endothermy to ectothermy through the set-up of a peripheral vessel network.

Vascularization in Ornamented Osteoderms: Physiological Implications in Ectothermy and Amphibious Lifestyle in the Crocodylomorphs?

Vascularization in the core of crocodylian osteoderms, and in their superficial pits has been hypothesized to be a key feature involved in physiological thermoregulation and/or acidosis buffering during anoxia (apnea). However, up to now, there have been no quantitative data showing that the inner, or superficial, blood supply of the osteoderms is greater than that occurring in neighboring dermal tissues. We provide such data: our results clearly indicate that the vascular networks in both the osteoderms and the pits forming their superficial ornamentation are denser than in the overlying dermis. These results support previous physiological assumptions and indicate that vascularization in pseudosuchian (crocodylians and close relatives) ornamented osteoderms could be part of a broad eco-physiological adaptation towards ectothermy and aquatic ambush predation acquired by the crocodylomorphs during their post-Triassic evolution. Moreover, regressions demonstrate that the number of enclosed vessels is correlated with the sectional area of the cavities housing them (superficial pits and inner cavities). These regressions can be used to infer the degree of vascularization on dry and fossilized osteoderms and thus document the evolution of the putative function of the osteoderms in the Pseudosuchia. Anat Rec, 2017. © 2017 Wiley Periodicals, Inc. Anat Rec, 301:175-183, 2018. © 2017 Wiley Periodicals, Inc.

Do the ornamented osteoderms influence the heat conduction through the skin? A finite element analysis in Crocodylomorpha.

In order to assess the implication of the crocodylomorph ornamented osteoderms on the skin conduction during basking, we have performed three dimensional modeling and finite element analyses on a sample which includes both extant dry bones and well-preserved fossils tracing back to the Early Jurassic. In purpose to reveal the possible implication of the superficial ornamentation on the osteoderm heat conduction, we repeated the simulation on an equivalent set of smoothed 3D-modeled osteoderms. The comparison of the results evidenced that the presence of the apical sculpture has no significant impact on the osteoderm global conduction. Furthermore, as we also aimed to assess the influence of the inner bone porosity on the osteoderm conduction, we modified the heat equation parameters so that the 3D-modeled osteoderms successively score the compact and the cancellous bone properties (i.e. mass density, heat capacity, thermal conductivity and thermal diffusivity). Finally, we repeated the analyses using the soft-dermis properties which lead to outline that neither the degree of porosity nor the presence of the osteoderms (in itself) significantly modifies the heat conduction through the crocodylomorph skin. Consequently, as hypothesized by previous authors, if the dermal shield happens to be involved into heat capture during basking for crocodylians, this process must mainly rely on a convective effect based on the osteoderm relative degree of vascularization. This last assumption could thus explain why the crocodylians which produce little metabolic heat would carry an entire vascularized osteoderm shield.

Does skull morphology constrain bone ornamentation? A morphometric analysis in the Crocodylia.

Previous quantitative assessments of the crocodylians' dermal bone ornamentation (this ornamentation consists of pits and ridges) has shown that bone sculpture results in a gain in area that differs between anatomical regions: it tends to be higher on the skull table than on the snout. Therefore, a comparative phylogenetic analysis within 17 adult crocodylian specimens representative of the morphological diversity of the 24 extant species has been performed, in order to test if the gain in area due to ornamentation depends on the skull morphology, i.e. shape and size. Quantitative assessment of skull size and shape through geometric morphometrics, and of skull ornamentation through surface analyses, produced a dataset that was analyzed using phylogenetic least-squares regression. The analyses reveal that none of the variables that quantify ornamentation, be they on the snout or the skull table, is correlated with the size of the specimens. Conversely, there is more disparity in the relationships between skull conformations (longirostrine vs. brevirostrine) and ornamentation. Indeed, both parameters GApit (i.e. pit depth and shape) and OArelat (i.e. relative area of the pit set) are negatively correlated with snout elongation, whereas none of the values quantifying ornamentation on the skull table is correlated with skull conformation. It can be concluded that bone sculpture on the snout is influenced by different developmental constrains than on the skull table and is sensible to differences in the local growth 'context' (allometric processes) prevailing in distinct skull parts. Whatever the functional role of bone ornamentation on the skull, if any, it seems to be restricted to some anatomical regions at least for the longirostrine forms that tend to lose ornamentation on the snout.

Differentiation and growth of bone ornamentation in vertebrates: a comparative histological study among the Crocodylomorpha.

Bone ornamentation, that is, hollow (pits and grooves) or protruding (ridges) repetitive reliefs on the surface of dermal bones, is a frequent, though poorly studied and understood, feature in vertebrates. One of the most typical examples of this characteristic is given by the Crurotarsi, a taxon formed by the crocodilians and their closest allies, which generally display deep ornamentation on skull roof and osteoderms. However, the ontogenetic process responsible for the differentiation and development of this character remains controversial. This study was conducted to settle the question on histological and microanatomical evidence in several crurotarsan taxa. Observational and experimental data in extant and extinct crocodyliforms show that bone ornamentation is initially created, and later maintained during somatic growth (that is indefinite in crocodilians), by a complex process of bone remodeling comprising local resorption of superficial bone cortices, followed by partial reconstruction. The superficial reliefs of crocodilian dermal bones are thus permanently modified through pit enlargement, drift, stretching, shrinking, or complete filling. Ridges are also remodeled in corresponding ways. These processes allow accommodation of unitary ornamental motifs to the overall dimensions of the bones during growth. A parsimony optimization based on the results of this study, but integrating also published data on bone histology in non-crocodyliform crurotarsans and some non-crurotarsan taxa, suggests that the peculiar mechanism described above for creating and maintaining bone ornamentation is a general feature of the Crurotarsi and is quite distinct from that attributed by previous authors to other vertebrates.

Figures and Institutions of the neurological sciences in Paris from 1800 to 1950. Part IV: Psychiatry and psychology.

We present a short historical review on the major institutions and figures who contributed to make Paris a renowned centre of physiology and neurology during the XIXth and the first half of the XXth century. We purposely chose to focus on the period 1800-1950, as 1800 corresponds to the actual beginning of neurosciences, and as 1950 marks their exponential rise. Our presentation is divided into four chapters, matching the main disciplines that have progressed and contributed most to the knowledge we have of the brain sciences: anatomy, physiology, neurology, and psychiatry-psychology. The present article is the fourth of the four parts of this review, which deals with the chapter on psychiatry and psychology. When the French Revolution occurred, only a few institutions were taking care of the mentally ill. In the Paris area, these included Maison Royale de Charenton, Les Petites Maisons, and one of the departments of larger hospitals such as Hôtel-Dieu, the Salpêtrière Hospital and Bicêtre Hospital. One of the founders of psychiatry in Paris at that time and thereafter was Philippe Pinel (1745-1826) who was the first to distinguish insane/alienated patients from misfits, beggars, and other vagabonds. During the first half of the XIXth century, his student Jean-Étienne Esquirol (1772-1840) also played a major role with his treatise on mental diseases and the 1838 law and the creation of asylums in all parts of France. Alienists were in general caregivers and learned by themselves. In contrast, at the academic level, the emerging disciplines psychiatry and neurology were very close to each other in the second half of the XIXth century, the best example being Jules Baillarger (1809-1890). The actual development of psychiatry and psychology and the foundation of psychoanalysis later in the XIXth century and in the first half of the XXth century owed much to several European doctors and scientists, particularly those from British institutions and from German-speaking universities in Central Europe. In France, important advances were once again initiated in Paris by Jean-Martin Charcot (1825-1893) and some of his pupils who renewed the concept of hysteria and the use of hypnosis. Sainte-Anne Hospital was created in 1867. This new institution located in the southern part of Paris became (and is still) one of the most important places in France for the treatment, research and teaching of mental diseases. Thereafter started new disciplines such as clinical psychology and neuropsychology; the scientific basis of psychology and notably the psychopathology hypothesis were established. A major revolutionary step occurred in Paris in the early 1950s with the discovery of neuroleptics and the birth of psychopharmacology. Here we present the biographical sketches of the most important Parisian scientists of these disciplines from that era, Philippe Pinel, Jean-Étienne Esquirol, Théodule Armand Ribot, Pierre Janet, Henri Louis Charles Piéron, Henry Ey, Jean Delay, Henri Laborit and Henri Hécaen.

Figures and institutions of the neurological sciences in Paris from 1800 to 1950. Part III: neurology.

We present a short historical review of the major figures, their administrative functions and their works that contributed to make Paris a renowned centre of physiology and neurology during the xixth and the first half of the xxth century. We purposely chose to focus on the period 1800-1950, as 1800 corresponds to the actual beginning of neurosciences, and 1950 marks their exponential rise. Our presentation is divided into four chapters, matching the main disciplines which have progressed and contributed the most to the knowledge we have of the brain sciences: anatomy, physiology, neurology, and psychiatry-psychology. The present article is the third of four parts of this review, and deals with neurology. A special credit should be given to Jean-Martin Charcot who founded the Salpêtrière School of neurology and became one of the world's most important neurologists of the xixth century. We provide below the biographical sketches of Armand Trousseau, Guillaume Benjamin Amand Duchenne, Jean-Martin Charcot, Alfred Vulpian, Désiré-Magloire Bourneville, Paul Richer, Henri Parinaud, Albert Pitres, Jules Joseph Dejerine, Mrs. Augusta Dejerine-Klumpke, Édouard Brissaud, Pierre Marie, Georges Édouard Brutus Gilles de la Tourette, Joseph Babinski, André Thomas, Georges Marinesco, Achille Alexandre Souques, Georges Guillain and Charles Foix.

Figures and institutions of the neurological sciences in Paris from 1800 to 1950. Part II: Neurophysiology.

We present a short historical review of the major figures and institutions that contributed to make Paris a renowned centre of physiology and neurology during the xixth and the first half of the xxth century. We purposely chose to focus on the period 1800-1950, as 1800 corresponds to the actual beginning of experimental physiology of the nervous system - what is here referred to as "neuroscience"-and 1950 marks its exponential rise. Our presentation is divided into four chapters, matching the main disciplines which have progressed and contributed the most to the knowledge we have of the brain sciences: anatomy, physiology, neurology, and psychiatry-psychology. The present article is the second of four parts of this review which includes the chapter on neurophysiology with selected biographical sketches of François Magendie, Marie Jean-Pierre Flourens, Claude Bernard, Charles-Édouard Brown-Séquard, Étienne-Jules Marey, Alfred Fessard and Denise Albe-Fessard.

Figures and institutions of the neurological sciences in Paris from 1800 to 1950. Introduction and Part I: Neuroanatomy.

We present a short historical review on the major institutions and figures that contributed to make Paris a renowned centre of physiology and neurology during the xixth and the first half of the xxth centuries. We purposely chose to focus on the period 1800-1950, as 1800 corresponds to the development of brain science and 1950 marks the true beginning of neuroscience. Our presentation is divided into four chapters, matching the main disciplines which have progressed and contributed the most to the knowledge we have of the brain sciences: anatomy, physiology, neurology, and psychiatry-psychology. The present article is the first of four parts of this review, which includes an introduction followed by the chapter on neuroanatomy and on anatomo-pathology, which includes biographical sketches of Félix Vicq d'Azyr, François-Xavier Bichat, Franz Joseph Gall, Jean Cruveilhier, Jules Bernard Luys, Paul Broca, Louis Ranvier, André-Victor Cornil, Albert Gombault, Jean Nageotte and René Couteaux.

The in vitro neonatal rat spinal cord preparation: a new insight into mammalian locomotor mechanisms.

The in vitro neonatal rat spinal cord preparation is the first mammalian nervous system isolated from the brainstem to the caudal end of the spinal cord. It permits the study of the cellular properties of mammalian locomotor networks and is unique in containing all the nervous structures related to locomotion. Although being a very immature system, this model has been considered as an adult preparation in which mammalian locomotor central pattern generators can be studied in detail. Nevertheless, one can also follow the development of locomotor functions during the perinatal period. Contrary to the adult, all neuroactive substances can directly reach the cellular structures in the brainstem-spinal cord preparation. When a neuroactive substance is applied to the bath, a single rhythmic activity is recorded along the cord. In fact, three rhythms can be isolated: one at the cervical level for the forelimbs, one at the lumbar level for the hind limbs and one in the sacrococcygeal region for the tail. Studies carried out on this preparation deal with three major areas: (1) relations between spontaneous activity and maturation of spinal network, (2) organisation of the different spinal networks, (3) key role of the descending pathways.

Gravity influences the development of inputs from the brain to lumbar motoneurons in the rat.

We investigated the influence of gravity on the maturation of electrical properties of lumbar motoneurons and the development of their inputs from ventral descending pathways, which are important for the control of posture and locomotion. Using electrophysiological approaches in the in vitro brain stem-spinal cord preparation of neonatal rats born and reared in hypergravity field we demonstrate that: (1) the postnatal development of descending inputs to lumbar enlargement was reduced in animals submitted to hypergravity; (2) similar developmental pattern of basic electrical properties observed between motoneurons of hypergravity and control animals could not account for the changes in descending inputs. We concluded that gravity was critical to shape development of the supraspinal afferents in the lumbar spinal cord throughout the postnatal period.

Close relationship between motor impairments and loss of functional motoneurons in a Charcot-Marie-Tooth type 1A model.

Charcot-Marie-Tooth disease type 1A is the most frequent hereditary neuropathy affecting the peripheral nervous system. A partial duplication of chromosome 17 (17p11.2) involving the PMP22 gene is responsible for dysmyelination-demyelination processes leading to motor and sensory impairments. Murine models of this disease are now widely used to investigate the mechanisms occurring at the behavioural and physiological levels. In this study, adult transgenic mice (6 months old) having integrated 7 copies of the human PMP22 gene were used to compare the motor performance, evaluated by using a complex locomotor test (the rotarod test), with both the number of functional motoneurons innervating the soleus muscle and the level of myelination in the sciatic nerve. Two levels of motor deficits were detected and led us to divide the population into two subgroups. In both impaired groups, the level of motor deficit was strongly correlated with the number of functional motoneurons evaluated by retrograde labeling from the muscle, but not with the number of myelinated fibers or the thickness of the myelin sheath (g-ratio). It therefore appears that the number of motor units may be a key element in motor impairments observed in Charcot-Marie-Tooth disease type 1A disease. These findings may have implications for therapeutic procedures, which should focus on the survival of the motoneuronal pool and/or the maintenance of functional neuro-muscular connexions to reduce motor impairments in humans.

PMP22 overexpression causes dysmyelination in mice.

Charcot-Marie-Tooth (CMT) disease is the most frequent hereditary peripheral neuropathy in humans. Its prevalence is about one in 2500. A subform, CMT1A, is transmitted as an autosomal dominant trait. An estimated 75% of patients are affected. This disorder has been shown to be associated with the duplication of a 1.5 Mb region of the short arm of chromosome 17, in which the PMP22 gene has been mapped. We have constructed a murine model of CMT1A by inserting into the murine genome a human YAC containing peripheral myelin protein 22 (PMP22) and its flanking controlling elements. We describe the behaviour of the C22 line (seven copies of YAC, 2.1 times PMP22 overexpression) during the myelination process. Electron microscopy, morphometry, electrophysiology, nerve conduction and expression of specific markers (e.g. Krox20) in normal and pathological Schwann cells demonstrated that PMP22 overexpression leads to a defect in the myelination of axons. The largest axons are the most affected. Only a few demyelination/remyelination processes were observed. Moreover, PMP22 overexpression probably enhances collagen synthesis by fibroblasts, before myelination, demonstrating that structures other than Schwann cells are affected by PMP22 overexpression. Classically, CMT1A was thought to be induced by a demyelination process following a phase of normal myelination, yet our data suggest that dysmyelination should be considered as a major factor for the disease.

Behavioural profiling of a murine Charcot-Marie-Tooth disease type 1A model.

Different features of motor behaviour were studied on a transgenic mouse model of Charcot-Marie-Tooth's disease (CMT). Mutants with 4 or 7 copies of the human PMP22 gene leading to a phenotype significantly close to CMT's disease type 1A were compared with control animals. The aim of the study was to validate this transgenic model and to characterise the impairments occurring in the various lines. Three main types of analysis were performed in 2-month-old mice without any peculiar visible deficit: (i) a study of standardised clinical tests (SHIRPA protocol) demonstrated that only a few motor deficits were expressed; (ii) a measurement of general spontaneous activity by means of a commercial video-tracking system was performed and revealed that the main spontaneous activities were identical in the three lines with, however, some slight localised modifications; and, (iii) by contrast, the three lines respond very differently to the footprints, grip strength, splay test and rotarod test. Even in lines with a significantly limited copy number of the transgene, we observed and quantified impairments. In conclusion, mutants of CMT1A seem to be a very pertinent model of this human pathology and will certainly be useful for therapeutic procedures and for theoretical studies on this disease.

Differential maturation of motoneurons innervating ankle flexor and extensor muscles in the neonatal rat.

The first postnatal week is a critical period for the development of posture in the rat. The use of ankle extensor muscles in postural reactions increases during this period. Changes in excitability of motoneurons are probably an important factor underlying this maturation. The aim of this study was to identify whether variations in the maturation exist between motor pools innervating antagonistic muscles. Intracellular recordings in the in vitro brain stem-spinal cord preparation of neonatal rats (from postnatal day 0-5) were used to examine the developmental changes in excitability of motoneurons innervating the ankle flexors (F-MNs) and the antigravity ankle extensors (E-MNs). No significant difference in resting potential, action potential threshold, input resistance or rheobase was observed at birth. The age-related increase in rheobase was more pronounced for F-MNs than for E-MNs. The development of discharge properties of E-MNs lagged behind that of F-MNs. More F-MNs than E-MNs were able to fire repetitively in response to current injection at birth. F-MNs discharged at a higher frequency than E-MNs at all ages. Differences in the duration of action potential afterhyperpolarization accounted, at least partly, for the differences in discharge frequency between E-MNs and F-MNs at birth, and for the age-related increase in firing rate. These results suggest that E-MNs are more immature at birth than F-MNs and that there is a differential development of motoneurons innervating antagonistic muscles. This may be a critical factor in the development of posture and locomotion.

Central control components of a 'simple' stretch reflex.

The monosynaptic stretch reflex is a fundamental feature of sensory-motor organization in most animal groups. In isolation, it serves largely as a negative feedback devoted to postural controls; however, when it is involved in diverse movements, it can be modified by central command circuits. In order to understand the implications of such modifications, a model system has been chosen that has been studied at many different levels: the crayfish walking system. Recent studies have revealed several levels of control and modulation (for example, at the levels of the sensory afferent and the output synapse from the sensory afferent, and via changes in the membrane properties of the postsynaptic neuron) that operate complex and highly adaptive sensory-motor processing. During a given motor task, such mechanisms reshape the sensory message completely, such that the stretch reflex becomes a part of the central motor command.

What do reflex and voluntary mean? Modern views on an ancient debate.

Are the words reflex and voluntary useful scientific concepts, or are they prescientific terms that should be discarded? Physiologists use these words routinely in their publications, in laboratory experiments and, indeed, like most lay people, in their daily lives. The tacit assumption is that we all know, more or less, what they mean. However, the issue has a rich history of philosophical and scientific debate; and, as this article demonstrates, present-day researchers still cannot reach a consensus on the meaning of the words and on whether it is possible to draw a scientific distinction between them. The five authors present five quite different analyses. In broad terms, they split into two camps: those who equate voluntary behaviours with consciousness and suppressibility and those who view all behaviours as sensorimotor interactions, the complexity of which determines whether they are reflexive or voluntary. According to the first view, most movements of daily life are neither purely reflex nor purely voluntary. They fall into the middle ground of automatic motor programs. According to the second view, as neuroscience advances the class of reflex behaviours will grow and the class of voluntary behaviours will shrink.

Load-regulating mechanisms in gait and posture: comparative aspects.

How is load sensed by receptors, and how is this sensory information used to guide locomotion? Many insights in this domain have evolved from comparative studies since it has been realized that basic principles concerning load sensing and regulation can be found in a wide variety of animals, both vertebrate and invertebrate. Feedback about load is not only derived from specific load receptors but also from other types of receptors that previously were thought to have other functions. In the central nervous system of many species, a convergence is found between specific and nonspecific load receptors. Furthermore, feedback from load receptors onto central circuits involved in the generation of rhythmic locomotor output is commonly found. During the stance phase, afferent activity from various load detectors can activate the extensor part in such circuits, thereby providing reinforcing force feedback. At the same time, the flexion is suppressed. The functional role of this arrangement is that activity in antigravity muscles is promoted while the onset of the next flexion is delayed as long as the limb is loaded. This type of reinforcing force feedback is present during gait but absent in the immoble resting animal.

Spontaneous and locomotor-related GABAergic input onto primary afferents in the neonatal rat.

The in vitro brain stem-spinal cord preparation of neonatal rats (0-5 days old) was used to examine the contribution of GABAA (gamma-aminobutyric acid) receptors to the spontaneous and locomotor-related antidromic firing in the dorsal roots of neonatal rats. Spontaneous bursts of antidromic discharges were generated by the underlying afferent terminal depolarizations reaching spiking threshold. The number of antidromic action potentials increased significantly in saline solution with Cl- concentration reduced to 50% of control. Bath application of the GABAA receptor antagonist bicuculline, at low concentrations (1-2 microM), or picrotoxin blocked the antidromic discharges in the dorsal roots almost completely. The increase in Cl- conductance was therefore mediated by an activation of GABAA receptors. Increasing the concentration of bicuculline to 10-20 microM never blocked these discharges further. On the contrary, in half of the preparations, the number of antidromic action potentials was higher in the presence of high concentrations of bicuculline (10-20 microM) than in the presence of picrotoxin or low concentrations of bicuculline. This suggests that bicuculline, at high concentrations, may have other effects, in addition to blocking GABAA receptors. Dorsal root firing was observed during fictive locomotion induced by bath application of excitatory amino acids and serotonin. A rhythmical pattern was often demonstrated. Bicuculline at low concentrations caused a decrease of the antidromic discharge whereas, at high concentrations, bursts of discharges appeared. A double-bath with a barrier built at the L3 level was then used to separate the mechanisms which generate locomotion from those mediating primary afferent depolarizations. Excitatory amino acids and serotonin were perfused in the rostral pool only. Decreasing the concentration of chloride in the caudal bath caused a sharp increase in the number of antidromic action potentials recorded from the L5 dorsal root. These discharges, which were modulated in phase with the locomotor rhythm, were blocked by bicuculline. These data demonstrate the existence of a locomotor-related GABAergic input onto primary afferent terminals in the neonatal rat.