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N J Strausfeld

Publications and source records attributed to N J Strausfeld.

At least 37 records · Page 2Linked to original sources

Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates.

Conserved neural characters identified in the brains of a variety of segmented invertebrates and outgroups have been used to reconstruct phylogenetic relationships. The analysis suggests that insects and crustaceans are sister groups and that the 'myriapods' are an artificial construct comprising unrelated chilopods and diplopods. Certain elements of the optic lobes and mid-brain support the notion that insects are more closely related to crustaceans than they are to any other arthropods. However, deep optic neuropils and optic chiasmata are homoplastic in insects and crustaceans. The organization of olfactory pathways suggests that insect olfactory lobes originated late, probably first appearing in orthopteroid or blattoid pterygotes. The present results are discussed with respect to recent studies on early development of arthropod nervous systems and the fossil record.

Animals↗

Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana.

Mushroom bodies are paired centers in insect brains that are thought to be crucial in olfactory learning and memory. Early neuroanatomical descriptions suggested that the mushroom bodies comprise rather simple arrangements of nerve cells. Intrinsic neurons within each mushroom body were believed to receive olfactory afferents and to supply long, branched axons to extrinsic neurons that lead from the mushroom body into the protocerebrum. More recent suggestions that the mushroom bodies integrate several sensory modalities find support from intracellular and extracellular recordings of extrinsic neurons in the brains of crickets, honey bees, and cockroaches. Here, we describe two major classes of extrinsic neurons, simple and complex cells, in the mushroom bodies of the cockroach Periplaneta americana. Each class is defined by its pattern of branching in the brain. Simple neurons correspond to extrinsic neurons described from other species that have one set of dendrites only within the mushroom bodies. Complex extrinsic neurons possess dendrite-like branches within and outside the mushroom bodies. This arrangement may account in part for their observed multimodality, as might newly identified afferent neurons that terminate in the mushroom body lobes among the dendrites of extrinsic neurons and that respond to multimodal stimuli. Organizational complexity within the mushroom bodies is suggested by the grouping of intrinsic cell axons into discrete laminae. These are intersected by the block-like arrangements of dendritic fields of extrinsic neurons in a manner reminiscent of Purkinje cell dendrites intersecting parallel fibers in the cerebellum. The present results demonstrate that the cockroach mushroom body processes multimodal sensory information and that its neural arrangements contribute to a precise architecture consisting of discrete longitudinal and transverse subdivisions.

Animals↗

The relevance of neural architecture to visual performance: phylogenetic conservation and variation in Dipteran visual systems.

In cyclorrhaphan flies, giant tangential neurons in the lobula plate are supplied by isomorphic arrays of evolutionarily conserved achromatic elementary motion detecting circuits originating in the retina. The arrangements among giant tangential neurons is characteristic of a taxon and can differ between taxa having different visual performances. Observations of 12 brachyceran and 4 nematoceran species have identified different behaviors associated with visually stabilized flight. Neuroanatomical comparisons between closely related species having different behaviors and phylogenetically distant species that have similar behaviors suggest that such differences relate to differences of giant tangential cell architecture in the lobula plate. These functionally related differences contrast to anatomical features that reflect phylogenetic affinities. For example, the lobula plates of robber flies, typified by ballistic flight behavior, all differ from other taxa in lacking cyclorrhaphan-type vertical motion-sensitive neurons; instead, they possess an extra complement of horizontal cells in their place. The results suggest that, although circuits that compute elementary motion are conserved across the Diptera, selective pressure has resulted in modifications of their target neurons, thus contributing to the wide variety of visual behaviors observed within this group of insects.

Animals↗

Visual motion-detection circuits in flies: parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate.

The neural circuitry of motion processing in insects, as in primates, involves the segregation of different types of visual information into parallel retinotopic pathways that subsequently are reunited at higher levels. In insects, achromatic, motion-sensitive pathways to the lobula plate are separated from color-processing pathways to the lobula. Further parallel subdivisions of the retinotopic pathways to the lobula plate have been suggested from anatomical observations. Here, we provide direct physiological evidence that the two most prominent of these latter pathways are, indeed, functionally distinct: recordings from the retinotopic pathway defined by small-field bushy T-cells (T4) demonstrate only weak directional selectivity to motion, in striking contrast with previously demonstrated strong directional selectivity in the second, T5-cell, pathway. Additional intracellular recordings and anatomical descriptions have been obtained from other identified neurons that may be crucial in early motion detection and processing: a deep medulla amacrine cell that seems well suited to provide the lateral interactions among retinotopic elements required for motion detection; a unique class of Y-cells that provide small-field, directionally selective feedback from the lobula plate to the medulla; and a new heterolateral lobula plate tangential cell that collates directional, motion-sensitive inputs. These results add important new elements to the set of identified neurons that process motion information. The results suggest specific hypotheses regarding the neuronal substrates for motion-processing circuitry and corroborate behavioral studies in bees that predict distinct pathways for directional and nondirectional motion.

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Visual motion-detection circuits in flies: small-field retinotopic elements responding to motion are evolutionarily conserved across taxa.

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 applicaton 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 motion-detecting 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 neurons, or the absence of orientation-specific motion-sensitive levels in the lobula plate.

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Oculomotor control in calliphorid flies: organization of descending neurons to neck motor neurons responding to visual stimuli.

In insects, head movements are mediated by neck muscles supplied by nerves originating in the brain and prothoracic ganglion. Extracellular recordings of the nerves demonstrate units that respond to visual stimulation of the compound eyes and to mechanosensory stimulation of the halteres. The number of neck muscles required for optokinetic eye movements in flies is not known, although in other taxa, eye movements can involve as few as three pairs of muscles. This study investigates which neck motor neurons are likely to be involved in head movements by examining the relationships between neck muscle motor neurons and the terminals visiting them from approximately 50 pairs of descending neurons. Many of these descending neurons have dendrites in neuropils that are associated with modalities other than vision, and recording show that visual stimuli activate only a few neck motor neurons, such as the sclerite depressor neurons, which respond to local or wide-field, directionally specific motion, as do a subset of descending neurons coupled to them. The results suggest that, like in the vertebrate eye or the retinas of jumping spiders, optokinetic head movements of flies require only a few muscles. In addition to the importance of visual inputs, a major supply to neck muscle centers by nonvisual descending neurons suggests a role for tactile, gustatory, and olfactory signals in controlling head position.

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Oculomotor control in calliphorid flies: head movements during activation and inhibition of neck motor neurons corroborate neuroanatomical predictions.

In tethered flying flies, moving contrast gratings or small spots elicit head movements which are suited to track retinal images moving at velocities up to 3,000 degrees/sec (about 50 Hz contrast frequency for gratings of spatial wavelength 15 degrees). To investigate the neural basis of these movements we have combined videomicroscopy with electrophysiological stimulation and recording to demonstrate that excitation of prothoracic motor neurons projecting in the anterodorsal (ADN) and frontal nerves (FN), respectively, generates the yaw and roll head movements measured behaviorally. Electrical stimulation of the ADN produces head yaw. The visual stimuli which excite the two ADN motor neurons (ADN MNs) are horizontal motion of gratings or spots moving clockwise around the yaw axis in the case of the right ADN (counterclockwise for left ADN). Activity is inhibited by motion in the opposite direction. Spatial sensitivity varies in the yaw plane with a maximum between 0 degree and 40 degrees ipsilaterally, but both excitation and inhibition are elicited out to 80 degrees in the ipsilateral and contralateral fields. ADN MNs respond to contrast frequencies up to 15-20 Hz, with a peak around 2-4 Hz for grating motion in the excitatory or inhibitory directions. Electrical stimulation of the FN primarily elicits roll down to the ipsilateral side. The one FN MN consistently driven by visual stimulation is excited by downward motion and inhibited by upward motion at 80 degrees azimuth in the ipsilateral visual field. At -80 degrees contralateral, visual motion has the opposite effect: Upward is excitatory and downward is inhibitory. The FN MN is tuned to contrast frequencies in the same range as the ADN MNs, with peak sensitivity around 4 Hz. The functional organization of inputs to the ADN and FN is discussed with respect to identified visual interneurons and parallel pathways controlling motor output.

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Oculomotor control in calliphorid flies: GABAergic organization in heterolateral inhibitory pathways.

In calliphorid Diptera, motor neurons mediating visually evoked head movements can be excited or inhibited by visual stimuli, depending on the directionality of the stimulus and whether it is in the ipsi- or contralateral visual field. The level at which inhibition occurs is of special interest because binocular activation of homolateral tangential neurons in the lobula plate demonstrates that excitatory interaction must occur between the left and right optic lobes. Recordings and dye fillings demonstrate a variety of motion-sensitive heterolateral pathways between the lobula plates, or between them and contralateral deutocerebral neuropil, which provides descending pathways to neck motor centers. The profiles of heterolateral tangential cells correspond to neurons stained by an antibody against gamma-aminobutyric acid (GABA). Other GABA-immunoreactive interneurons linking each side of the brain correspond to uniquely identified motion-sensitive neurons linking the deutocerebral. Additional inhibitory pathways include heterolateral GABAergic descending and ascending neurons, as well as heterolateral GABAergic neurons in the thoracic ganglia. The functional significance of heterolateral GABAergic pathways was tested surgically by making selective microlesions and monitoring the oculomotor output. The results demonstrate an important new attribute of the insect visual system. Although lesions can initially abolish an excitatory or inhibitory response, this response is reestablished through alternative pathways that provide inhibitory and excitatory information to the same motor neurons.

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Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns.

Phylogenetically conserved brain centers known as mushroom bodies are implicated in insect associative learning and in several other aspects of insect behavior. Kenyon cells, the intrinsic neurons of mushroom bodies, have been generally considered to be disposed as homogenous arrays. Such a simple picture imposes constraints on interpreting the diverse behavioral and computational properties that mushroom bodies are supposed to perform. Using a P[GAL4] enhancer-trap approach, we have revealed axonal processes corresponding to intrinsic cells of the Drosophila mushroom bodies. Rather than being homogenous, we find the Drosophila mushroom bodies to be compound neuropils in which parallel subcomponents exhibit discrete patterns of gene expression. Different patterns correspond to hitherto unobserved differences in Kenyon cell trajectory and placement. On the basis of this unexpected complexity, we propose a model for mushroom body function in which parallel channels of information flow, perhaps with different computational properties, subserve different behavioral roles.

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Visual motion detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons.

Giant motion-sensitive tangential neurons in the lobula plate are thought to be cardinal elements in the oculomotor pathways of flies. However, these large neurons do not themselves compute motion, and elementary motion detectors have been proposed only from theory. Here we identify the forms, projections, and responses of small-field retinotopic neurons that comprise a well known pathway from the retina to the lobula plate. Already at the level of the second and third synapses beneath the photoreceptor layer, certain of these small elements show responses that distinguish motion from flicker. At a level equivalent to the vertebrate inner plexiform layer (the fly's outer medulla) at least one retinotopic element is directionally selective. At the inner medulla, small retinotopic neurons with bushy dendrites extending through a few neighboring columns leave the inner medulla and supply inputs onto lobula plate tangentials. These medulla relays have directionally selective responses that are indistinguishable from those of large-field tangentials except for their amplitude and modulation with contrast frequency. Centrifugal neurons leading back from the inner medulla out to the lamina also show orientation-selective responses to motion. The results suggest that specific cell types between the lamina and inner medulla correspond to stages of the Hassenstein-Reichardt correlation model of motion detection.

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Two visual systems in one brain: neuropils serving the secondary eyes of the spider Cupiennius salei.

Like other araneans, the wandering spider Cupiennius salei is equipped with one pair of principal eyes and three pairs of secondary eyes. Primary and secondary eyes serve two distinct sets of visual neuropils in the brain. This paper describes cellular organization in neuropils supplied by the secondary eyes, which individually send axons into three laminas resembling their namesakes serving insect superposition eyes. Secondary eye photoreceptors send axons to small-field projection neurons (L-cells) which extend from each lamina to supply three separate medullas. Each medulla is a vault of neuropil comprising only a few morphological types of neurons. These can be compared to a subset of retinotopic neurons in the medullas of calliphorid Diptera supplying giant motion-sensitive neurons in the lobula plate. In Cupiennius, neurons from secondary eye medullas converge at a single target neuropil called the "mushroom body." This region contains giant output neurons which, like their counterparts in the calliphorid lobula plate, lead to descending pathways that supply thoracic motor circuits. It is suggested that the cellular arrangements serving Cupiennius's secondary eyes are color independent pathways specialized for detecting horizontal motion. The present results do not support the classical view that the spider "mushroom body" is phylogenetically homologous or functionally analogous to its namesake in insects.

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Two visual systems in one brain: neuropils serving the principal eyes of the spider Cupiennius salei.

Principal (anterior median) eyes of the wandering spider Cupiennius are served by three successive neuropils, the organization of which is distinct from those serving secondary eyes. Photoreceptors terminate in the first optic neuropil amongst second order neurons with overlapping dendritic fields. Second order neurons terminate at various depths in anterior median eye medulla where they are visited by bush-like dendritic trees of third order projection neurons. These supply tracts which extend into the "central body." This crescent-shaped neuropil lies midsagittally in the rear of the brain near its dorsal surface. It is organized into columns and it supplies both columnar and tangential efferents to other brain centers. The supply to and organization of the "central body" neuropil is reminiscent of retinotopic neuropils supplying the lobula of insects. Channels to the "central body" comprise one of two concurrent visual pathways, the other provided by the secondary eyes supplying the "mushroom body." We suggest that principal eye pathways may be involved in form and texture perception whereas secondary eyes detect motion, as is known for jumping spiders. Our data do not support Hanström's classical view that the "central body" is specifically associated with web-building, nor that it is homologous to its namesake in insect brains.

Afferent Pathways↗

Small-field neurons associated with oculomotor control in muscoid flies: cellular organization in the lobula plate.

In muscoid flies, the lobula plate is the last station in the optic lobes for processing spectrally independent information from retinotopic afferents. Until recently, it was thought that most lobula plate neurons were color-insensitive wide-field tangential neurons that respond to direction-specific motion. It has been suggested that certain of these supply inputs to premotor descending neurons involved in the control of flight and head movements. The present account describes a Golgi and cobalt-silver analysis that reports evidence for additional lobula plate outputs, which are numerically complex and structurally elaborate. Beneath a retina with approximately 4,000 ommatidia, each of at least 15 populations of morphologically distinct small-field neurons comprises approximately 110-440 elements that contribute to an isomorphic neural assembly subtending the whole retina. Morphologically small-field efferents form three classes according to the origin of their axons and their arborization in the lobula plate and lobula. Neurons arising from the lobula plate, or shared by it and the lobula, visit dorsal descending neurons supplying the neck and flight motor in contrast to output neurons from the lobula, which project to ventral descending neurons supplying leg motor neuropils. The possible functional significance of small-field lobula plate outputs onto descending neurons in the dorsal deutocerebrum is discussed.

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Small-field neurons associated with oculomotor and optomotor control in muscoid flies: functional organization.

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 degrees 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.

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Premotor descending neurons responding selectively to local visual stimuli in flies.

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.

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Structural organization of male-specific visual neurons in calliphorid optic lobes.

The superiority of male flies over female flies in locating and intercepting small rapidly moving targets has been ascribed to differences in their visual systems. In males, this sexual dimorphism is externally expressed by an area of high visual acuity called the acute zone. Selective cobalt uptake reveals 12 types of male-specific visual interneurons in the male lobula, the axons of which terminate in neuropil supplying premotor descending neurons to neck and flight motor circuits. The dendritic fields of the individual male-specific neurons can be extrapolated out into visual space to demonstrate that each is assigned a discrete area of the visual panorama. The dendritic fields of 10 of the 12 male-specific neurons subtend areas of the retina associated with the male acute zone. The functional significance of male-specific neurons is discussed with respect to their putative receptive field and a model circuit for target location by male flies.

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The functional organization of male-specific visual neurons in flies.

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.

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