Novelty detection and context dependent processing of sky-compass cues in the brain of the desert locust Schistocerca gregaria

NERVOUS SYSTEMS facilitate purposeful interactions between animals and their environment, based on the perceptual powers, cognition and higher motor control. Through goal-directed behavior, the animal aims to increase its advantage and minimize risk. For instance, the migratory desert locust should profit from being fast in finding a fresh habitat, thus minimizing the investment of bodily resources in locomotion as well as the risk of starvation or capture by a predator en route. Efficient solutions to this and similar tasks – be it finding your way to work, the daily foraging of worker bees or the seasonal long-range migration of monarch butterflies - strongly depend on spatial orientation in local or global frames of reference. Local settings may include visual landmarks at stable positions that can be mapped onto egocentric space and learned for orientation, e.g. to remember a short route to a source of benefit (e.g. food) that is distant or visually less salient than the landmarks. Compass signals can mediate orientation to a global reference-frame (allothetic orienation), e.g. for locomotion in a particular compass direction or to merely ensure motion along a straight line. Whilst spatial orientation is a prerequisite of doing the planned in such tasks, animal survival in general depends on the ability to adequately respond to the unexpected, i.e. to unpredicted events such as the approach of a predator or mate. The process of identifying relevant events in the outside world that are not predictable from preceding events is termed novelty detection. Yet, the definition of ‘novelty’ is highly contextual: depending on the current situation and goal, some changes may be irrelevant and remain ´undetected´. The present thesis describes neuronal representations of a compass stimulus, correlates of novelty detection and interactions between the two in the minute brain of an insect, the migratory desert locust Schistocerca gregaria. Experiments were carried out in tethered locusts with legs and wings removed. More precisely, adult male subjects in the gregarious phase (see phase theory, Uvarov 1966) that migrates in swarms across territories in North Africa and the Middle East were used. The author performed electrophysiological recordings from single neurons in the locust brain, while either the compass stimulus (Chapter I) or events in the visual scenery (Chapter II) or combinations of both (Chapter III) were being presented to the animal. Injections of a tracer through the recording electrode, visualized by means of fluorescent-dye coupling, allowed the allocation of cellular morphologies to previously described types of neuron or the characterization of novel cell types, respectively. Recordings were focused on cells of the central complex, a higher integration area in the insect brain that was shown to be involved in the visually mediated control of goal-directed locomotion. Experiments delivered insights into how representations of the compass cue are modulated in a manner suited for their integration in the control of goal-directed locomotion. In particular, an interaction between compass-signaling and novelty detection was found, corresponding to a process in which input in one sensory domain (object vision) modulates the processing of concurrent input to a different exteroceptive sensory system (compass sense). In addition to deepening the understanding of the compass network in the locust brain, the results reveal fundamental parallels to higher context-dependent processing of sensory information by the vertebrate cortex, both with respect to spatial cues and novelty detection

Brain fiber tract plasticity in experimental spinal cord injury: diffusion tensor imaging.

Diffusion tensor imaging (DTI) and immunohistochemistry were performed in spinal cord injured rats to understand the basis for activation of multiple regions in the brain observed in functional magnetic resonance imaging (fMRI) studies. The measured fractional anisotropy (FA), a scalar measure of diffusion anisotropy, along the region encompassing corticospinal tracts (CST) indicates significant differences between control and injured groups in the 3 to 4 mm area posterior to bregma that correspond to internal capsule and cerebral peduncle. Additionally, DTI-based tractography in injured animals showed increased number of fibers that extend towards the cortex terminating in the regions that were activated in fMRI. Both the internal capsule and cerebral peduncle demonstrated an increase in GFAP-immunoreactivity compared to control animals. GAP-43 expression also indicates plasticity in the internal capsule. These studies suggest that the previously observed multiple regions of activation in spinal cord injury are, at least in part, due to the formation of new fibers

Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust, Schistocerca gregaria.

For compass orientation many insects rely on the pattern of sky polarization, but some species also exploit the sky chromatic contrast. Desert locusts, Schistocerca gregaria, detect polarized light through a specialized dorsal rim area (DRA) in their compound eye. To better understand retinal mechanisms underlying visual navigation, we compared opsin expression, spectral and polarization sensitivities and response-stimulus intensity functions in the DRA and main retina of the locust. In addition to previously characterized opsins of long-wavelength-absorbing (Lo1) and blue-absorbing visual pigments (Lo2), we identified an opsin of an ultraviolet-absorbing visual pigment (LoUV). DRA photoreceptors exclusively expressed Lo2, had peak spectral sensitivities at 441 nm and showed high polarization sensitivity (PS 1.3-31.7). In contrast, ommatidia in the main eye co-expressed Lo1 and Lo2 in five photoreceptors, expressed Lo1 in two proximal photoreceptors, and Lo2 or LoUV in one distal photoreceptor. Correspondingly, we found broadband blue- and green-peaking spectral sensitivities in the main eye and one narrowly tuned UV peaking receptor. Polarization sensitivity in the main retina was low (PS 1.3-3.8). V-log I functions in the DRA were steeper than in the main retina, supporting a role in polarization vision. Desert locusts occur as two morphs, a day-active gregarious and a night-active solitarious form. In solitarious locusts, sensitivities in the main retina were generally shifted to longer wavelengths, particularly in ventral eye regions, supporting a nocturnal lifestyle at low light levels. The data support the role of the DRA in polarization vision and suggest trichromatic colour vision in the desert locust

Novelty detection and context dependent processing of sky-compass cues in the brain of the desert locust Schistocerca gregaria

NERVOUS SYSTEMS facilitate purposeful interactions between animals and their environment, based on the perceptual powers, cognition and higher motor control. Through goal-directed behavior, the animal aims to increase its advantage and minimize risk. For instance, the migratory desert locust should profit from being fast in finding a fresh habitat, thus minimizing the investment of bodily resources in locomotion as well as the risk of starvation or capture by a predator en route. Efficient solutions to this and similar tasks – be it finding your way to work, the daily foraging of worker bees or the seasonal long-range migration of monarch butterflies - strongly depend on spatial orientation in local or global frames of reference. Local settings may include visual landmarks at stable positions that can be mapped onto egocentric space and learned for orientation, e.g. to remember a short route to a source of benefit (e.g. food) that is distant or visually less salient than the landmarks. Compass signals can mediate orientation to a global reference-frame (allothetic orienation), e.g. for locomotion in a particular compass direction or to merely ensure motion along a straight line. Whilst spatial orientation is a prerequisite of doing the planned in such tasks, animal survival in general depends on the ability to adequately respond to the unexpected, i.e. to unpredicted events such as the approach of a predator or mate. The process of identifying relevant events in the outside world that are not predictable from preceding events is termed novelty detection. Yet, the definition of ‘novelty’ is highly contextual: depending on the current situation and goal, some changes may be irrelevant and remain ´undetected´. The present thesis describes neuronal representations of a compass stimulus, correlates of novelty detection and interactions between the two in the minute brain of an insect, the migratory desert locust Schistocerca gregaria. Experiments were carried out in tethered locusts with legs and wings removed. More precisely, adult male subjects in the gregarious phase (see phase theory, Uvarov 1966) that migrates in swarms across territories in North Africa and the Middle East were used. The author performed electrophysiological recordings from single neurons in the locust brain, while either the compass stimulus (Chapter I) or events in the visual scenery (Chapter II) or combinations of both (Chapter III) were being presented to the animal. Injections of a tracer through the recording electrode, visualized by means of fluorescent-dye coupling, allowed the allocation of cellular morphologies to previously described types of neuron or the characterization of novel cell types, respectively. Recordings were focused on cells of the central complex, a higher integration area in the insect brain that was shown to be involved in the visually mediated control of goal-directed locomotion. Experiments delivered insights into how representations of the compass cue are modulated in a manner suited for their integration in the control of goal-directed locomotion. In particular, an interaction between compass-signaling and novelty detection was found, corresponding to a process in which input in one sensory domain (object vision) modulates the processing of concurrent input to a different exteroceptive sensory system (compass sense). In addition to deepening the understanding of the compass network in the locust brain, the results reveal fundamental parallels to higher context-dependent processing of sensory information by the vertebrate cortex, both with respect to spatial cues and novelty detection

Compass Cells in the Brain of an Insect Are Sensitive to Novel Events in the Visual World

<div><p>The central complex of the insect brain comprises a group of neuropils involved in spatial orientation and memory. In fruit flies it mediates place learning based on visual landmarks and houses neurons that encode the orientation for goal-directed locomotion, based on landmarks and self-motion cues for angular path-integration. In desert locusts, the central complex holds a compass-like representation of head directions, based on the polarization pattern of skylight. Through intracellular recordings from immobilized locusts, we investigated whether sky compass neurons of the central complex also represent the position or any salient feature of possible landmarks, in analogy to the observations in flies. Neurons showed strongest responses to the novel appearance of a small moving square, but we found no evidence for a topographic representation of object positions. Responses to an individual square were independent of direction of motion and trajectory, but showed rapid adaptation to successive stimulation, unaffected by changing the direction of motion. Responses reappeared, however, if the moving object changed its trajectory or if it suddenly reversed moving direction against the movement of similar objects that make up a coherent background-flow as induced by ego-motion. Response amplitudes co-varied with the precedent state of dynamic background activity, a phenomenon that has been related to attention-dependent saliency coding in neurons of the mammalian primary visual cortex. The data show that neurons of the central complex of the locust brain are visually bimodal, signaling sky compass direction and the novelty character of moving objects. These response properties might serve to attune compass-aided locomotor control to unexpected events in the environment. The difference to data obtained in fruit flies might relate to differences in the lifestyle of landmark learners (fly) and compass navigators (locust), point to the existence of parallel networks for the two orientation strategies, or reflect differences in experimental conditions.</p></div

Background activity and responses to small-field motion in four types of central-complex neuron.

<p>Subfigures show data from a CL1 neuron (A-D), TB1 neuron (A'-D'), CPU1 neuron (A''-D'') and CPU2 neuron (A'''-D''') of the central complex. A-A'''. Traces illustrating background activity. B-B'''. Spike count distribution and ISI histogram of background activity (trial duration for spike count 1 s). Asterisks and x-marks indicate the location of spike rates observed at the peak (or nadir) of the trial-averaged responses shown in D-D'''. C-C'''. Responses to presentations of a translating black, rectangular small-field square (about 2° visual angle azimuthal extent and 1.5° elevational extent) against a blank background showed fast adaptation to motion along the same trajectory. Stimulus types and periods, indicated below the recording traces, also hold for raster plots in D-D''', unless indicated otherwise. Stimulus abbreviations: f (b), forward (backward) small-field translation; H (L) trajectory with high (low) elevation. D-D'''. Raster plots and trial-averaged, Gaussian-smoothed PSTHs of additional responses. Spike rates occurring at the peak (or nadir) of the averaged response (marked by asterisks or x-marks) are located at the edges of the spike count distribution obtained from long-term background activity (see B-B'''). This indicates that responsiveness is robust across the trials shown here, but response amplitudes vary and individual responses resemble sections of background activity. In particular, arrows in A' and C' mark prominent bursts in background activity and in the phasic response period for the TB-neuron. In the two subtypes of CPU neuron (D'' and D'''), responses are independent from direction of motion. Dashed lines indicate periods of rebound-like increase in spike rate in D and a period of tonic increase in spike rate in C'. Bars, 1 s; 10 mV.</p

Gross anatomy of the locust brain, visual pathways, and relevant types of central complex neurons.

<p>A. Bilateral pathways of light-sensitive neurons from the optic lobes converge onto a network in the central complex (frontal view). Stages of early visual processing include the lamina (LA), medulla (ME) and lobula (LO) of the optic lobe. Neuropils shaded red (green) are involved in an anterior (posterior) pathway of interneurons sensitive to sky compass signals. Additional pathways (yellow neuropils) might signal optic flow and / or represent features of the visual object-background scenery. DRLA (DRME), dorsal rim area of the lamina (medulla); ALO, anterior lobe of the lobula; AME, accessory medulla; AOTU, anterior optic tubercle; POTU, posterior optic tubercle; MBU (LBU) medial (lateral) bulb; LAL, lateral accessory lobe; together with the LAL, the MBU and LBU make up the lateral complex (LX). CBL (CBU) lower (upper) division of the central body; PB, protocerebral bridge; SMP, superior medial protocerebrum; CA, calyx of mushroom body. B. Relevant cell types of the central complex (frontal view). Tangential neurons invade all slices of the CBL (TL neurons) or some slices in the PB (TB1 neurons), as well as regions in a lateral complex (TL) or layers in a POTU (TB). Columnar neurons connect distinct slices of the PB to the CBU (CPU neurons) or CBL (CL neurons) of the central body and have additional arborizations in the lateral complexes. Scale bar, 100 <i>μ</i>m.</p

Experimental setup and visual stimulation.

<p>A. Experimental setup with display showing stationary background clutter. CRT, cathode ray tube display; asterisk, fronto-dorsal corner mark of CRT; MM, micromanipulator for positioning of intracellular electrode; ELi, intracellular electrode; ELref, reference electrode; LOC, locust (viewed from dorsal); arrow, stimulated (left) eye. Note the slight tilt of the CRT and the mesh wire shielding which prevented inductive interference between display and measurement circuit. B. Region in the left antero-lateral visual field covered by the stimulus display. Arrow, position of stimulated (left) eye; asterisk, fronto-dorsal corner mark of CRT; LOC, locust (viewed from lateral). Dashed horizontal lines tagged H and L indicate high- and low-elevation trajectories for translations of single small-field squares. sr, br: commonly applied square- and bar-shaped stimulus; about 2°x1.5° and 2°x60°, respectively. Albeit both types of stimulus are shown together here, they were never presented simultaneously. B'. Terminology for directions of translational motion, illustrated according to the orientation of the diagram in B. Abbreviations are given in parentheses. Forward (backward) direction of translation is abbreviated "f" ("b") and high (low) elevation is abbreviated "H" ("L"). Thus, the term "b, L" ("f, H") refers to the backward (forward) translation of a 2°x1.5° square -29.5° (+25.5°) in elevation. See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0144501#pone.0144501.s001" target="_blank">S1 Fig</a> for commonly applied sequences of such simple stimuli. C, C'. Components (C) and time course (C') of a more complex stimulus sequence designed to mimic sudden forward small-field motion against a backward optic-background flow. The sequence begins with a stationary display of the "background clutter" pattern, followed by repeated backward translations of the entire pattern (indicated by horizontal arrows) in an optic-flow like manner at 70°/s (dashed horizontal line in C'). In the late phase of the sequence, an individual object in the background flow (short vertical arrows in C) pops out of it twice by changing its direction of motion, i.e. the object suddenly moved forward against the backward background flow (absolute velocity 80°/s; velocity relative to background flow -150°/s). The object, a black, rectangle square of about 2° visual angle azimuthal extent and 1.5° elevational extent, is identical to the one used in the simple stimulus regimes and moves at the same high elevation of 25.5° also applied in the latter. For further details on stimuli, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0144501#sec002" target="_blank">Materials and Methods</a>.</p

SYCL compute kernels for ExaHyPE *

We discuss three SYCL realisations of a simple Finite Volume scheme over multiple Cartesian patches. The realisation flavours differ in the way how they map the compute steps onto loops and tasks: We compare an implementation that is exclusively using a sequence of for-loops to a version that uses nested parallelism, and finally benchmark these against a version modelling the calculations as task graph. Our work proposes realisation idioms to realise these flavours within SYCL. The results suggest that a mixture of classic task and data parallelism performs if we map this hybrid onto a solely data-parallel SYCL implementation, taking into account SYCL specifics and the problem size

Modulation of responses to moving small-field objects by variable background activity.

<p>A. Raster plots show selected responses to a translating small-field square (dashed line: stimulus window) which are modulated by relatively low states (left subplot) and relatively high states (right subplot) of precedent background activity (BA). The relevant period of background activity may roughly cover the last 500 ms (grey shading) preceding the stimulus. B. Correlation analysis in CPU neurons. Spike counts within the first (second) 700 ms-window during stimulus presentation were plotted against those in the 700 ms-window of background activity directly preceding the stimulus. Data points close to or above the bisecting line correspond to trials that lacked the inhibitory response typical for CPU neurons; strongest responses are reflected by data points closest to the x-axis. Data were obtained from 3 CPU1- and 4 CPU2 neurons and cover 62 responses to the first stimulus in sequences of single small-field squares translating against a blank background; different plot marks correspond to different neurons. Plot marks are not scaled to the frequency of observations, thus identical values from the same experiment appear as a single data point. Dotted lines show linear regressions. C. Response amplitudes compared to different states of background activity. Box plots show distributions of relative response amplitudes (changes in spike rate relative to different levels of background activity). These were calculated for responses to the first stimulus in a respective sequence of small-field squares translating against a blank background (N responses from n neurons). For estimation of relative response amplitudes, we subtracted the spike rates of different levels of background activity (1s bins), obtained from the same respective cell throughout the entire experiment. These levels include the median and two additional quantiles of the background activity's spike count distribution that lie beyond the median in the same side of the distribution as expected for responses. In case of the inhibitory responses in CL- and CPU neurons, the 25% and 2.5% quantile of the spike rate distribution were used. For the excitatory responses of TB neurons, the 75% and 97.5% quantile provide relevant normalization. Indicated above each box-plot is the result of a two-sided sign test for zero median (* <i>p</i>_<i>corr</i><0.05, ** <i>p</i>_<i>corr</i><0.01, *** <i>p</i>_<i>corr</i><0.001, ns not significant). Note that a non-significant test result here does not imply that responses did not involve a significant change in spike rate as compared to the local background activity that <i>actually</i> preceded the responses (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0144501#pone.0144501.g004" target="_blank">Fig 4A</a>). While responses are relatively robust compared to the median levels of background activity (left columns of subplots), the additional response-type specific normalizations (middle and right columns) reveal that more extreme levels of background activity may result in masking of responses, as the difference to zero change decreases substantially and may become non-significant. Notches in box plots indicate 95% confidence interval of the median. Some outliers were truncated for the sake of better visualization.</p