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1 The Center for Advanced Studies in the Space Life Sciences, Marine Biological Laboratory, Woods Hole, Massachusetts
2 Boston University Marine Program, Marine Biological Laboratory, Woods Hole, Massachusetts 02453
This workshop—entitled "Invertebrate Sensory Information Processing: Implications for Biologically Inspired Autonomous Systems"—was sponsored by the Center for Advanced Studies in the Space Life Sciences at the Marine Biological Laboratory. At this meeting, scientific leaders in the fields of invertebrate sensory biology and sensory-guided behavior were brought together with biologists and engineers who develop robotic systems that are based on biologically inspired algorithms and architectures. The participants discussed how moderately complex metazoan organisms (e.g., insects, crustaceans, and cephalopods) process the sensory information that is required to perform natural tasks in a changeable, dynamic environment. They also critiqued the extant, man-made autonomous systems that were built to emulate various invertebrate abilities (e.g., fly in-flight control of air-speed for landing or maintaining course; crustacean ability to track a turbulent odor plume to its source; sensory compensation for lost appendages in walking insects; cricket and parasitic fly recognition; and tracking of a specific acoustic signature in a noisy background). The participants considered the gaps in our knowledge about biological sensory information processing and the limitations in our present technology, both of which limit the transfer of biological competence to man-made autonomous systems. They also identified and debated established and speculative biological concepts and technologies that will facilitate the development of autonomous systems with invertebrate levels of capabilities.
The proceedings of this workshop comprise a substantial subset of the presentations delivered at the meeting, and thus reflect the major themes that emerged during those discussions. These themes are highlighted in the following summary of the papers making up the proceedings.
The variety of modalities of information processing that are used by invertebrates are well represented in the proceedings. In many cases, these modalities may be useful in the exploration of novel environments. For example, invertebrates use polarization and multi-spectral imaging (Cronin and Marshall, 2001). Invertebrate chemoreception includes examples of the identification and classification of complex odors via a range of bimodal sensors (Derby and Steullet, 2001). Tunable sensors are used in acoustic processing to expand the available range, while filtering out background noise and locking onto important or new signals (Mountain and Hubbard, 2001; Robert, 2001; Webb, 2001). Understanding these forms of information processing and their roles in certain environmental niches can illuminate our knowledge of sensory biology and expand our options for sensory processing in autonomous systems.
Many invertebrate systems are robust across a wide range of conditions and make efficient use of limited material and energy. This robustness results, in part, from close coupling between sensory and motor systems: vision (Srinivasan et al., 2001; Barlow et al., 2001); olfaction (Derby and Steullet, 2001; Grasso, 2001); audition (Mountain and Hubbard, 2001; Robert, 2001); vestibular senses (Fraser, 2001); rheo-sense (Breithaupt, 2001). Natural organisms seem not to calculate exact solutions to equations; rather they perform tasks only approximately—just exactly enough to survive—as stick insects do when they target the posterior leg onto the position of the anterior leg during walking (Schmitz et al., 2001). Elegant studies of visual guidance for fly landing provide a powerful example of this coupling (Srinivasan et al., 2001): simple mechanisms suffice because the motor systems provide a predictable sampling context. Examples like this clearly show that, as the functional origins of robust invertebrate behavior in dynamic environments are better understood, valuable insights about the engineering of autonomous systems that can explore unfamiliar or variable environments will be provided.
Invertebrate sensory systems are flexible, and dynamism is built into every processing stage. Contrary to traditional neurobiological dogma, we find plasticity present in abundance in invertebrate systems. Sensory receptors are plastic and show adaptation (Barlow et al., 2001; Fraser, 2001; Mountain and Hubbard, 2001; Robert, 2001); central processes, including learning and memory, augment sensory processing, and the animals themselves show behavioral plasticity (Macmillan and Patullo, 2001; Breithaupt, 2001). Changes in sensory networks have been interpreted as instances of a system adapting to ("discovering") causal relationships in the environment (Birmingham, 2001; Schmitz et al., 2001). Sensory systems can adapt to the statistics of natural scenes, as noted by Breithaupt in crayfish. Indeed, the ability to express these levels of dynamic processing means that an animal is capable of engineering new circuits "on the fly."
Redundancy is a feature of biological sensory systems that assures the attainability of a particular goal. During olfactory learning in spiny lobsters, for example, discrimination, local searching, and distance orientation are carried out by two separate pathways, as described by Derby and Steullet (2001). But apparent redundancy can, in fact, disguise an organization that produces deeper computational and energetic savings (Higgins, 2001).
In general, invertebrates make greater use than vertebrates of multi-modal, multifunctional sensor arrays. Thus, statocysts are used for angular and linear acceleration, vibration, and hydrostatic pressure sensing (Fraser, 2001). Birmingham described the stretch receptor in the crustacean foregut that functions at different times, either as a strain gauge or a volume sensor. Crustacean antennules combine information from flow and chemical sensors located on the same anatomical structure, and can therefore make spatial and temporal correlations across these two modalities (Breithaupt, 2001; Grasso, 2001; Derby and Steullet, 2001). This ability to multitask sensory inputs has implications for the design and implementation of light, efficient systems.
Our understanding of sensory systems and our development of useful autonomous systems depend upon having the best information possible about the to-be-explored environment, as well as stimulus dynamics in those environments. Understanding the stimulus environment speaks to the "design" of sensory receptors and processors and clarifies the evolutionary pressures that shape both the sensory biology and the behavioral choices of an organism. Several investigators, particularly those examining chemosensory behaviors (e.g., Breithaupt, 2001; Grasso, 2001; and Ishida et al., 2001), described their work in stimulus dynamics (e.g., the odor plume as viewed through a single stationary or moving sensor shows complex time series). Obviously, an unexplored environment is one for which limited information is available, but systems deployed in unfamiliar environments must be able to survive and function through interpretation of the sense data that are available to them.
Two strategies for robot building emerged at this workshop. First, ideas borrowed from biology can be used in the design and construction of robots that are meant to accomplish a particular task. Examples of this approach include the robots designed by Ishida et al. (2001). In the second strategy, followed for example by Grasso (2001) and Webb (2001), biomimetic robots were used as platforms for hypothesis testing. Both approaches involve common ground upon which biologists and engineers can collaborate and progress effectively.
Robert Barlow, in his presentation (Barlow et al., 2001), noted that the field of invertebrate sensory biology began in 1926 at Woods Hole with the investigations of Haldan Keffer Hartline (co-recipient of the Nobel Prize in Medicine, 1967). It is thus appropriate that more than 70 years later, scientists and engineers gathered at Woods Hole to assess our present understanding of invertebrate information processing. From the theoretical and empirical insights of neuroscientists and neuroethologists like H. K. Hartline, we look toward a deeper, future understanding that will use physical models to implement theories of biological information processing in natural physical environments. These are the most rigorous and realistic of testing conditions for theories. They are also our best models for the complex historic environments that shaped the evolution of the invertebrate body, brain, and behavior.
The Center for Advanced Studies in the Space Life Sciences (CASSLS) was established in 1999 through a cooperative agreement between the Marine Biological Laboratory and the Life Sciences Division of the National Aeronautics and Space Administration. The Center acts as an interface between NASA and the basic science community, promoting interactions and discussion in areas of basic biology that are of mutual interest. This workshop is an example of the many ways in which the Center achieves these goals.
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  L. M. Koch, B. W. Patullo, and D. L. Macmillan Exploring with damaged antennae: do crayfish compensate for injuries? J. Exp. Biol., August 15, 2006; 209(16): 3226 - 3233. [Abstract] [Full Text] [PDF]
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