The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions

Cockroaches ( Periplaneta americana) orient their antennae toward moving objects based on visual cues. Presumably, this allows exploration of novel objects by the antennal flagellum. We used videographic and electrophysiological methods to determine if receptors on the flagellum are essential for triggering escape, or if they enable cockroaches to discriminate threatening from non-threatening objects that are encountered. When a flagellum was removed, and replaced with a plastic fiber, deflection of a "prosthetic flagellum" still activated the descending mechanosensory interneurons associated with escape and produced typical escape responses. However, escape was essentially eliminated by constraining the movement of the scape and pedicel at the antennal base. When cockroaches approached and briefly explored the surface of a spider or another cockroach with the flagellum, they produced escape significantly more often in response to subsequent controlled contact from a spider than from a cockroach. This discrimination did not depend on visual or wind-sensory input, but required flagellar palpation of the surface. The crucial sensory cues appear to involve texture rather than surface chemicals. These results indicate that cockroaches acquire basic information on stimulus identity during exploration of surfaces with flagellar receptors, but that basal receptors are triggers for escape behavior.     

Active touch in orthopteroid insects: behaviours, multisensory substrates and evolution

Orthopteroid insects (cockroaches, crickets, locusts and related species) allow examination of active sensory processing in a comparative framework. Some orthopteroids possess long, mobile antennae endowed with many chemo- and mechanoreceptors. When the antennae are touched, an animal's response depends upon the identity of the stimulus. For example, contact with a predator may lead to escape, but contact with a conspecific may usually not. Active touch of an approaching object influences the likelihood that a discrimination of identity will be made. Using cockroaches, we have identified specific descending mechanosensory interneurons that trigger antennal-mediated escape. Crucial sensory input to these cells comes from chordotonal organs within the antennal base. However, information from other receptors on the base or the long antennal flagellum allows active touch to modulate escape probability based on stimulus identity. This is conveyed, at least to some extent, by textural information. Guidance of the antennae in active exploration depends on visual information. Some of the visual interneurons and the motor neurons necessary for visuomotor control have been identified. Comparisons across Orthoptera suggest an evolutionary model where subtle changes in the architecture of interneurons, and of sensorimotor control loops, may explain differing levels of vision-touch interaction in the active guidance of behaviour.     

Noninformative vision improves the spatial resolution of touch in humans

Research on sensory perception now often considers more than one sense at a time. This approach reflects real-world situations, such as when a visible object touches us. Indeed, vision and touch show great interdependence: the sight of a body part can reduce tactile target detection times [1], visual and tactile attentional systems are spatially linked [2], and the texture of surfaces that are actively touched with the fingertips is perceived using both vision and touch [3]. However, these previous findings might be mediated by spatial attention [1, 2] or by improved guidance of movement [3] via visually enhanced body position sense [4--6]. Here, we investigate the direct effects of viewing the body on passive touch. We measured tactile two-point discrimination thresholds [7] on the forearm while manipulating the visibility of the arm but holding gaze direction constant. The spatial resolution of touch was better when the arm was visible than when it was not. Tactile performance was further improved when the view of the arm was magnified. In contrast, performance was not improved by viewing a neutral object at the arm's location, ruling out improved spatial orienting as a possible account. Controls confirmed that no information about the tactile stimulation was provided by visibility of the arm. This visual enhancement of touch may point to online reorganization of tactile receptive fields.     

Early vision impairs tactile perception in the blind

Researchers have known for more than a century that crossing the hands can impair both tactile perception and the execution of appropriate finger movements. Sighted people find it more difficult to judge the temporal order when two tactile stimuli, one applied to either hand, are presented and their hands are crossed over the midline as compared to when they adopt a more typical uncrossed-hands posture. It has been argued that because of the dominant role of vision in motor planning and execution, tactile stimuli are remapped into externally defined coordinates (predominantly determined by visual inputs) that takes longer to achieve when external and body-centered codes (determined primarily by somatosensory/proprioceptive inputs) are in conflict and that involves both multisensory parietal and visual cortex. Here, we show that the performance of late, but not of congenitally, blind people was impaired by crossing the hands. Moreover, we provide the first empirical evidence for superior temporal order judgments (TOJs) for tactile stimuli in the congenitally blind. These findings suggest a critical role of childhood vision in modulating the perception of touch that may arise from the emergence of specific crossmodal links during development.     

Visually elicited turning behavior in Rana pipiens: comparative organization and neural control of escape and prey capture

High-speed videography was used to describe the initial turning movement of visually triggered escape in frogs and to compare it with the initial turn of frog prey capture behavior. These two types of turning had some general similarities, e.g. turn duration and peak velocity were positively correlated with turn angle. However, there were kinematic differences: for turns of a given angular amplitude, escape turns consistently demonstrated shorter duration and higher peak velocity than prey capture turns. There also were differences predictably matched to stimulus angles; escape turn angles were more variably related to stimulus angles. Both turning movements are believed to depend upon the optic tectum. However, given the observed differences in kinematics and spatial organization, we used lesion experiments to determine if distinct tectal efferent pathways subserve turning under each circumstance. Large unilateral lesions of the brainstem simultaneously disrupted both types of turning. However, smaller laterally placed lesions disrupted escape turning without disrupting prey capture turns. The kinematic differences in combination with the lesion results support the idea that the post-tectal circuitry for visually elicited turning movements is based upon separate descending pathways that control turning toward prey and turning away from threat.Abbreviations CG central gray - OT optic tectum - SEM standard error of the mean     

Descending influences on escape behavior and motor pattern in the cockroach

The escape behavior of the cockroach is a ballistic behavior with well characterized kinematics. The circuitry known to control the behavior lies in the thoracic ganglia, abdominal ganglia, and abdominal nerve cord. Some evidence suggests inputs may occur from the brain or suboesophageal ganglion. We tested this notion by decapitating cockroaches, removing all descending inputs, and evoking escape responses. The decapitated cockroaches exhibited directionally appropriate escape turns. However, there was a front-to-back gradient of change: the front legs moved little if at all, the middle legs moved in the proper direction but with reduced excursion, and the rear legs moved normally. The same pattern was seen when only inputs from the brain were removed, the suboesophageal ganglion remaining intact and connected to the thoracic ganglia. Electromyogram (EMG) analysis showed that the loss of or reduction in excursion was accompanied by a loss of or reduction in fast motor neuron activity. The loss of fast motor neuron activity was also observed in a reduced preparation in which descending neural signals were reversibly blocked via an isotonic sucrose solution superfusing the neck connectives, indicating that the changes seen were not due to trauma. Our data demonstrate that while the thoracic circuitry is sufficient to produce directional escape, lesion or blockage of the connective affects the excitability of components of the escape circuitry. Because of the rapidity of the escape response, such effects are likely due to the elimination of tonic descending inputs.     

A model of antennal wall-following and escape in the cockroach

Cockroaches exploit tactile cues from their antennae to avoid predators. During escape running the same sensors are used to follow walls. We hypothesise that selection of these mutually exclusive behaviours can be explained without representation of the stimulus or an explicit switching mechanism. A neural model is presented that embodies this hypothesis. The model incorporates behavioural and neurophysiological data and is embedded in a mobile robot in order to test the response to stimuli in the real world. The system is shown to account for data on escape direction and high-speed wall-following in the cockroach, including the counter-intuitive observation that faster running cockroaches maintain a closer distance to the wall. The wall-following behaviour is extended to include discrimination of tactile escape cues according to behavioural context. We conclude by highlighting questions arising from the robot experiments that suggest interesting hypotheses to test in the cockroach.     

Response of thoracic interneurons to tactile stimulation in the cockroach,Periplaneta americana

Receåfindings indicate that cockroaches escape in response to tactile stimulation as well as they do in response to the classic wind puff stimulus. The thoracic interneurons that receive inputs from ventral giant interneurons also respond to tactile stimulation and therefore, represent a potential site of convergence between wind and tactile stimulation as well as other sensory modalities. In this article, we characterize the tactile response of these interneurons, which are referred to as type-A thoracic interneurons (TI_As). In response to tactile stimulation of the body cuticle, TI_As typically respond with a short latency biphasic depolarization which often passes threshold for action potentials. The biphasic response is not typical of responses to wind stimulation nor of tactile stimulation of the antennae. It is also not seen in tactile responses of thoracic interneurons that are not part of the TI_A group. The responses of individual TI_As to stimulation of various body locations were mapped. The left-right directional properties of TI_As are consistent with their responses to wind puffs from various different directions. Cells that respond equally well to wind from the left and right side also respond equally well to tactile stimuli on the left and right side of the animal's body. In contrast, cells that are biased to wind on one side are also biased to tactile stimulation on the same side. In general, tactile responses directed at body cuticle are phasic rather than tonic, occurring both when the tactile stimulator is depressed and released. The response reflects stimulus strength and follows repeated stimulation quite well. However, the first phase of the biphasic response is more robust during high-frequency stimulation than the second phase. TI_As also respond to antennal stimulation. However, here the response characteristics are complicated by the fact that movement of either antenna evokes descending activity in both left and right thoracic connectives. The data suggest that the TI_As make up a multimodal site of sensory convergence that is capable of generating an oriental escape turn in response to any one of several sensory cues. 1994 John Wiley & Sons, Inc.     

Visual control of turning responses to tactile stimuli in the crayfishProcambarus clarkii

Summary Specimens of the crayfishProcambarus clarkii turn to face in the direction of a brief tactile stimulus delivered to a walking leg. The control system that guides this directed behavior was investigated under closed-loop and open-loop conditions. The accuracy of turns exhibited in these experiments was compared to baseline accuracy established by animals restrained from forward and backward walking but allowed to rotate in the yaw plane. Procambarus clarkii individuals deprived of visual feedback tended to undershoot the target angle. Response accuracy increased when a uniform field of stripes moved across the visual field in accordance with the turning movements of the animal. Response accuracy did not match the accuracy observed under baseline conditions, however, unless the responding animal encountered a novel visual image, such as the silhouette of a crayfish, in the moving visual field.Visual feedback thus influences the accuracy of turning in crayfish in two important ways. Movement of stripes across the visual field of a crayfish feeds back positively and promotes rapid turning during the initial phase of a response. This effect obtains regardless of the direction or rate of movement of the stripes in the visual field. The appearance of a novel image in the visual field feeds back negatively to inhibit at least partially further turning. Feedback from the visual system appears to fine tune basic turning movements initiated by a tactile stimulus and crudely directed according to that input. Turning behavior in the crayfish resembles in this respect compensatory eye movements in the lobster and escape responses in a number of arthropods.Neural mechanisms that may explain the experimental results are discussed with particular emphasis on the possibility of interaction between voluntary turning responses and optomotor reactions.     

Touch Influences Visual Perception with a Tight Orientation-Tuning

Stimuli from different sensory modalities are thought to be processed initially in distinct unisensory brain areas prior to convergence in multisensory areas. However, signals in one modality can influence the processing of signals from other modalities and recent studies suggest this cross-modal influence may occur early on, even in ‘unisensory’ areas. Some recent psychophysical studies have shown specific cross-modal effects between touch and vision during binocular rivalry, but these cannot completely rule out a response bias. To test for genuine cross-modal integration of haptic and visual signals, we investigated whether congruent haptic input could influence visual contrast sensitivity compared to incongruent haptic input in three psychophysical experiments using a two-interval, two-alternative forced-choice method to eliminate response bias. The initial experiment demonstrated that contrast thresholds for a visual grating were lower when exploring a haptic grating that shared the same orientation compared to an orthogonal orientation. Two subsequent experiments mapped the orientation and spatial frequency tunings for the congruent haptic facilitation of vision, finding a clear orientation tuning effect but not a spatial frequency tuning. In addition to an increased contrast sensitivity for iso-oriented visual-haptic gratings, we found a significant loss of sensitivity for orthogonally oriented visual-haptic gratings. We conclude that the tactile influence on vision is a result of a tactile input to orientation-tuned visual areas.     

How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization

Diurnal flying animals such as birds depend primarily on vision to coordinate their flight path during goal-directed flight tasks. To extract the spatial structure of the surrounding environment, birds are thought to use retinal image motion (optical flow) that is primarily induced by motion of their head. It is unclear what gaze behaviors birds perform to support visuomotor control during rapid maneuvering flight in which they continuously switch between flight modes. To analyze this, we measured the gaze behavior of rapidly turning lovebirds in a goal-directed task: take-off and fly away from a perch, turn on a dime, and fly back and land on the same perch. High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles. In between saccades, gaze orientation is held constant. By comparing saccade and wingbeat phase, we find that these super-fast saccades are coordinated with the downstroke when the lateral visual field is occluded by the wings. Lovebirds thus maximize visual perception by overlying behaviors that impair vision, which helps coordinate maneuvers. Before the turn, lovebirds keep a high contrast edge in their visual midline. Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline. The perch on which the birds land swings, like a branch in the wind, and we find that retinal size of the perch is the most parsimonious visual cue to initiate landing. Our observations show that rapidly maneuvering birds use precisely timed stereotypic gaze behaviors consisting of rapid head turns and frontal feature stabilization, which facilitates optical flow based flight control. Similar gaze behaviors have been reported for visually navigating humans. This finding can inspire more effective vision-based autopilots for drones.     

Mechanisms for turn alternation in four invertebrate species

Free-choice behavior following one or more forced turns was observed in representatives of four invertebrate classes (earthworms, woodlice, millipedes, earwigs). While all animals alternated, species differences occurred in free turn angle and the effects of varied angle and number of forced turns. Overall, woodlice and millipedes turned at sharper angles and responded more to the forced turn conditions than earthworms and earwigs. From behavior observed following three forced turns in one direction and then one in the opposite, it was concluded that, in earlier experiments, earthworms alternated via tactile cues, woodlice mainly used kinesthetic but could also use tactile cues, millipedes mainly used tactile but could also use kinesthetic cues and earwigs may have relied on kinesthetic cues alone. Since phyletic differences did not seem appropriate, the results were discussed in terms of other characteristics such as body shape and life style.     

Interaction between descending input and thoracic reflexes for joint coordination in cockroach: I. Descending influence on thoracic sensory reflexes

Tethered cockroaches turn from unilateral antennal contact using asymmetrical movements of mesothoracic (T2) legs (Mu and Ritzmann in J Comp Physiol A 191:1037–1054, 2005). During the turn, the leg on the inside of the turn (the inside T2 leg) has distinctly different motor patterns from those in straight walking. One possible neural mechanism for the transformation from walking to inside leg turning could be that the descending commands alter a few critical reflexes that start a cascade of physical changes in leg movement or posture, leading to further alterations. This hypothesis has two implications: first, the descending activities must be able to influence thoracic reflexes. Second, one should be able to initiate the turning motor pattern without descending signals by mimicking a point farther down in the reflex cascade. We addressed the first implication in this paper by experiments on chordotonal organ reflexes. The activity of depressor muscle (Ds) and slow extensor tibia muscle (SETi) was excited and inhibited by stretching and relaxing the femoral chordotonal organ. However, the Ds responses were altered after eliminating the descending activity, while the SETi responses remain similar. The inhibition to Ds activity by stretching the coxal chordotonal organ was also altered after eliminating the descending activity.     

Interaction between descending input and thoracic reflexes for joint coordination in cockroach. II Comparative studies on tethered turning and searching

Tethered cockroaches turn from unilateral antennal contact using asymmetrical movements of mesothoracic (T2) legs (Mu and Ritzmannin J Comp Physiol A 191:1037–1054, 2005). During the turn, the leg on the inside of the turn (the inside T2 leg) has distinctly different motor patterns from those in straight walking. The transformation from walking to inside leg turning could be triggered by descending commands that alter a few critical reflexes that start a cascade of physical changes in leg movement or posture, leading to further alterations. This hypothesis has two implications: First, the descending activities must be able to influence thoracic reflexes. Second, one should be able to initiate the turning motor pattern in the absence of descending signals by mimicking a point farther down in the reflex cascade. We addressed the first implication in the companion paper. To examine the second implication, we compared kinematics and motor activities of the T2 leg during searching with that of inside leg turning. The reaching movements made during searching were found to be similar to the movements made by the inside leg during turning. Moreover, even after disconnecting the brain from the thoracic ganglia the reaching movements were similar. This observation is consistent with the second implication from the hypothesis.     

Lateralized visual behavior in bottlenose dolphins (Tursiops truncatus) performing audio-visual tasks: the right visual field advantage

Analyzing cerebral asymmetries in various species helps in understanding brain organization. The left and right sides of the brain (lateralization) are involved in different cognitive and sensory functions. This study focuses on dolphin visual lateralization as expressed by spontaneous eye preference when performing a complex cognitive task; we examine lateralization when processing different visual stimuli displayed on an underwater touch-screen (two-dimensional figures, three-dimensional figures and dolphin/human video sequences). Three female bottlenose dolphins (Tursiops truncatus) were submitted to a 2-, 3- or 4-, choice visual/auditory discrimination problem, without any food reward: the subjects had to correctly match visual and acoustic stimuli together. In order to visualize and to touch the underwater target, the dolphins had to come close to the touch-screen and to position themselves using monocular vision (left or right eye) and/or binocular naso-ventral vision. The results showed an ability to associate simple visual forms and auditory information using an underwater touch-screen. Moreover, the subjects showed a spontaneous tendency to use monocular vision. Contrary to previous findings, our results did not clearly demonstrate right eye preference in spontaneous choice. However, the individuals' scores of correct answers were correlated with right eye vision, demonstrating the advantage of this visual field in visual information processing and suggesting a left hemispheric dominance. We also demonstrated that the nature of the presented visual stimulus does not seem to have any influence on the animals' monocular vision choice.     

Directional cues in tactile stimuli involved in agonistic encounters in cockroaches

ABSTRACT. The ability of male cockroaches, Nauphoeta cinerea and Periplaneta americana , to respond directionally to tactile agonistic acts was tested using stimulation by artificially manipulated appendages. Responses by Nauphoeta included turning towards the stimulus at preferred angles of c. 40°, 90° and 180°, apparently relying on internally-stored directional sensory information. This turning responsiveness depended in part on the social status of the receiving individual, since subordinate individuals often retreated or failed to respond. Periplaneta males reacted to tactile stimuli by quick movements away from the stimulus or by kicking towards it. The leg used in kicking was that nearest to the part of the body which was stimulated.     

Cross-modal interactions between olfaction and touch

We report two experiments designed to investigate the nature of any cross-modal interactions between olfactory and tactile information processing. In Experiment 1, we assessed the influence of olfactory cues on the tactile perception of fabric softness using computer-controlled stimulus presentation. The results showed that participants rated fabric swatches as feeling significantly softer when presented with a lemon odor than when presented with an animal-like odor, demonstrating that olfactory cues can modulate tactile perception. In Experiment 2, we assessed whether this modulatory effect varied as a function of the particular odors being used and/or of the spatial coincidence between the olfactory and tactile stimuli. The results replicated those reported in Experiment 1 thus further supporting the claim that people's rating of tactile stimuli can be modulated by the presence of an odor. Taken together, the results of the two experiments reported here support the existence of a cross-modal interaction between olfaction and touch.     

Active tactile sensing for localization of objects by the cockroach antenna

Antennal movement during tactile orientation behavior was examined three-dimensionally in American cockroaches during tethered walking. When a wooden rod was presented to the tip of one antenna in an upright orientation at one of the three different horizontal positions (30°, 60°, or 90° from the center of the head), the animal touched it repeatedly with the antenna, and tried to approach it (positive thigmotaxis). Positional shifts were also observed for the contralateral unstimulated antenna. The ipsilateral antenna tended to touch the object during inward movement (adduction) at all three test angles. The cumulative turn angle made during a continuous test period of 24 s clearly depended on the object’s position; however, the contact frequencies were almost the same regardless of the position. The relationships between contact frequency and some locomotion parameters were also investigated on a shorter time scale of 3 s. The contact frequency positively correlated with the turn angle, with the accuracy of orientation at all three test angles, and with the translation velocity at test angles of 30° and 60°. It is concluded that the performance during tactile orientation can be represented effectively by the frequency with which the antennae touch the attractive objects.