Papers by nicholas strausfeld
Current Biology, Jul 1, 2015
Understanding the identity of segments and the evolution of their appendages is a prime concern o... more Understanding the identity of segments and the evolution of their appendages is a prime concern of arthropod evolution studies. This has been challenging for long extinct stem-groups. Now, Cambrian fossils offer insights that will help further evolutionary considerations.
Proceedings of the National Academy of Sciences of the United States of America, Aug 3, 2020
Journal of comparative neurology, Feb 1, 1992
In fleshflies, Sarcophaga bullata, intracellular recording and Lucifer yellow dye‐filling have re... more In fleshflies, Sarcophaga bullata, intracellular recording and Lucifer yellow dye‐filling have revealed small‐field elements of sexually isomorphic retinotopic arrays in the lobula and lobula plate, the axons of which project to premotor channels in the deutocerebrum that supply head‐turning and flight‐steering motor neurons. The dendrites of the small‐field elements visit very restricted oval areas of the retinotopic mosaic, comprising fields that are typically 6–8 input columns wide and 12–20 high. Their physiologically determined receptive fields are also small, typically 20° or less in diameter. The neurons are hyperpolarized in stationary illumination and are transiently depolarized by light OFF and to a lesser degree by light ON. Motion of a striped grating elicits a periodic excitation at the fundamental or second harmonic of the stimulus temporal contrast frequency. The arrangement of these elements in retinotopic arrays with their small receptive fields and flicker‐sensitive dynamic properties make these neurons well suited for the position‐dependent, direction‐insensitive detection of small objects in the fly's visual field, which, is known to drive fixation and tracking.
Journal of comparative neurology, 2006
Intracellular recordings accompanied by dye fills were made from neurons associated with optic gl... more Intracellular recordings accompanied by dye fills were made from neurons associated with optic glomeruli in the lateral protocerebrum of the brain of the blowfly Phaenicia sericata. The present account describes the morphology of these cells and their electrophysiological responses to oriented bar motion. The most dorsal glomeruli are each supplied by retinotopic efferent neurons that have restricted dendritic fields in the lobula and lobula plate of the optic lobes. Each of these lobula complex cells represents a morphologically identified type of neuron arranged as an ensemble that subtends the entire monocular visual field. Of the four recorded and filled efferent types, three were broadly tuned to the orientation of bar stimuli. At the level of optic glomeruli a relay neuron extending centrally from optic foci and a local interneuron that arborizes among glomeruli showed narrow tuning to oriented bar motion. The present results are discussed with respect to the behavioral significance of oriented motion discrimination by flies and other insects, and with respect to neuroanatomical data demonstrating the organization of deep visual neuropils.
Microscopy Research and Technique, Sep 3, 2003
Anatomical methods have identified conserved neuronal morphologies and synaptic relationships amo... more Anatomical methods have identified conserved neuronal morphologies and synaptic relationships among small-field retinotopic neurons in insect optic lobes. These conserved cell shapes occur across many species of dipteran insects and are also shared by Lepidoptera and Hymenoptera. The suggestion that such conserved neurons should participate in motion computing circuits finds support from intracellular recordings as well as older studies that used radioactive deoxyglucose labeling to reveal strata with motion-specific activity in an achromatic neuropil called the lobula plate. While intracellular recordings provide detailed information about the motionsensitive or motion-selective responses of identified neurons, a full understanding of how arrangements of identified neurons compute and integrate information about visual motion will come from a multidisciplinary approach that includes morphological circuit analysis, the use of genetic mutants that exhibit specific deficits in motion processing, and biomimetic models. The latter must be based on the organization and connections of real neurons, yet provide output properties similar to those of more traditional theoretical models based on behavioral observations that date from the 1950s.
The Journal of Neuroscience, Aug 1, 1996
The Hassenstein-Reichardt autocorrelation model for motion computation was derived originally fro... more The Hassenstein-Reichardt autocorrelation model for motion computation was derived originally from studies of optomotor turning reactions of beetles and further refined from studies of houseflies. Its application for explaining a variety of optokinetic behaviors in other insects assumes that neural correlates to the model are principally similar across taxa. This account examines whether this assumption is warranted. The results demonstrate that an evolutionarily conserved subset of neurons corresponds to small retinotopic neurons implicated in motiondetecting circuits that link the retina to motion-sensitive neuropils of the lobula plate. The occurrence of these neurons in basal groups suggests that they must have evolved at least 240 million years before the present time. Functional contiguity among the neurons is suggested by their having layer relationships that are independent of taxon-specific variations such as medulla stratification, the shape of terminals or dendrites, the presence of other taxon-specific neurons, or the absence of orientation-specific motion-sensitive levels in the lobula plate.
Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology, Oct 1, 1991
During sexual pursuit, male flies Sarcophaga bullata, stabilize the image of a pursued target on ... more During sexual pursuit, male flies Sarcophaga bullata, stabilize the image of a pursued target on the dorso-frontal acute zone of their compound eyes. By retinotopic projection, this region is represented in the upper frontal part of the lobula where it is sampled by ensembles of male-specific motion-and flicker-sensitive interneurons. Intracellular recordings of descending neurons, followed by biocytin injection, demonstrate that male-specific neurons are dye-coupled to specific descending neurons and that the response characteristics of these descending neurons closely resemble those of male-specific lobula neurons. Such descending neurons are biocytin-coupled in the thoracic ganglia, revealing their connections with ipsilateral frontal nerve motor neurons supplying muscles that move the head and with contralateral basalar muscle motor neurons that control wing beat amplitude. Recordings from neck muscle motor neurons demonstrate that although they respond to movement of panoramic motion, they also selectively respond to movement of small targets presented to the male-specific acute zone. The present results are discussed with respect to anatomical and physiological studies of sex-specific interneurons and with respect to sexspecific visual behavior. The present study, and those of the two preceding papers, provide a revision of Land and Collett's hypothetical circuit underlying target localization and motor control in males pursuing females.
Science, Mar 4, 1977
Enzymatic treatment was used to test the function ofsome surface peptides and carbohydrates in he... more Enzymatic treatment was used to test the function ofsome surface peptides and carbohydrates in hematopoietic spleen colony formation. Proteases and most glycosidases had no effect on spleen colony formation, whereas treatment with Vibrio cholerae neuraminidase reduced colonies by one-half. Intact sialic acid (residues) appear to play an important role in colony formation.
Oxford University Press eBooks, Dec 1, 2017
A 1915 monograph by the Nobel Prize–winning neuroanatomist Santiago Ramón y Cajal and Domingo Sán... more A 1915 monograph by the Nobel Prize–winning neuroanatomist Santiago Ramón y Cajal and Domingo Sánchez y Sánchez, describing neurons and their organization in the optic lobes of insects, is now standard fare for those studying the microcircuitry of the insect visual system. The work contains prescient assumptions about possible functional arrangements, such as lateral interactions, centrifugal pathways, and the convergence of neurons onto wider dendritic trees, to provide central integration of information processed at peripheral levels of the system. This chapter will consider further indications of correspondence between the insect-crustacean and the vertebrate visual systems, with particular reference to the deep organization of the optic lobe’s third optic neuropil, the lobula, and part of the lateral forebrain (protocerebrum) that receives inputs from it. Together, the lobula and lateral protocerebrum suggest valid comparison with the visual cortex and olfactory centers.
Springer eBooks, 1989
In insects, the organization of neurons in visual and olfactory neuropils is comparable to arrang... more In insects, the organization of neurons in visual and olfactory neuropils is comparable to arrangements in analogous systems in the brains of higher vertebrates. However, although the two modalities of vision and olfaction are subjectively quite different from each other, in insects they are served by common neuroarchitectures, the glomeruli, which are here suggested to be paramount in the processing of qualitative information. Visual and olfactory systems show other specific similarities with respect to the parallel organization of large- and small-axoned neurons. In the visual system, two parallel channels comprise large color-insensitive and small color-sensitive relay neurons that are linked to two major descending pathways. Color insensitive pathways supply motor circuits mediating visually stabilized flight and optokinetic head movements. This pathway is distinct from the parallel subsystem comprising numerous smaller neurons and many synaptic stations that supply leg and direct flight muscle motor neuropils. These two subsystems provide a simple model of magno- and parvocellular organizations identified in the mammalian visual system. Surprisingly, there exists a similar parallel organization amongst large- and small-axoned neurons in the insect olfactory system. Magnocellular olfactory projection neurons provide a relatively direct route to descending pathways. Smaller parvocellular projection neurons provide the first step in a complex sequence of neurons in which higher brain centers play a cardinal role.
Journal of comparative neurology, Feb 1, 1992
The responses of dorsal descending neurons suggest great versatility of the visual system in dete... more The responses of dorsal descending neurons suggest great versatility of the visual system in detecting features of the visual world. Although wide‐field motion‐sensitive neurons respond to symmetric visual flow fields presented to both eyes, other neurons are known to respond selectively to asymmetric movement of the visual surround. The present account distinguishes yet a third class of descending neurons (DNs) that is selectively activated by local presentation of moving gratings or small contrasting objects. Excitation of these DNs in response to local motion contrasts with their inhibitory responses to wide‐field motion. The described DNs invade dorsal neuropil of the pro‐ and mesothoracic ganglia where they converge with other morphologically and physiologically characterized descending elements. Axon collaterals of DNs visit thoracic neuropil containing the dendrites of motor neurons supplying indirect neck and flight muscles. The present results are discussed with respect to the organization of small‐field retinotopic outputs from the lobula, and with respect to the parallel projection of many information channels from the brain to the neck and flight motors.
Journal of comparative neurology, Apr 1, 1990
Intersegmental descending neurons (DNs) link the insect brain to t.he thoracic ganglia. Iontophor... more Intersegmental descending neurons (DNs) link the insect brain to t.he thoracic ganglia. Iontophoresis of cobalt or fluorescent dyes reveals DNs as uniquely identifiable elements, the dendrites of which are situated within a characteristic region of the lateral deutocerebrum. Here we demonstrate that, DNs occur as discrete groups of elements termed DN clusters (DNCs). A DNC is a characteristic combination of neurons that arises from a multiglomerular complex in which the main components of each glomerulus are a characteristic ensemble of sensory afferents. Other neurons involved in the complex are local interneurons, heterolateral interneurons that connect DNCs on both sides of the brain, and neurons originating in higher centers of the brain. We describe the structure, relationships, and projections of eight DNs that contribute to a descending neuron cluster located ventrally in the lateral deutocerebrum, an area interposed between the ventral antenna1 lobes and the laterally disposed optic lobes. We have named this cluster the GDNC because its most prominent member is the giant descending neuron (GDN), which plays a cardinal role in the midleg "jump" response and which is implicated in the initiation of flight. The GDN and its companion neurons receive primary mechanosensory aff'erents from the antennae, terminals of wide-and small-field retinotopic neurons originating in the lobula, and endings derived from sensory interneurons that originate in leg neuropil of the thoracic ganglia. We demonstrate that DNs of this cluster share morphological and functional properties. They have similar axon trajectories into the thoracic ganglia, where they invade functionally related neuropils. h'eurons of the GDNC respond to identical stimulus paradigms and share similar electrophysiological characteristics. Neither the GDN nor other members of its cluster show spontaneous activity. These neurons are reluctant to respond to unimodal stimuli, but respond to specific combinations of visual and mechanosensory stimulation. These results suggest that in flies groups of morphologically similar DNs responding to context,-specific environmental cues may cooperate in motor control.
Arthropod Structure & Development, May 1, 2011
Traditional hypotheses regarding the relationships of the major arthropod lineages focus on suite... more Traditional hypotheses regarding the relationships of the major arthropod lineages focus on suites of comparable characters, often those that address features of the exoskeleton. However, because of the enormous morphological variety among arthropods, external characters may lead to ambiguities of interpretation and definition, particularly when species have undergone evolutionary simplification and reversal. Here we present the results of a cladistic analysis using morphological characters associated with brains and central nervous systems, based on the evidence that cerebral organization is generally robust over geological time. Well-resolved, strongly supported phylogenies were obtained from a neuromorphological character set representing a variety of discrete neuroanatomical traits. Phylogenetic hypotheses from this analysis support many accepted relationships, including monophyletic Chelicerata, Myriapoda, and Hexapoda, paraphyletic Crustacea and the union of Hexapoda and Crustacea (Tetraconata). They also support Mandibulata (Myriapoda þ Tetraconata). One problematic result, which can be explained by symplesiomorphies that are likely to have evolved in deep time, is the inability to resolve Onychophora as a taxon distinct from Arthropoda. Crucially, neuronal cladistics supports the heterodox conclusion that both Hexapoda and Malacostraca are derived from a common ancestor that possessed a suite of discrete neural centers comprising an elaborate brain. Remipedes and copepods, both resolved as basal to Branchiopoda share a neural ground pattern with Malacostraca. These findings distinguish Hexapoda (Insecta) from Branchiopoda, which is the sister group of the clade Malacostraca þ Hexapoda. The present study resolves branchiopod crustaceans as descendents of an ancestor with a complex brain, which means that they have evolved secondary simplification and the loss or reduction of numerous neural systems.
Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology, Oct 1, 1991
Intracellular recording and Lucifer yellow dye filling of male fleshflies, Sarcophaga bullata, ha... more Intracellular recording and Lucifer yellow dye filling of male fleshflies, Sarcophaga bullata, have revealed male-specific neurons in the lobula, the axons of which project to the origin of premotor channels supplying flight motor neurons. Dendrites of male-specific neurons visit areas of the retinotopic mosaic supplied by the retina's acute zone, which is used by males to keep the image of a conspecific female centered during aerial pursuit. Only males engage in high-speed aerobatic chases, and male-specific neurons are suspected to underlie this behavior. Physiological determination of receptive fields of male-specific neurons substantiates the fields predicted from anatomical studies and demonstrates that they subtend the acute zone. Male-specific neurons respond in a manner predicted on theoretical grounds from observations of tracking behavior. Such properties include directional selectivity to visual motion and higher sensitivity to motion of small images than to wide-field motion. The present account substantiates and extends neuroanatomical evidence that predicts that male-specific lobula neurons comprise a distinct circuit mediating conspecific tracking.
Journal of comparative neurology, Jul 12, 1999
Previous studies of honey bee and cockroach mushroom bodies have proposed that afferent terminals... more Previous studies of honey bee and cockroach mushroom bodies have proposed that afferent terminals and intrinsic neurons (Kenyon cells) in the calyces are arranged according to polar coordinates. It has been suggested that there is a transformation by Kenyon cell axons of the polar arrangements of their dendrites in the calyces to laminar arrangements of their terminals in the lobes. Findings presented here show that cellular organization in the calyx of an evolutionarily basal neopteran, Periplaneta americana, is instead rectilinear, as it is in the lobes. It is shown that each calyx is divided into two halves (hemicalyces), each supplied by its own set of Kenyon cells. Each calyx is separately represented in the medial lobe where the dendritic trees of some efferent neurons receive inputs from one calyx only. Kenyon cell dendrites are arranged as narrow elongated fields, organized as rows in each hemicalyx. Dendritic fields arise from 14 to 16 sheets of Kenyon cell axons stacked on top of each other lining the inner surface of the calyx cup. A sheet consists of approximately 60 small bundles, each containing 5-15 axons that converge from the rim of the calyx to its neck. Each sheet contributes to a pair oflaminae, one dark one pale, called a doublet, that extends through the mushroom body. Dark laminae contain Kenyon cell axons packed with synaptic vesicles. Axons in pale laminae are sparsely equipped with vesicles. By analogy with photoreceptors, and with reference to field potential recordings, it is speculated that dark laminae are continuously active, being modulated by odor stimuli, whereas pale laminae are intermittently activated. Timm's silver staining and immunocytology reveal a second type of longitudinal division of the lobes. Five layers extend through the pedunculus and lobes, each composed of subsets of doublets. Four layers represent zones of afferent endings in the calyces. A fifth (the y layer) represents a specific type of Kenyon cell. It is concluded that the mushroom bodies comprise two independent modular systems, doublets and layers. Developmental studies show that new doublets are added at each instar to layers that are already present early in second instar nymphs. There are profound similarities between the mushroom bodies of Periplaneta, an evolutionarily basal taxon, and those of Drosophila melanogaster and the honey bee.
Journal of comparative neurology, Dec 22, 1990
In dipterous insects, a volume of behavioral and electrophysiological studies promote the content... more In dipterous insects, a volume of behavioral and electrophysiological studies promote the contention that three wide-field motion-sensitive tangential neurons provide a necessary and sufficient input to specific channels that drive the torque motor during flight. The present studies describe the results of neuroanatomical investigations of the relationships between motion-sensitive neuropil in the fly optic lobes and descending neurons that arise from a restricted area of the brain and supply segmental neck and flight motor neuropil. The present observations resolve at least 50 pairs of descending neurons supplying flight motor centers in the thoracic ganglia. The majority of descending neurons receive a distributed output from horizontal motion-sensitive neurons. However, the same descending neurons are also visited by numerous small-field retinotopic neurons from the lobula plate as well as hitherto undescribed small tangential neurons. Neuroanatomical studies, using cobalt, Golgi, and Texas red histology, demonstrate that these smaller inputs onto descending neurons have dendrites that are organized at specific strata in retinotopic neuropil and that these correspond to horizontal and vertical motion sensitivity layers. Conclusions that only a restricted number of wide-field neurons are necessary and sufficient for visually stabilized flight may be premature. Rather, neuroanatomical evidence suggests that descending neurons to the flight motor may each be selectively tuned to specific combinations of wide-and small-field visual cues, so providing a cooperative descending network controlling the rich repertoire of visually evoked flight behavior.
Journal of comparative neurology, Jul 9, 2002
Studies of the mushroom bodies of Drosophila melanogaster have suggested that their gamma lobes s... more Studies of the mushroom bodies of Drosophila melanogaster have suggested that their gamma lobes specifically support short‐term memory, whereas their vertical lobes are essential for long‐term memory. Developmental studies have demonstrated that the Drosophila gamma lobe, like its equivalent in the cockroach Periplaneta americana, is supplied by a special class of intrinsic neuron—the clawed Kenyon cells—that are the first to differentiate during early development. To date, however, no account identifies a corresponding lobe in the honey bee, another taxon used extensively for learning and memory research. Received opinion is that, in this taxon, each of the mushroom body lobes comprises three parallel divisions representing one of three concentric zones of the calyces, called the lip, collar, and basal ring. The present account shows that, although these zones are represented in the lobes, they occupy only two thirds of the vertical lobe. Its lowermost third receives the axons of the clawed class II Kenyon cells, which are the first to differentiate during early development and which represent the whole calyx. This component of the lobe is anatomically and developmentally equivalent to the gamma lobe of Drosophila and has been here named the gamma lobe of the honey bee. A new class of intrinsic neurons, originating from perikarya distant from the mushroom body, provides a second system of parallel fibers from the calyx to the gamma lobe. A region immediately beneath the calyces, called the neck, is invaded by these neurons as well as by a third class of intrinsic cell that provides connections within the neck of the pedunculus and the basal ring of the calyces. In the honey bee, the gamma lobe is extensively supplied by afferents from the protocerebrum and gives rise to a distinctive class of efferent neurons. The terminals of these efferents target protocerebral neuropils that are distinct from those receiving efferents from divisions of the vertical lobe that represent the lip, collar, and basal ring. The identification of a gamma lobe unites the mushroom bodies of evolutionarily divergent taxa. The present findings suggest the need for critical reinterpretation of studies that have been predicated on early descriptions of the mushroom body's lobes. J. Comp. Neurol. 450:4–33, 2002. © 2002 Wiley‐Liss, Inc.
Springer series in experimental entomology, 1983
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Papers by nicholas strausfeld