Cynthia M. Harley

Characterization of obstacle negotiation behaviors in the cockroach,Blaberus discoidalis

SUMMARY Within natural environments, animals must be able to respond to a wide range of obstacles in their path. Such responses require sensory information to facilitate appropriate and effective motor behaviors. The objective of this study was to characterize sensors involved in the complex control of obstacle negotiation behaviors in the cockroach Blaberus discoidalis. Previous studies suggest that antennae are involved in obstacle detection and negotiation behaviors. During climbing attempts, cockroaches swing their front leg that then either successfully reaches the top of the block or misses. The success of these climbing attempts was dependent on their distance from the obstacle. Cockroaches with shortened antennae were closer to the obstacle prior to climbing than controls, suggesting that distance was related to antennal length. Removing the antennal flagellum resulted in delays in obstacle detection and changes in climbing strategy from targeted limb movements to less directed attempts. A more complex scenario – a shelf that the cockroach could either climb over or tunnel under – allowed us to further examine the role of sensory involvement in path selection. Ultimately, antennae contacting the top of the shelf led to climbing whereas contact on the underside led to tunneling However, in the light, cockroaches were biased toward tunnelling; a bias which was absent in the dark. Selective covering of visual structures suggested that this context was determined by the ocelli.

Central-Complex Control of Movement in the Freely Walking Cockroach

To navigate in the world, an animals brain must produce commands to move, change direction, and negotiate obstacles. In the insect brain, the central complex integrates multiple forms of sensory information and guides locomotion during behaviors such as foraging, climbing over barriers, and navigating to memorized locations. These roles suggest that the central complex influences motor commands, directing the appropriate movement within the current context. Such commands are ultimately carried out by the limbs and must therefore interact with pattern generators and reflex circuits that coordinate them. Recent studies have described how neurons of the central complex encode sensory information: neurons subdivide the space around the animal, encoding the direction or orientation of stimuli used in navigation. Does a similar central-complex code directing movement exist, and if so, how does it effect changes in the control of limbs? Recording from central-complex neurons in freely walking cockroaches (Blaberus discoidalis), we identified classes of movement-predictive cells selective for slow or fast forward walking, left or right turns, or combinations of forward and turning speeds. Stimulation through recording wires produced consistent trajectories of forward walking or turning in these animals, and those that elicited turns also altered an inter-joint reflex to a pattern resembling spontaneous turning. When an animal transitioned to climbing over an obstacle, the encoding of movement in this new context changed for a subset of cells. These results indicate that encoding of movement in the central complex participates in motor control by a distributed, flexible code targeting limb reflex circuits.

Insect-like Antennal Sensing for Climbing and Tunneling Behavior in a Biologically-inspired Mobile Robot

Through the use of mechanical, actuated antennae a biologically-inspired robot is capable of autonomous decision-making and navigation when faced with an obstacle that can be climbed over or tunneled under. Vertically-sweeping mechanical antennae and interface microcontrollers have been added to the Whegs ™ II [1] sensor platform that allow it to autonomously sense the presence of, and successfully navigate a horizontal shelf placed in its path. The obstacle is sensed when the antennae make contact with it, and navigation is made possible through articulation of the Whegs ™ II body flexion joint.

Deciding Which Way to Go: How Do Insects Alter Movements to Negotiate Barriers?

Animals must routinely deal with barriers as they move through their natural environment. These challenges require directed changes in leg movements and posture performed in the context of ever changing internal and external conditions. In particular, cockroaches use a combination of tactile and visual information to evaluate objects in their path in order to effectively guide their movements in complex terrain. When encountering a large block, the insect uses its antennae to evaluate the object’s height then rears upward accordingly before climbing. A shelf presents a choice between climbing and tunneling that depends on how the antennae strike the shelf; tapping from above yields climbing, while tapping from below causes tunneling. However, ambient light conditions detected by the ocelli can bias that decision. Similarly, in a T-maze turning is determined by antennal contact but influenced by visual cues. These multi-sensory behaviors led us to look at the central complex as a center for sensori-motor integration within the insect brain. Visual and antennal tactile cues are processed within the central complex and, in tethered preparations, several central complex units changed firing rates in tandem with or prior to altered step frequency or turning, while stimulation through the implanted electrodes evoked these same behavioral changes. To further test for a central complex role in these decisions, we examined behavioral effects of brain lesions. Electrolytic lesions in restricted regions of the central complex generated site specific behavioral deficits. Similar changes were also found in reversible effects of procaine injections in the brain. Finally, we are examining these kinds of decisions made in a large arena that more closely matches the conditions under which cockroaches forage. Overall, our studies suggest that CC circuits may indeed influence the descending commands associated with navigational decisions, thereby making them more context dependent.

Electrolytic lesions within central complex neuropils of the cockroach brain affect negotiation of barriers

SUMMARY Animals must negotiate obstacles in their path in order to successfully function within natural environments. These actions require transitions from walking to other behaviors, many of which are more involved than simple reflexes. For these behaviors to be successful, insects must evaluate objects in their path and then use that information to change posture or re-direct leg movements. Some of this control may occur within a region of the brain known as the central complex (CC). We used discrete electrolytic lesions to examine the role of certain sub-regions of the CC in various obstacle negotiation behaviors. We found that cockroaches with lesions to the protocerebral bridge (PB) and ellipsoid body (EB) exhibit abnormalities in turning and dealing with shelf-like objects; whereas, individuals with lesions to the fan-shaped body (FB) and lateral accessory lobe (LAL), exhibit abnormalities of those behaviors as well as climbing over blocks and up walls to a horizontal plane. Abnormalities in block climbing include decreased success rate, changes in climbing strategy, and delayed response to the block. Increases in these abnormal behaviors were significant in individuals with lesions to the FB and LAL. Although turning abnormalities are present in individuals with lesions to the LAL, EB and the lateral region of the FB, there are some differences in how these deficits present. For instance, the turning deficits seen in individuals with lateral FB lesions only occurred when turning in the direction opposite to the side of the brain on which the lesion occurred. By contrast, individuals with lesions to the EB and LAL exhibited turning abnormalities in both directions. Lesions in the medial region of the FB did not result in directional turning deficits, but in abnormalities in block climbing.

Discontinuous locomotion and prey sensing in the leech

SUMMARY The medicinal leech, Hirudo verbana, is an aquatic predator that utilizes water waves to locate its prey. However, to reach their prey, the leeches must move within the same water that they are using to sense prey. This requires that they either move ballistically towards a pre-determined prey location or that they account for their self-movement and continually track prey. We found that leeches do not localize prey ballistically. Instead, they require continual sensory information to track their prey. Indeed, in the event that the prey moves, leeches will approach the preys new location. While leeches need to continually sense water disturbances to update their percept of prey location, their own behavior is discontinuous – approaching prey involves switching between swimming, crawling and non-locomoting. Each of these behaviors may allow for different sensory capabilities and may require different sensory filters. Here, we examined the sensory capabilities of leeches during each of these behaviors. We found that while one could expect the non-locomoting phases to direct subsequent behaviors, crawling phases were more effective than non-locomotor phases for providing direction. During crawling bouts, leeches adjusted their heading so as to become more directed towards the stimulus. This was not observed during swimming. Furthermore, in the presence of prey-like stimuli, leeches crawled more often and for longer periods of time.

Compensatory plasticity restores locomotion after chronic removal of descending projections.

Homeostatic plasticity is an important attribute of neurons and their networks, enabling functional recovery after perturbation. Furthermore, the directed nature of this plasticity may hold a key to the restoration of locomotion after spinal cord injury. Here we studied the recovery of crawling in the leech Hirudo verbana after descending cephalic fibers were surgically separated from crawl central pattern generators shown previously to be regulated by dopamine. We observed that immediately after nerve cord transection leeches were unable to crawl, but remarkably, after a day to weeks, animals began to show elements of crawling and intersegmental coordination. Over a similar time course, excessive swimming due to the loss of descending inhibition returned to control levels. Additionally, removal of the brain did not prevent crawl recovery, indicating that connectivity of severed descending neurons was not essential. After crawl recovery, a subset of animals received a second transection immediately below the anterior-most ganglion remaining. Similar to their initial transection, a loss of crawling with subsequent recovery was observed. These data, in recovered individuals, support the idea that compensatory plasticity directly below the site of injury is essential for the initiation and coordination of crawling. We maintain that the leech provides a valuable model to understand the neural mechanisms underlying locomotor recovery after injury because of its experimental accessibility, segmental organization, and dependence on higher-order control involved in the initiation, modulation, and coordination of locomotor behavior.

Scanning Behavior in the Medicinal Leech Hirudo verbana

While moving through their environment, medicinal leeches stop periodically and wave their head or body back and forth. This activity has been previously described as two separate behaviors: one called ‘head movement’ and another called ‘body waving’. Here, we report that these behaviors exist on a continuum, and provide a detailed description of what we now call ‘scanning’. Scanning-related behavior has been thought to be involved in orientation; its function has never before been assessed. While previous studies suggested an involvement of scanning in social behavior, or sucker placement, our behavioral studies indicate that scanning is involved in orienting the leech towards prey stimuli. When such stimuli are present, scanning behavior is used to re-orient the leech in the direction of a prey-like stimulus. Scanning, however, occurs whether or not prey is present, but in the presence of prey-like stimuli scanning becomes localized to the stimulus origin. Most likely, this behavior helps the leech to gain a more detailed picture of its prey target. The display of scanning, regardless of the presence or absence of prey stimuli, is suggestive of a behavior that is part of an internally driven motor program, which is not released by the presence of sensory stimuli. The data herein include first steps to understanding the neural mechanisms underlying this important behavior.

Plasmon resonance and the imaging of metal-impregnated neurons with the laser scanning confocal microscope

The staining of neurons with silver began in the 1800s, but until now the great resolving power of the laser scanning confocal microscope has not been utilized to capture the in-focus and three-dimensional cytoarchitecture of metal-impregnated cells. Here, we demonstrate how spectral confocal microscopy, typically reserved for fluorescent imaging, can be used to visualize metal-labeled tissues. This imaging does not involve the reflectance of metal particles, but rather the excitation of silver (or gold) nanoparticles and their putative surface plasmon resonance. To induce such resonance, silver or gold particles were excited with visible-wavelength laser lines (561 or 640 nm), and the maximal emission signal was collected at a shorter wavelength (i.e., higher energy state). Because the surface plasmon resonances of noble metal nanoparticles offer a superior optical signal and do not photobleach, our novel protocol holds enormous promise of a rebirth and further development of silver- and gold-based cell labeling protocols. DOI: http://dx.doi.org/10.7554/eLife.09388.001

Animal-inspired sensing for autonomously climbing or avoiding obstacles

The way that natural systems navigate their environments with agility, intelligence and efficiency is an inspiration to engineers. Biological attributes such as modes of locomotion, sensory modalities, behaviours and physical appearance have been used as design goals. While methods of locomotion allow robots to move through their environment, the addition of sensing, perception and decision making are necessary to perform this task with autonomy. This paper contrasts how the addition of two separate sensing modalities --tactile antennae and non-contact sensing --and a low-computation, capable microcontroller allow a biologically abstracted mobile robot to make insect-inspired decisions when encountering a shelflike obstacle, navigating a cluttered environment without collision and seeking vision-based goals while avoiding obstacles.