Hans Straka

Ludwig-Maximilians-University of Munich, München, Bavaria, Germany

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Publications (68)249.28 Total impact

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    ABSTRACT: Pit vipers (Crotalinae) have a specific sensory system that detects infrared radiation with bilateral pit organs in the upper jaw. Each pit organ consists of a thin membrane, innervated by three trigeminal nerve branches that project to a specific nucleus in the dorsal hindbrain. The known topographic organization of infrared signals in the optic tectum prompted us to test the implementation of spatiotopically aligned sensory maps through hierarchical neuronal levels from the peripheral epithelium to the first central site in the hindbrain, the nucleus of the lateral descending trigeminal tract (LTTD). The spatial organization of the anatomical connections was revealed in a novel in vitro whole brain preparation of the western diamondback-rattlesnake (Crotalus atrox) that allowed specific application of multiple neuronal tracers to identified pit organ-supplying trigeminal nerve branches. After adequate survival times, the entire peripheral and central projections of fibers within the pit membrane and the LTTD became visible. This approach revealed a morphological partition of the pit membrane into three well-defined sensory areas with largely separated innervations by the three main branches, respectively. The peripheral segregation of infrared afferents in the sensory epithelium was matched by a differential termination of the respective afferents within different areas of the LTTD with little overlap. This result demonstrates a topographic organizational principle of the snake infrared system that is implemented by maintaining spatially aligned representations of environmental infrared cues on the sensory epithelium through specific neuronal projections at the level of the first central processing stage, comparable to the visual system. J. Comp. Neurol., 2014. © 2014 Wiley Periodicals, Inc.
    The Journal of Comparative Neurology 12/2014; 522(18). DOI:10.1002/cne.23644 · 3.51 Impact Factor
  • Francisco Branoner, Hans Straka
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    ABSTRACT: Gaze stabilization during head/body movements is achieved to a large extent by vestibular-evoked compensatory eye movements. These reflexes derive from semicircular canal and otolith organs and depend on the transformation of the respective sensory signals into extraocular motor commands. In order to elicit directionally and dynamically appropriate compensatory eye movements, extraocular motoneurons require spatio-temporally specific inputs from semicircular canals and regions of the utricular epithelium with matching directional sensitivity. The ontogenetic establishment and maturation of the directional tuning of otolith inputs in extraocular motoneurons was studied in Xenopus laevis tadpoles. In young larvae at stage 46-48, superior oblique extraocular motoneurons receive omnidirectional utricular signals during horizontal translational motion, indicating an absence of spatial tuning. In contrast, in older larvae beyond stage 49 these motoneurons were activated by directionally more restricted otolith inputs with an increasingly enhanced spatial tuning until stage 53. This developmental process limited the origin of otolith signals to a utricular epithelial sector with a hair cell sensitivity that is co-aligned with the pulling direction of the superior oblique eye muscle. The maturation of the otolith response vector was abolished by enzymatic prevention of semicircular canal formation in post-embryonic tadpoles at stage 44, suggesting that functionally intact semicircular canals are causally responsible for the observed directional tuning of utricular responses. A likely mechanism by which semicircular canals might influence the tuning of the otolith responses includes stabilization of co-activated and centrally converging sensory signals from semicircular canal and spatially aligned epithelial utricular regions during natural head/body motion. © 2014 Wiley Periodicals, Inc. Develop Neurobiol, 2014
    Developmental Neurobiology 09/2014; DOI:10.1002/dneu.22234 · 4.19 Impact Factor
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    ABSTRACT: Anesthetics are drugs that reversibly relieve pain, decrease body movements and suppress neuronal activity. Most drugs only cover one of these effects; for instance, analgesics relieve pain but fail to block primary fiber responses to noxious stimuli. Alternately, paralytic drugs block synaptic transmission at neuromuscular junctions, thereby effectively paralyzing skeletal muscles. Thus, both analgesics and paralytics each accomplish one effect, but fail to singularly account for all three. Tricaine methanesulfonate (MS-222) is structurally similar to benzocaine, a typical anesthetic for anamniote vertebrates, but contains a sulfate moiety rendering this drug more hydrophilic. MS-222 is used as anesthetic in poikilothermic animals such as fish and amphibians. However, it is often argued that MS-222 is only a hypnotic drug and its ability to block neural activity has been questioned. This prompted us to evaluate the potency and dynamics of MS-222-induced effects on neuronal firing of sensory and motor nerves alongside a defined motor behavior in semi-intact in vitro preparations of Xenopus laevis tadpoles. Electrophysiological recordings of extraocular motor discharge and both spontaneous and evoked mechanosensory nerve activity were measured before, during and after administration of MS-222, then compared to benzocaine and a known paralytic, pancuronium. Both MS-222 and benzocaine, but not pancuronium caused a dose-dependent, reversible blockade of extraocular motor and sensory nerve activity. These results indicate that MS-222 as benzocaine blocks the activity of both sensory and motor nerves compatible with the mechanistic action of effective anesthetics, indicating that both caine-derivates are effective as single-drug anesthetics for surgical interventions in anamniotes.
    PLoS ONE 07/2014; 9(7):e101606. DOI:10.1371/journal.pone.0101606 · 3.53 Impact Factor
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    ABSTRACT: The vertebrate hindbrain develops as a series of well-defined neuroepithelial segments or rhombomeres. While rhombomeres are visible in all vertebrate embryos, there is not generally any visible segmental anatomy in the brains of adults. Teleost fish are exceptional in retaining a rhombomeric pattern of reticulospinal neurons through embryonic, larval and adult periods. We use this feature to more precisely map the segmental imprint in the reticular and motor basal hindbrain of adult goldfish. Analysis of serial sections cut in three planes and computer reconstructions of retrogradely labeled reticulospinal neurons yielded a segmental framework compatible with previous reports and more amenable to correlation with surrounding neuronal features. Cranial nerve motoneurons and octavo-lateral efferent neurons were aligned to the reticulospinal scaffold by mapping neurons immunopositive for choline acetyltransferase or retrogradely labeled from cranial nerve roots. The mapping corresponded well with the known ontogeny of these neurons and helps confirm the segmental territories defined by reticulospinal anatomy. Since both the reticulospinal and motoneuronal segmental patterns persist in the hindbrain of adult goldfish, we hypothesize that a permanent "hindbrain framework" may be a general property that is retained in adult vertebrates. The establishment of a relationship between individual segments and neuronal phenotypes provides a convenient method for future studies that combine form, physiology and function in adult vertebrates. J. Comp. Neurol., 2014. © 2014 Wiley Periodicals, Inc.
    The Journal of Comparative Neurology 07/2014; 522(10). DOI:10.1002/cne.23544 · 3.51 Impact Factor
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    ABSTRACT: Developmental and evolutionary data from vertebrates are beginning to elucidate the origin of the sensorimotor pathway that links gravity and motion detection to image-stabilizing eye movements - the vestibulo-ocular reflex (VOR). Conserved transcription factors coordinate the development of the vertebrate ear into three functional sensory compartments (graviception/translational linear acceleration, angular acceleration and sound perception). These sensory components connect to specific populations of vestibular and auditory projection neurons in the dorsal hindbrain through undetermined molecular mechanisms. In contrast, a molecular basis for the patterning of the vestibular projection neurons is beginning to emerge. These are organized through the actions of rostrocaudally and dorsoventrally restricted transcription factors into a 'hodological mosaic' within which coherent and largely segregated subgroups are specified to project to different targets in the spinal cord and brain stem. A specific set of these regionally diverse vestibular projection neurons functions as the central element that transforms vestibular sensory signals generated by active and passive head and body movements into motor output through the extraocular muscles. The large dynamic range of motion-related sensory signals requires an organization of VOR pathways as parallel, frequency-tuned, hierarchical connections from the sensory periphery to the motor output. We suggest that eyes, ears and functional connections subserving the VOR are vertebrate novelties that evolved into a functionally coherent motor control system in an almost stereotypic organization across vertebrate taxa. © 2014 S. Karger AG, Basel.
    Brain Behavior and Evolution 01/2014; 83(2):162-75. DOI:10.1159/000357833 · 4.29 Impact Factor
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    Bernd Fritzsch, Hans Straka
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    ABSTRACT: Among the major distance senses of vertebrates, the ear is unique in its complex morphological changes during evolution. Conceivably, these changes enable the ear to adapt toward sensing various physically well-characterized stimuli. This review develops a scenario that integrates sensory cell with organ evolution. We propose that molecular and cellular evolution of the vertebrate hair cells occurred prior to the formation of the vertebrate ear. We previously proposed that the genes driving hair cell differentiation were aggregated in the otic region through developmental re-patterning that generated a unique vertebrate embryonic structure, the otic placode. In agreement with the presence of graviceptive receptors in many vertebrate outgroups, it is likely that the vertebrate ear originally functioned as a simple gravity-sensing organ. Based on the rare occurrence of angular acceleration receptors in vertebrate outgroups, we further propose that the canal system evolved with a more sophisticated ear morphogenesis. This evolving morphogenesis obviously turned the initial otocyst into a complex set of canals and recesses, harboring multiple sensory epithelia each adapted to the acquisition of a specific aspect of a given physical stimulus. As support for this evolutionary progression, we provide several details of the molecular basis of ear development.
    Journal of Comparative Physiology 11/2013; DOI:10.1007/s00359-013-0865-z · 1.63 Impact Factor
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    Hans Straka, Robert Baker
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    ABSTRACT: Central vestibular neurons form identifiable subgroups within the boundaries of classically outlined octavolateral nuclei in primitive vertebrates that are distinct from those processing lateral line, electrosensory, and auditory signals. Each vestibular subgroup exhibits a particular morpho-physiological property that receives origin-specific sensory inputs from semicircular canal and otolith organs. Behaviorally characterized phenotypes send discrete axonal projections to extraocular, spinal, and cerebellar targets including other ipsi- and contralateral vestibular nuclei. The anatomical locations of vestibuloocular and vestibulospinal neurons correlate with genetically defined hindbrain compartments that are well conserved throughout vertebrate evolution though some variability exists in fossil and extant vertebrate species. The different vestibular subgroups exhibit a robust sensorimotor signal processing complemented with a high degree of vestibular and visual adaptive plasticity.
    Frontiers in Neural Circuits 11/2013; 7:182. DOI:10.3389/fncir.2013.00182 · 2.95 Impact Factor
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    ABSTRACT: Adolescent idiopathic scoliosis in humans is often associated with vestibulomotor deficits. Compatible with a vestibular origin, scoliotic deformations were provoked in adult Xenopus frogs by unilateral labyrinthectomy (UL) at larval stages. The aquatic ecophysiology and absence of body-weight-supporting limb proprioceptive signals in amphibian tadpoles as a potential sensory substitute after UL might be the cause for a persistent asymmetric descending vestibulospinal activity. Therefore, peripheral vestibular lesions in larval Xenopus were used to reveal the morphophysiological alterations at the cellular and network levels. As a result, spinal motor nerves that were modulated by the previously intact side before UL remained permanently silent during natural vestibular stimulation after the lesion. In addition, retrograde tracing of descending pathways revealed a loss of vestibular neurons on the ipsilesional side with crossed vestibulospinal projections. This loss facilitated a general mass imbalance in descending premotor activity and a permanent asymmetric motor drive to the axial musculature. Therefore, we propose that the persistent asymmetric contraction of trunk muscles exerts a constant, uncompensated differential mechanical pull on bilateral skeletal elements that enforces a distortion of the soft cartilaginous skeletal elements and bone shapes. This ultimately provokes severe scoliotic deformations during ontogenetic development similar to the human syndrome.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 04/2013; 33(16):6845-56. DOI:10.1523/JNEUROSCI.4842-12.2013 · 6.75 Impact Factor
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    ABSTRACT: In swimming Xenopus laevis tadpoles, gaze stabilization is achieved by efference copies of spinal locomotory CPG output that produce rhythmic extraocular motor activity appropriate for minimizing motion-derived visual disturbances. During metamorphosis, Xenopus switches its locomotory mechanism from larval tail-based undulatory movements to bilaterally synchronous hindlimb kick propulsion in the adult. The change in locomotory mode leads to body motion dynamics that no longer require conjugate left-right eye rotations for effective retinal image stabilization. Using in vivo kinematic analyses, in vitro electrophysiological recordings and specific CNS lesions, we have investigated spino-extraocular motor coupling in the juvenile frog and the underlying neural pathways to understand how gaze control processes are altered in accordance with the animal's change in body plan and locomotor strategy. Recordings of extraocular and limb motor nerves during spontaneous "fictive" swimming in isolated CNS preparations revealed that there is indeed a corresponding change in spinal efference copy control of extraocular motor output. In contrast to fictive larval swimming where alternating bursts occur in bilateral antagonistic horizontal extraocular nerves, during adult fictive limb-kicking, these motor nerves are synchronously active in accordance with the production of convergent eye movements during the linear head accelerations resulting from forward propulsion. Correspondingly, the neural pathways mediating spino-extraocular coupling have switched from contralateral to strictly ipsilateral ascending influences that ensure a coactivation of bilateral extraocular motoneurons with synchronous left-right limb extensions. Thus, adaptive developmental plasticity during metamorphosis enables spinal CPG-driven extraocular motor activity to match the changing requirements for eye movement control during self-motion.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 03/2013; 33(10):4253-64. DOI:10.1523/JNEUROSCI.4521-12.2013 · 6.75 Impact Factor
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    ABSTRACT: In guiding adaptive behavior, efference copy signals or corollary discharge are traditionally considered to serve as predictors of self-generated sensory inputs and by interfering with their central processing are able to counter unwanted consequences of an animal's own actions. Here, in a speculative reflection on this issue, we consider a different functional role for such intrinsic predictive signaling, namely in stabilizing gaze during locomotion where resultant changes in head orientation in space require online compensatory eye movements in order to prevent retinal image slip. The direct activation of extraocular motoneurons by locomotor-related efference copies offers a prospective substrate for assisting self-motion derived sensory feedback, rather than being subtracted from the sensory signal to eliminate unwanted reafferent information. However, implementing such a feed-forward mechanism would be critically dependent on an appropriate phase coupling between rhythmic propulsive movement and resultant head/visual image displacement. We used video analyzes of actual locomotor behavior and basic theoretical modeling to evaluate head motion during stable locomotion in animals as diverse as Xenopus laevis tadpoles, teleost fish and horses in order to assess the potential suitability of spinal efference copies to the stabilization of gaze during locomotion. In all three species, and therefore regardless of aquatic or terrestrial environment, the head displacements that accompanied locomotor action displayed a strong correlative spatio-temporal relationship in correspondence with a potential predictive value for compensatory eye adjustments. Although spinal central pattern generator-derived efference copies offer appropriately timed commands for extraocular motor control during self-generated motion, it is likely that precise image stabilization requires the additional contributions of sensory feedback signals. Nonetheless, the predictability of the visual consequences of stereotyped locomotion renders intrinsic efference copy signaling an appealing mechanism for offsetting these disturbances, thus questioning the exclusive role traditionally ascribed to sensory-motor transformations in stabilizing gaze during vertebrate locomotion.
    Biological Cybernetics 11/2012; 106(11-12). DOI:10.1007/s00422-012-0528-0 · 1.93 Impact Factor
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    ABSTRACT: Self-generated body movements require compensatory eye and head adjustments in order to avoid perturbation of visual information processing. Retinal image stabilization is traditionally ascribed to the transformation of visuovestibular signals into appropriate extraocular motor commands for compensatory ocular movements. During locomotion, however, intrinsic "efference copies" of the motor commands deriving from spinal central pattern generator (CPG) activity potentially offer a reliable and rapid mechanism for image stabilization, in addition to the slower contribution of movement-encoding sensory inputs. Using a variety of in vitro and in vivo preparations of Xenopus tadpoles, we demonstrate that spinal locomotor CPG-derived efference copies do indeed produce effective conjugate eye movements that counteract oppositely directed horizontal head displacements during undulatory tail-based locomotion. The efference copy transmission, by which the extraocular motor system becomes functionally appropriated to the spinal cord, is mediated by direct ascending pathways. Although the impact of the CPG feedforward commands matches the spatiotemporal specificity of classical vestibulo-ocular responses, the two fundamentally different signals do not contribute collectively to image stabilization during swimming. Instead, when the CPG is active, horizontal vestibulo-ocular reflexes resulting from head movements are selectively suppressed. These results therefore challenge our traditional understanding of how animals offset the disruptive effects of propulsive body movements on visual processing. Specifically, our finding that predictive efference copies of intrinsic, rhythmic neural signals produced by the locomotory CPG supersede, rather than supplement, reactive vestibulo-ocular reflexes in order to drive image-stabilizing eye adjustments during larval frog swimming, represents a hitherto unreported mechanism for vertebrate ocular motor control.
    Current biology: CB 07/2012; 22(18):1649-58. DOI:10.1016/j.cub.2012.07.019 · 9.92 Impact Factor
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    François M Lambert, Hans Straka
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    ABSTRACT: Studies of behavioral consequences after unilateral labyrinthectomy have a long tradition in the quest of determining rules and limitations of the central nervous system (CNS) to exert plastic changes that assist the recuperation from the loss of sensory inputs. Frogs were among the first animal models to illustrate general principles of regenerative capacity and reorganizational neural flexibility after a vestibular lesion. The continuous successful use of the latter animals is in part based on the easy access and identifiability of nerve branches to inner ear organs for surgical intervention, the possibility to employ whole brain preparations for in vitro studies and the limited degree of freedom of postural reflexes for quantification of behavioral impairments and subsequent improvements. Major discoveries that increased the knowledge of post-lesional reactive mechanisms in the CNS include alterations in vestibular commissural signal processing and activation of cooperative changes in excitatory and inhibitory inputs to disfacilitated neurons. Moreover, the observed increase of synaptic efficacy in propriospinal circuits illustrates the importance of limb proprioceptive inputs for postural recovery. Accumulated evidence suggests that the lesion-induced neural plasticity is not a goal-directed process that aims toward a meaningful restoration of vestibular reflexes but rather attempts a survival of those neurons that have lost their excitatory inputs. Accordingly, the reaction mechanism causes an improvement of some components but also a deterioration of other aspects as seen by spatio-temporally inappropriate vestibulo-motor responses, similar to the consequences of plasticity processes in various sensory systems and species. The generality of the findings indicate that frogs continue to form a highly amenable vertebrate model system for exploring molecular and physiological events during cellular and network reorganization after a loss of vestibular function.
    Frontiers in Neurology 04/2012; 3:42. DOI:10.3389/fneur.2012.00042
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    Hans Straka, John Simmers
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    ABSTRACT: The amphibian Xenopus laevis represents a highly amenable model system for exploring the ontogeny of central neural networks, the functional establishment of sensory-motor transformations, and the generation of effective motor commands for complex behaviors. Specifically, the ability to employ a range of semi-intact and isolated preparations for in vitro morphophysiological experimentation has provided new insights into the developmental and integrative processes associated with the generation of locomotory behavior during changing life styles. In vitro electrophysiological studies have begun to explore the functional assembly, disassembly and dynamic plasticity of spinal pattern generating circuits as Xenopus undergoes the developmental switch from larval tail-based swimming to adult limb-based locomotion. Major advances have also been made in understanding the developmental onset of multisensory signal processing for reactive gaze and posture stabilizing reflexes during self-motion. Additionally, recent evidence from semi-intact animal and isolated CNS experiments has provided compelling evidence that in Xenopus tadpoles, predictive feed-forward signaling from the spinal locomotor pattern generator are engaged in minimizing visual disturbances during tail-based swimming. This new concept questions the traditional view of retinal image stabilization that in vertebrates has been exclusively attributed to sensory-motor transformations of body/head motion-detecting signals. Moreover, changes in visuomotor demands associated with the developmental transition in propulsive strategy from tail- to limb-based locomotion during metamorphosis presumably necessitates corresponding adaptive alterations in the intrinsic spinoextraocular coupling mechanism. Consequently, Xenopus provides a unique opportunity to address basic questions on the developmental dynamics of neural network assembly and sensory-motor computations for vertebrate motor behavior in general.
    Developmental Neurobiology 04/2012; 72(4):649-63. DOI:10.1002/dneu.20965 · 4.19 Impact Factor
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    ABSTRACT: Head motion-related sensory signals are transformed by second-order vestibular neurons (2°VNs) into appropriate commands for retinal image stabilization during body motion. In frogs, these 2°VNs form two distinct subpopulations that have either tonic or highly phasic intrinsic properties, essentially compatible with low-pass and bandpass filter characteristics, respectively. In the present study, physiological data on cellular properties of 2°VNs of the grass frog (Rana temporaria) have been used to construct conductance-based spiking cellular models that were fine-tuned by fitting to recorded spike-frequency data. The results of this approach suggest that low-threshold, voltage-dependent potassium channels in phasic and spike-dependent potassium channels in tonic 2°VNs are important contributors to the differential, yet complementary response characteristics of the two vestibular subtypes. Extension of the cellular model with conductance-based synapses allowed simulation of afferent excitation and evaluation of the emerging properties of local feedforward inhibitory circuits. This approach revealed the relative contributions of intrinsic and synaptic factors on afferent signal processing in phasic 2°VNs. Additional extension of the single-cell model to a population model allowed testing under more natural conditions including asynchronous afferent labyrinthine input and synaptic noise. This latter approach indicated that the feedforward inhibition from the local inhibitory network acts as a high-pass filter, which reinforces the impact of the intrinsic membrane properties of phasic 2°VNs on peak response amplitude and timing. Thus, the combination of cellular and network properties enables phasic 2°VNs to work as a noise-resistant detector, suitable for central processing of short-duration vestibular signals.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 06/2011; 31(23):8359-72. DOI:10.1523/JNEUROSCI.6161-10.2011 · 6.75 Impact Factor
  • C Rössert, H Straka
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    ABSTRACT: Head/body motion-related sensory signals are transformed in second-order vestibular neurons (2°VN) into commands for appropriate motor reactions that stabilize gaze and posture during locomotion. In all vertebrates, these neurons form functional subgroups with different membrane properties and response dynamics, compatible with the necessity to process a wide range of motion-related sensory signals. In frog, 2°VN subdivide into two well-defined populations with distinctly different intrinsic membrane properties, discharge dynamics and synaptic response characteristics. Tonic 2°VN form low-pass filters with membrane properties that cause synaptic amplification, whereas phasic 2°VN form band-pass filters that cause shunting of repetitive inputs. The different, yet complementary, filter properties render tonic neurons suitable for integration and phasic neurons for differentiation and event detection. Specific insertion of phasic 2°VN into local vestibular networks of inhibitory interneurons reinforces the functional consequences of the intrinsic membrane properties of this particular cell type with respect to the processing of afferent sensory signals. Thus, the combination of matching intrinsic cellular and emerging network properties generates sets of neuronal elements that form adjustable, frequency-tuned filter components for separate transformation of the various dynamic aspects of head motion-related signals. The overall frequency tuning of central vestibular neurons differs between vertebrates along with variations in species-specific locomotor dynamics, thereby illustrating an ecophysiological plasticity of the involved neuronal elements. Moreover, separation into multiple, dynamically different subtypes at any neuronal level along the vestibulo-motor reflex pathways suggests an organization of head motion-related sensory-motor transformation in parallel, frequency-tuned channels.
    Experimental Brain Research 03/2011; 210(3-4):437-49. DOI:10.1007/s00221-011-2585-3 · 2.17 Impact Factor
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    Mathieu Beraneck, Hans Straka
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    ABSTRACT: Second-order vestibular neurons (2°VN) are the central element for the transformation of body motion-related sensory signals into extraocular motor commands for retinal image stabilization during locomotion. The wide range of motion dynamics necessitates sensory signal transformation in parallel, frequency-tuned channels. Accordingly, in various vertebrates, 2°VN have been shown to form differently tuned functional subgroups. In frog, these neurons subdivide into two separate populations with distinctly different intrinsic membrane properties, discharge dynamics and synaptic response characteristics. Frog tonic 2°VN exhibit low-pass filter characteristics and membrane properties that cause amplification of synaptic inputs, whereas phasic 2°VN form band-pass filters that allow frequency-dependent shunting of repetitive inputs. The differential, yet complementary membrane properties render tonic 2°VN particularly suitable for synaptic integration and phasic 2°VN for differentiation and event detection. Differential insertion of the two cell types into local circuits reinforces the functional consequences of the intrinsic membrane properties, respectively. As a consequence, the synergy of cellular and network properties creates sets of neuronal elements with particular filter characteristics that form flexible, frequency-tuned components for optimal transformation of all dynamic aspects of body motion-related multisensory signals.
    Journal of Vestibular Research 01/2011; 21(1):5-19. DOI:10.3233/VES-2011-0396 · 1.46 Impact Factor
  • Hans Straka
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    ABSTRACT: Vestibulo-ocular reflexes (VOR) assist retinal image stabilization during vertebrate locomotion thereby ensuring accurate visual perception. The importance of this motor behavior for animal survival requires that the underlying circuitry and all individual components are fully developed and functional as soon as post-embryonic animals initiate self-motion. Recent progress on the genetic, molecular, and activity-dependent regulation of placode development, vestibular sensory organ formation, circuit assembly, and acquisition of neuronal properties revealed rules and restrictions that give insight into how hindbrain VOR neuronal networks are assembled and become functional during ontogeny. Major crucial steps that correlate with early/delayed functional VOR onsets concern the maturation of cellular properties (precocial/altricial species) and the acquisition of minimal semicircular canal dimensions (small-sized vertebrates).
    Current opinion in neurobiology 12/2010; 20(6):689-95. DOI:10.1016/j.conb.2010.06.003 · 6.77 Impact Factor
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    ABSTRACT: Central vestibular neurons receive substantial inputs from the contralateral labyrinth through inhibitory and excitatory brainstem commissural pathways. The functional organization of these pathways was studied by a multi-methodological approach in isolated frog whole brains. Retrogradely labeled vestibular commissural neurons were primarily located in the superior vestibular nucleus in rhombomeres 2/3 and the medial and descending vestibular nucleus in rhombomeres 5-7. Restricted projections to contralateral vestibular areas, without collaterals to other classical vestibular targets, indicate that vestibular commissural neurons form a feedforward push-pull circuitry. Electrical stimulation of the contralateral coplanar semicircular canal nerve evoked in canal-related second-order vestibular neurons (2 degrees VN) commissural IPSPs (approximately 70%) and EPSPs (approximately 30%) with mainly (approximately 70%) disynaptic onset latencies. The dynamics of commissural responses to electrical pulse trains suggests mediation predominantly by tonic vestibular neurons that activate in all tonic 2 degrees VN large-amplitude IPSPs with a reversal potential of -74 mV. In contrast, phasic 2 degrees VN exhibited either nonreversible, small-amplitude IPSPs (approximately 40%) of likely dendritic origin or large-amplitude commissural EPSPs (approximately 60%). IPSPs with disynaptic onset latencies were exclusively GABAergic (mainly GABA(A) receptor-mediated) but not glycinergic, compatible with the presence of GABA-immunopositive (approximately 20%) and the absence of glycine-immunopositive vestibular commissural neurons. In contrast, IPSPs with longer, oligosynaptic onset latencies were GABAergic and glycinergic, indicating that both pharmacological types of local inhibitory neurons were activated by excitatory commissural fibers. Conservation of major morpho-physiological and pharmacological features of the vestibular commissural pathway suggests that this phylogenetically old circuitry plays an essential role for the processing of bilateral angular head acceleration signals in vertebrates.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 03/2010; 30(9):3310-25. DOI:10.1523/JNEUROSCI.5318-09.2010 · 6.75 Impact Factor
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    ABSTRACT: Human idiopathic scoliosis is characterized by severe deformations of the spine and skeleton. The occurrence of vestibular-related deficits in these patients is well established but it is unclear whether a vestibular pathology is the common cause for the scoliotic syndrome and the gaze/posture deficits or if the latter behavioral deficits are a consequence of the scoliotic deformations. A possible vestibular origin was tested in the frog Xenopus laevis by unilateral removal of the labyrinthine endorgans at larval stages. After metamorphosis into young adult frogs, X-ray images and three-dimensional reconstructed micro-computer tomographic scans of the skeleton showed deformations similar to those of scoliotic patients. The skeletal distortions consisted of a curvature of the spine in the frontal and sagittal plane, a transverse rotation along the body axis and substantial deformations of all vertebrae. In terrestrial vertebrates, the initial postural syndrome after unilateral labyrinthectomy recovers over time and requires body weight-supporting limb proprioceptive information. In an aquatic environment, however, this information is absent. Hence, the lesion-induced asymmetric activity in descending spinal pathways and the resulting asymmetric muscular tonus persists. As a consequence the mostly cartilaginous skeleton of the frog tadpoles progressively deforms. Lack of limb proprioceptive signals in an aquatic environment is thus the element, which links the Xenopus model with human scoliosis because a comparable situation occurs during gestation in utero. A permanently imbalanced activity in descending locomotor/posture control pathways might be the common origin for the observed structural and behavioral deficits in humans as in the different animal models of scoliosis.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 10/2009; 29(40):12477-83. DOI:10.1523/JNEUROSCI.2583-09.2009 · 6.75 Impact Factor
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    ABSTRACT: Computational modeling of the vestibulo-ocular circuitry is essential for understanding the sensory-motor transformation that generates spatially and dynamically appropriate compensatory eye movements during self-motion. Central vestibular neurons in the brainstem are responsible for the major computational step that transforms head acceleration-related sensory vestibular signals into extraocular motor commands that cause compensatory eye motion for gaze stabilization. In frog, second-order vestibular neurons (2°VN) separate into two functional subgroups (tonic - phasic neurons) that distinctly differ in their intrinsic membrane properties and discharge characteristics. While tonic 2°VN exhibit a continuous discharge in response to positive current steps, phasic 2°VN display a brief, high-frequency burst of spikes but no continuous discharge, corresponding to class 1 and class 3 excitability, respectively. Based on the dynamics of sinusoidally modulated changes of the membrane potential, tonic 2°VN show low-pass filter-like response properties, whereas phasic 2°VN have band-pass filter-like characteristics. Correlated with these cellular properties, tonic and phasic 2°VN exhibit pronounced differences in subthreshold response dynamics and discharge kinetics during synaptic activation of individual labyrinthine nerve branches with sinusoidally modulated trains of single electrical pulses. Physio-pharmacological analyses indicated that the two types of 2°VN are differentially embedded into local inhibitory circuits that reinforce the cellular properties of these neurons, respectively, thus indicating a co-adaptation of intrinsic membrane and emerging network properties in the two neuronal subtypes. The channel mechanisms responsible for the different discharge characteristics of the two neuronal subtypes were revealed by a frequency-domain analysis in the subthreshold domain: tonic 2°VN exhibit an increasing impedance with membrane depolarization which likely results from an activation of persistent sodium currents, while phasic 2°VN show a decreasing impedance and increasing resonance with membrane depolarization due to the activation of low-threshold, voltage-dependent ID-type potassium channels. These results also revealed the necessary channel mechanisms to generate spiking multi-compartment models. By extending these models with conductance-based synapses that simulate the corresponding activation and inhibition it was possible to reproduce the distinct firing behavior of the two neuronal subtypes during intracellular and synaptic activation, respectively. By modifying different components of the intrinsic cellular or the synaptic circuit properties it is now possible to determine the relative contributions of membrane and network properties for vestibular signal processing. Selective modifications of different neuronal circuit components or particular properties of ion channel conductances in the model allow making predictions of how eco-physiological or patho-physiological changes affect vestibular signal processing and how cellular and network mechanisms might compensate for induced alterations.
    Frontiers in Computational Neuroscience 08/2009; DOI:10.3389/conf.neuro.10.2009.14.157 · 2.23 Impact Factor

Publication Stats

1k Citations
249.28 Total Impact Points


  • 2001–2014
    • Ludwig-Maximilians-University of Munich
      • • Department of Biology II
      • • Faculty of Biology
      München, Bavaria, Germany
  • 2004–2013
    • Université René Descartes - Paris 5
      • Centre d'Études de la Sensorimotricité (Cesem) (UMR 8194)
      Lutetia Parisorum, Île-de-France, France
  • 2005–2009
    • French National Centre for Scientific Research
      Lutetia Parisorum, Île-de-France, France
  • 2006
    • New York University
      • Department of Physiology and Neuroscience
      New York City, NY, United States
  • 2003
    • Technische Universität München
      München, Bavaria, Germany
  • 1998–2003
    • NYU Langone Medical Center
      New York, New York, United States