Ronny Rosner | Newcastle University (original) (raw)
Papers by Ronny Rosner
Journal of Physiology-Paris, 2013
Journal of Comparative Physiology A
Praying mantids are the only insects proven to have stereoscopic vision (stereopsis): the ability... more Praying mantids are the only insects proven to have stereoscopic vision (stereopsis): the ability to perceive depth from the slightly shifted images seen by the two eyes. Recently, the first neurons likely to be involved in mantis stereopsis were described and a speculative neuronal circuit suggested. Here we further investigate classes of neurons in the lobula complex of the praying mantis brain and their tuning to stereoscopically-defined depth. We used sharp electrode recordings with tracer injections to identify visual projection neurons with input in the optic lobe and output in the central brain. In order to measure binocular response fields of the cells the animals watched a vertical bar stimulus in a 3D insect cinema during recordings. We describe the binocular tuning of 19 neurons projecting from the lobula complex and the medulla to central brain areas. The majority of neurons (12/19) were binocular and had receptive fields for both eyes that overlapped in the frontal region. Thus, these neurons could be involved in mantis stereopsis. We also find that neurons preferring different contrast polarity (bright vs dark) tend to be segregated in the mantis lobula complex, reminiscent of the segregation for small targets and widefield motion in mantids and other insects.
The Journal of Experimental Biology
The central complex, a group of midline neuropils in the insect brain, plays a key role in spatia... more The central complex, a group of midline neuropils in the insect brain, plays a key role in spatial orientation and navigation. Work in locusts, crickets, dung beetles, bees and butterflies suggests that it harbors a network of neurons which determines the orientation of the insect relative to the pattern of polarized light in the blue sky. In locusts, these 'compass cells' also respond to simulated approaching objects. Here, we investigated in the locust Schistocerca gregaria whether compass cells change their activity when the animal experiences large-field visual motion or when the animal is engaged in walking behavior. We recorded intracellularly from these neurons while the tethered animals were allowed to perform walking movements on a slippery surface. We concurrently presented moving grating stimuli from the side or polarized light through a rotating polarizer from above. Large-field motion was combined with simulation of approaching objects to evaluate whether responses differed from those presented on a stationary background. We show for the first time that compass cells are sensitive to large-field motion. Responses to looming stimuli were often more conspicuous during large-field motion. Walking activity influenced spiking rates at all stages of the network. The strength of responses to the plane of polarized light was affected in some compass cells during leg motor activity. The data show that signaling in compass cells of the locust central complex is modulated by visual context and locomotor activity.
Journal of Comparative Neurology
The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting o... more The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting of the protocerebral bridge (PB), the upper (CBU) and lower division (CBL) of the central body and a pair of globular noduli. It receives prominent input from the visual system and plays a major role in spatial orientation of the animals. Vertical slices and horizontal layers of the CX are formed by columnar, tangential, and pontine neurons.
A puzzle for neuroscience - and robotics - is how insects achieve surprisingly complex behaviours... more A puzzle for neuroscience - and robotics - is how insects achieve surprisingly complex behaviours with such tiny brains1,2. One example is depth perception via binocular stereopsis in the praying mantis, a predatory insect. Praying mantids use stereopsis, the computation of distances from disparities between the two retinas, to trigger a raptorial strike of their forelegs3,4 when prey is within reach. The neuronal basis of this ability is entirely unknown. From behavioural evidence, one view is that the mantis brain must measure retinal disparity locally across a range of distances and eccentricities4–7, very like disparity-tuned neurons in vertebrate visual cortex8. Sceptics argue that this “retinal disparity hypothesis” implies far too many specialised neurons for such a tiny brain9. Here we show the first evidence that individual neurons in the praying mantis brain are indeed tuned to specific disparities and eccentricities, and thus locations in 3D-space. This disparity informat...
Apparent motion is the perception of a motion created by rapidly presenting still frames in which... more Apparent motion is the perception of a motion created by rapidly presenting still frames in which objects are displaced in space. Observers can reliably discriminate the direction of apparent motion when inter-frame object displacement is below a certain limit, Dmax. Earlier studies of motion perception in humans found that Dmax scales with spatial element size, interpreting the relationship between the two as linear, and that Dmax appears to be lower-bounded at around 15 arcmin. Here, we run corresponding experiments in the praying mantis Sphodromantis lineola to investigate how Dmax scales with element size. We used moving random chequerboard patterns of varying element and displacement step sizes to elicit the optomotor response, a postural stabilization mechanism that causes mantids to lean in the direction of large-field motion. Subsequently, we calculated Dmax as the displacement step size corresponding to a 50% probability of detecting an optomotor response in the same direct...
Recently, we showed a novel property of the Hassenstein-Reichardt detector: namely, that insect m... more Recently, we showed a novel property of the Hassenstein-Reichardt detector: namely, that insect motion detection can be masked by “invisible” noise, i.e. visual noise presented at spatial frequencies to which the animals do not respond when presented as a signal. While this study compared the effect of noise on human and insect motion perception, it used different ways of quantifying masking in two species. This was because the human studies measured contrast thresholds, which were too time-consuming to acquire in the insect given the large number of stimulus parameters examined. Here, we run longer experiments in which we obtained contrast thresholds at just two signal and two noise frequencies. We examine the increase in threshold produced by noise at either the same frequency as the signal, or a different frequency. We do this in both humans and praying mantises (Sphodromantis lineola), enabling us to compare these species directly in the same paradigm. Our results confirm our ea...
Journal of Comparative Neurology
Newcastle University ePrints -eprint.ncl.ac.uk Rosner R, von Hadeln J, Salden T, Homberg U. Anato... more Newcastle University ePrints -eprint.ncl.ac.uk Rosner R, von Hadeln J, Salden T, Homberg U. Anatomy of the lobula complex in the brain of the praying mantis compared to the lobula complexes of the locust and cockroach.
The motion energy model is the standard account of motion detection in animals from beetles to hu... more The motion energy model is the standard account of motion detection in animals from beetles to humans. Despite this common basis, we show here that a difference in the early stages of visual processing between mammals and insects leads this model to make radically different behavioural predictions. In insects, early filtering is spatially lowpass, which makes the surprising prediction that motion detection can be impaired by “invisible” noise, i.e. noise at a spatial frequency that elicits no response when presented on its own as a signal. We confirm this prediction using the optomotor response of praying mantis Sphodromantis lineola. This does not occur in mammals, where spatially bandpass early filtering means that linear systems techniques, such as deriving channel sensitivity from masking functions, remain approximately valid. Counter-intuitive effects such as masking by invisible noise may occur in neural circuits wherever a nonlinearity is followed by a difference operation.
Biochemical substances are sensitively recognized and processed by living cells, either to provid... more Biochemical substances are sensitively recognized and processed by living cells, either to provide life-energy or to trigger an adequate cell-type specific response. For on-line monitoring of cellular reactions we develop(ed) different Cell Monitoring Systems (CMS ® ). In the last years we ...
Scientific Reports, 2016
Stereopsis -3D vision -has become widely used as a model of perception. However, all our knowledg... more Stereopsis -3D vision -has become widely used as a model of perception. However, all our knowledge of possible underlying mechanisms comes almost exclusively from vertebrates. While stereopsis has been demonstrated for one invertebrate, the praying mantis, a lack of techniques to probe invertebrate stereopsis has prevented any further progress for three decades. We therefore developed a stereoscopic display system for insects, using miniature 3D glasses to present separate images to each eye, and tested our ability to deliver stereoscopic illusions to praying mantises. We find that while filtering by circular polarization failed due to excessive crosstalk, "anaglyph" filtering by spectral content clearly succeeded in giving the mantis the illusion of 3D depth. We thus definitively demonstrate stereopsis in mantises and also demonstrate that the anaglyph technique can be effectively used to deliver virtual 3D stimuli to insects. This method opens up broad avenues of research into the parallel evolution of stereoscopic computations and possible new algorithms for depth perception.
The Journal of neuroscience : the official journal of the Society for Neuroscience, Jan 8, 2013
In many situations animals are confronted with approaching objects. Depending on whether the appr... more In many situations animals are confronted with approaching objects. Depending on whether the approach represents a potential threat or is intended during a goal-oriented approach, the adequate behavioral strategies differ. In all of these cases the visual system experiences an expanding or looming shape. The neuronal machinery mediating looming elicited behavioral responses has been studied most comprehensively in insects but is still far from being fully understood. It is particularly unknown how insects adjust their behavior to objects approaching from different directions. A brain structure that is thought to play an important role in spatial orientation in insects is the central complex (CC). We investigated whether CC neurons process information about approaching objects on a collision course. We recorded intracellularly from CC neurons in the locust Schistocerca gregaria during visual stimulation via lateral LCD screens. Many neurons in the locust CC, including columnar and ta...
Genetic manipulations of neuronal activity are a corner stone of studies aimed to 78 identify the... more Genetic manipulations of neuronal activity are a corner stone of studies aimed to 78 identify the functional impact of defined neurons for animal behavior. With its small 79 nervous system, rapid life cycle and genetic amenability, the fruit fly Drosophila 80 melanogaster provides an attractive model system to study neuronal circuit function. 81
Journal of Experimental Biology, 2010
The strength of stimulus-induced responses at the neuronal and the behavioural level often depend... more The strength of stimulus-induced responses at the neuronal and the behavioural level often depends on the internal state of an animal. Within pathways processing sensory information and eventually controlling behavioural responses, such gain changes can originate at several sites. Using motion-sensitive lobula plate tangential cells (LPTCs) of blowflies, we address whether and in which way information processing changes for two different states of motor activity. We distinguish between the two states on the basis of haltere movements. Halteres are the evolutionarily transformed hindwings of flies. They oscillate when the animals walk or fly. LPTCs mediate, amongst other behaviours, head optomotor responses. These are either of large or small amplitude depending on the state of motor activity. Here we find that LPTC responses also depend on the motor activity of flies. In particular, LPTC responses are enhanced when halteres oscillate. Nevertheless, the response changes of LPTCs do not account for the corresponding large gain changes of head movements. Moreover, haltere activity itself does not change the activity of LPTCs. Instead, we propose that a central signal associated with motor activity changes the gain of head optomotor responses and the response properties of LPTCs.
Journal of Experimental Biology, 2009
Behavioural responses of an animal are variable even when the animal experiences the same sensory... more Behavioural responses of an animal are variable even when the animal experiences the same sensory input several times. This variability can arise from stochastic processes inherent to the nervous system. Also, the internal state of an animal may influence a particular behavioural response. In the present study, we analyse the variability of visually induced head pitch responses of tethered blowflies by high-speed cinematography. We found these optomotor responses to be highly variable in amplitude. Most of the variability can be attributed to two different internal states of the flies with high and low optomotor gain, respectively. Even within a given activity state, there is some variability of head optomotor responses. The amount of this variability differs for the two optomotor gain states. Moreover, these two activity states can be distinguished on a fine timescale and without visual stimulation, on the basis of the occurrence of peculiar head jitter movements. Head jitter goes along with high gain optomotor responses and haltere oscillations. Halteres are evolutionary transformed hindwings that oscillate when blowflies walk or fly. Their main function is to serve as equilibrium organs by detecting Coriolis forces and to mediate gaze stabilisation. However, their basic oscillating activity was also suggested to provide a gain-modulating signal. Our experiments demonstrate that halteres are not necessary for high gain head pitch to occur. Nevertheless, we find the halteres to be responsible for one component of head jitter movements. This component may be the inevitable consequence of their function as equilibrium and gaze-stabilising organs.
PLoS ONE, 2011
Behavioral responses of an animal vary even when they are elicited by the same stimulus. This var... more Behavioral responses of an animal vary even when they are elicited by the same stimulus. This variability is due to stochastic processes within the nervous system and to the changing internal states of the animal. To what extent does the variability of neuronal responses account for the overall variability at the behavioral level? To address this question we evaluate the neuronal variability at the output stage of the blowfly's (Calliphora vicina) visual system by recording from motion-sensitive interneurons mediating head optomotor responses. By means of a simple modelling approach representing the sensorymotor transformation, we predict head movements on the basis of the recorded responses of motion-sensitive neurons and compare the variability of the predicted head movements with that of the observed ones. Large gain changes of optomotor head movements have previously been shown to go along with changes in the animals' activity state. Our modelling approach substantiates that these gain changes are imposed downstream of the motion-sensitive neurons of the visual system. Moreover, since predicted head movements are clearly more reliable than those actually observed, we conclude that substantial variability is introduced downstream of the visual system.
Journal of Physiology-Paris, 2013
Journal of Comparative Physiology A
Praying mantids are the only insects proven to have stereoscopic vision (stereopsis): the ability... more Praying mantids are the only insects proven to have stereoscopic vision (stereopsis): the ability to perceive depth from the slightly shifted images seen by the two eyes. Recently, the first neurons likely to be involved in mantis stereopsis were described and a speculative neuronal circuit suggested. Here we further investigate classes of neurons in the lobula complex of the praying mantis brain and their tuning to stereoscopically-defined depth. We used sharp electrode recordings with tracer injections to identify visual projection neurons with input in the optic lobe and output in the central brain. In order to measure binocular response fields of the cells the animals watched a vertical bar stimulus in a 3D insect cinema during recordings. We describe the binocular tuning of 19 neurons projecting from the lobula complex and the medulla to central brain areas. The majority of neurons (12/19) were binocular and had receptive fields for both eyes that overlapped in the frontal region. Thus, these neurons could be involved in mantis stereopsis. We also find that neurons preferring different contrast polarity (bright vs dark) tend to be segregated in the mantis lobula complex, reminiscent of the segregation for small targets and widefield motion in mantids and other insects.
The Journal of Experimental Biology
The central complex, a group of midline neuropils in the insect brain, plays a key role in spatia... more The central complex, a group of midline neuropils in the insect brain, plays a key role in spatial orientation and navigation. Work in locusts, crickets, dung beetles, bees and butterflies suggests that it harbors a network of neurons which determines the orientation of the insect relative to the pattern of polarized light in the blue sky. In locusts, these 'compass cells' also respond to simulated approaching objects. Here, we investigated in the locust Schistocerca gregaria whether compass cells change their activity when the animal experiences large-field visual motion or when the animal is engaged in walking behavior. We recorded intracellularly from these neurons while the tethered animals were allowed to perform walking movements on a slippery surface. We concurrently presented moving grating stimuli from the side or polarized light through a rotating polarizer from above. Large-field motion was combined with simulation of approaching objects to evaluate whether responses differed from those presented on a stationary background. We show for the first time that compass cells are sensitive to large-field motion. Responses to looming stimuli were often more conspicuous during large-field motion. Walking activity influenced spiking rates at all stages of the network. The strength of responses to the plane of polarized light was affected in some compass cells during leg motor activity. The data show that signaling in compass cells of the locust central complex is modulated by visual context and locomotor activity.
Journal of Comparative Neurology
The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting o... more The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting of the protocerebral bridge (PB), the upper (CBU) and lower division (CBL) of the central body and a pair of globular noduli. It receives prominent input from the visual system and plays a major role in spatial orientation of the animals. Vertical slices and horizontal layers of the CX are formed by columnar, tangential, and pontine neurons.
A puzzle for neuroscience - and robotics - is how insects achieve surprisingly complex behaviours... more A puzzle for neuroscience - and robotics - is how insects achieve surprisingly complex behaviours with such tiny brains1,2. One example is depth perception via binocular stereopsis in the praying mantis, a predatory insect. Praying mantids use stereopsis, the computation of distances from disparities between the two retinas, to trigger a raptorial strike of their forelegs3,4 when prey is within reach. The neuronal basis of this ability is entirely unknown. From behavioural evidence, one view is that the mantis brain must measure retinal disparity locally across a range of distances and eccentricities4–7, very like disparity-tuned neurons in vertebrate visual cortex8. Sceptics argue that this “retinal disparity hypothesis” implies far too many specialised neurons for such a tiny brain9. Here we show the first evidence that individual neurons in the praying mantis brain are indeed tuned to specific disparities and eccentricities, and thus locations in 3D-space. This disparity informat...
Apparent motion is the perception of a motion created by rapidly presenting still frames in which... more Apparent motion is the perception of a motion created by rapidly presenting still frames in which objects are displaced in space. Observers can reliably discriminate the direction of apparent motion when inter-frame object displacement is below a certain limit, Dmax. Earlier studies of motion perception in humans found that Dmax scales with spatial element size, interpreting the relationship between the two as linear, and that Dmax appears to be lower-bounded at around 15 arcmin. Here, we run corresponding experiments in the praying mantis Sphodromantis lineola to investigate how Dmax scales with element size. We used moving random chequerboard patterns of varying element and displacement step sizes to elicit the optomotor response, a postural stabilization mechanism that causes mantids to lean in the direction of large-field motion. Subsequently, we calculated Dmax as the displacement step size corresponding to a 50% probability of detecting an optomotor response in the same direct...
Recently, we showed a novel property of the Hassenstein-Reichardt detector: namely, that insect m... more Recently, we showed a novel property of the Hassenstein-Reichardt detector: namely, that insect motion detection can be masked by “invisible” noise, i.e. visual noise presented at spatial frequencies to which the animals do not respond when presented as a signal. While this study compared the effect of noise on human and insect motion perception, it used different ways of quantifying masking in two species. This was because the human studies measured contrast thresholds, which were too time-consuming to acquire in the insect given the large number of stimulus parameters examined. Here, we run longer experiments in which we obtained contrast thresholds at just two signal and two noise frequencies. We examine the increase in threshold produced by noise at either the same frequency as the signal, or a different frequency. We do this in both humans and praying mantises (Sphodromantis lineola), enabling us to compare these species directly in the same paradigm. Our results confirm our ea...
Journal of Comparative Neurology
Newcastle University ePrints -eprint.ncl.ac.uk Rosner R, von Hadeln J, Salden T, Homberg U. Anato... more Newcastle University ePrints -eprint.ncl.ac.uk Rosner R, von Hadeln J, Salden T, Homberg U. Anatomy of the lobula complex in the brain of the praying mantis compared to the lobula complexes of the locust and cockroach.
The motion energy model is the standard account of motion detection in animals from beetles to hu... more The motion energy model is the standard account of motion detection in animals from beetles to humans. Despite this common basis, we show here that a difference in the early stages of visual processing between mammals and insects leads this model to make radically different behavioural predictions. In insects, early filtering is spatially lowpass, which makes the surprising prediction that motion detection can be impaired by “invisible” noise, i.e. noise at a spatial frequency that elicits no response when presented on its own as a signal. We confirm this prediction using the optomotor response of praying mantis Sphodromantis lineola. This does not occur in mammals, where spatially bandpass early filtering means that linear systems techniques, such as deriving channel sensitivity from masking functions, remain approximately valid. Counter-intuitive effects such as masking by invisible noise may occur in neural circuits wherever a nonlinearity is followed by a difference operation.
Biochemical substances are sensitively recognized and processed by living cells, either to provid... more Biochemical substances are sensitively recognized and processed by living cells, either to provide life-energy or to trigger an adequate cell-type specific response. For on-line monitoring of cellular reactions we develop(ed) different Cell Monitoring Systems (CMS ® ). In the last years we ...
Scientific Reports, 2016
Stereopsis -3D vision -has become widely used as a model of perception. However, all our knowledg... more Stereopsis -3D vision -has become widely used as a model of perception. However, all our knowledge of possible underlying mechanisms comes almost exclusively from vertebrates. While stereopsis has been demonstrated for one invertebrate, the praying mantis, a lack of techniques to probe invertebrate stereopsis has prevented any further progress for three decades. We therefore developed a stereoscopic display system for insects, using miniature 3D glasses to present separate images to each eye, and tested our ability to deliver stereoscopic illusions to praying mantises. We find that while filtering by circular polarization failed due to excessive crosstalk, "anaglyph" filtering by spectral content clearly succeeded in giving the mantis the illusion of 3D depth. We thus definitively demonstrate stereopsis in mantises and also demonstrate that the anaglyph technique can be effectively used to deliver virtual 3D stimuli to insects. This method opens up broad avenues of research into the parallel evolution of stereoscopic computations and possible new algorithms for depth perception.
The Journal of neuroscience : the official journal of the Society for Neuroscience, Jan 8, 2013
In many situations animals are confronted with approaching objects. Depending on whether the appr... more In many situations animals are confronted with approaching objects. Depending on whether the approach represents a potential threat or is intended during a goal-oriented approach, the adequate behavioral strategies differ. In all of these cases the visual system experiences an expanding or looming shape. The neuronal machinery mediating looming elicited behavioral responses has been studied most comprehensively in insects but is still far from being fully understood. It is particularly unknown how insects adjust their behavior to objects approaching from different directions. A brain structure that is thought to play an important role in spatial orientation in insects is the central complex (CC). We investigated whether CC neurons process information about approaching objects on a collision course. We recorded intracellularly from CC neurons in the locust Schistocerca gregaria during visual stimulation via lateral LCD screens. Many neurons in the locust CC, including columnar and ta...
Genetic manipulations of neuronal activity are a corner stone of studies aimed to 78 identify the... more Genetic manipulations of neuronal activity are a corner stone of studies aimed to 78 identify the functional impact of defined neurons for animal behavior. With its small 79 nervous system, rapid life cycle and genetic amenability, the fruit fly Drosophila 80 melanogaster provides an attractive model system to study neuronal circuit function. 81
Journal of Experimental Biology, 2010
The strength of stimulus-induced responses at the neuronal and the behavioural level often depend... more The strength of stimulus-induced responses at the neuronal and the behavioural level often depends on the internal state of an animal. Within pathways processing sensory information and eventually controlling behavioural responses, such gain changes can originate at several sites. Using motion-sensitive lobula plate tangential cells (LPTCs) of blowflies, we address whether and in which way information processing changes for two different states of motor activity. We distinguish between the two states on the basis of haltere movements. Halteres are the evolutionarily transformed hindwings of flies. They oscillate when the animals walk or fly. LPTCs mediate, amongst other behaviours, head optomotor responses. These are either of large or small amplitude depending on the state of motor activity. Here we find that LPTC responses also depend on the motor activity of flies. In particular, LPTC responses are enhanced when halteres oscillate. Nevertheless, the response changes of LPTCs do not account for the corresponding large gain changes of head movements. Moreover, haltere activity itself does not change the activity of LPTCs. Instead, we propose that a central signal associated with motor activity changes the gain of head optomotor responses and the response properties of LPTCs.
Journal of Experimental Biology, 2009
Behavioural responses of an animal are variable even when the animal experiences the same sensory... more Behavioural responses of an animal are variable even when the animal experiences the same sensory input several times. This variability can arise from stochastic processes inherent to the nervous system. Also, the internal state of an animal may influence a particular behavioural response. In the present study, we analyse the variability of visually induced head pitch responses of tethered blowflies by high-speed cinematography. We found these optomotor responses to be highly variable in amplitude. Most of the variability can be attributed to two different internal states of the flies with high and low optomotor gain, respectively. Even within a given activity state, there is some variability of head optomotor responses. The amount of this variability differs for the two optomotor gain states. Moreover, these two activity states can be distinguished on a fine timescale and without visual stimulation, on the basis of the occurrence of peculiar head jitter movements. Head jitter goes along with high gain optomotor responses and haltere oscillations. Halteres are evolutionary transformed hindwings that oscillate when blowflies walk or fly. Their main function is to serve as equilibrium organs by detecting Coriolis forces and to mediate gaze stabilisation. However, their basic oscillating activity was also suggested to provide a gain-modulating signal. Our experiments demonstrate that halteres are not necessary for high gain head pitch to occur. Nevertheless, we find the halteres to be responsible for one component of head jitter movements. This component may be the inevitable consequence of their function as equilibrium and gaze-stabilising organs.
PLoS ONE, 2011
Behavioral responses of an animal vary even when they are elicited by the same stimulus. This var... more Behavioral responses of an animal vary even when they are elicited by the same stimulus. This variability is due to stochastic processes within the nervous system and to the changing internal states of the animal. To what extent does the variability of neuronal responses account for the overall variability at the behavioral level? To address this question we evaluate the neuronal variability at the output stage of the blowfly's (Calliphora vicina) visual system by recording from motion-sensitive interneurons mediating head optomotor responses. By means of a simple modelling approach representing the sensorymotor transformation, we predict head movements on the basis of the recorded responses of motion-sensitive neurons and compare the variability of the predicted head movements with that of the observed ones. Large gain changes of optomotor head movements have previously been shown to go along with changes in the animals' activity state. Our modelling approach substantiates that these gain changes are imposed downstream of the motion-sensitive neurons of the visual system. Moreover, since predicted head movements are clearly more reliable than those actually observed, we conclude that substantial variability is introduced downstream of the visual system.