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Studies of mechanisms of adaptive behavior generally focus on neurons and circuits. But adaptive
behavior also depends on interactions among the nervous system, body and environment: sensory
preprocessing and motor post-processing filter inputs to and outputs from the nervous system;
co-evolution and co-development of nervous system and periphery create matching and
complementarity between them; body structure creates constraints and opportunities for neural
control; and continuous feedback between nervous system, body and environment are essential
for normal behavior. This broader view of adaptive behavior has been a major underpinning of
ecological psychology and has influenced behavior-based robotics. Computational neuroethology,
which jointly models neural control and periphery of animals, is a promising methodology for
understanding adaptive behavior.
Trends Neurosci. (1997) 20, 553–557
Copyright © 1997, Elsevier Science Ltd. All rights reserved. 0166 - 2236/97/$17.00 PII: S0166-2236(97)01149-1 TINS Vol. 20, No. 12, 1997 553
VIEWPOINT H. Chiel and R. Beer – Brain, body and environmental interactions in adaptive behavior
constraints: for example, activation of postural muscles biologically useful patterns of activity39. Recent results
must minimize shear stresses on bone29. Structures from the leech have provided further evidence for the
composed entirely of muscle, such as tentacles, fundamental role of sensory feedback in normal pat-
tongues or trunks (muscular hydrostats) have an tern generation. First, the frequency of firing of swim
extraordinarily large number of degrees of freedom30, interneurons is too low in reduced preparations to
but changes in the mechanical advantage of their con- provide functional outputs, but in the presence of nor-
stituent muscles greatly affect the forces and move- mal sensory feedback, the neurons fire at an effective
ments they can generate31. rate. Second, a realistic model of the leech body does
Properties of the periphery also offer significant not generate effective crawling movements when acti-
simplifications for neural control. For example, when vated with fictive crawling motor patterns observed in
an octopus uses a tentacle to reach for an object, it isolated nervous systems, but does generate effective
generates a propagating bend that moves within a movements when activated by crawling motor pat-
single plane and has a tangential velocity (a velocity terns observed in intact leeches, which only occur
in the direction of movement) that is stereotyped. when sensory feedback is present40. In the absence of
Controlling this bend may simplify the control prob- feedback from an animal’s own movements, the ner-
lem of moving a muscular hydrostatic structure with vous system may not generate meaningful activity
many degrees of freedom32. The musculoskeletal prop- patterns for behavior.
erties of the human body restrict the feasible acceler- Feedback from the environment, and the dynamical
ations that can restore posture in response to a pertur- properties of the environment itself, also play a vital
bation that causes the body to sway. These restrictions role in the generation of adaptive behavior. A detailed
provide a rationale for understanding the rotations biomechanical model of the lamprey indicated that
around the ankle or hip that are experimentally the hydrodynamics of water was essential for generat-
observed33. Using a mass–spring model to represent ing normal traveling waves of contraction along the
running animals clarifies the absorption and release body of the animal. If this hydrodynamics was not
of energy by the musculoskeletal system, and pro- present, the model generated inappropriate whole
vides a unified perspective for understanding animals body contractions. Removing a lamprey from water
with different numbers of legs and different body and inducing it to swim generated the same inappro-
masses, locomoting at different speeds and over ter- priate movements predicted by the model41. Thus, the
rains of different stiffnesses34. The relative stiffness of embedding of an animal’s body in an environment is
muscles around a joint create an equilibrium point to crucial for the behavior that it generates.
which a limb will return after perturbation, and this
A broader viewpoint and its implications
may be exploited by spinal cord networks to simplify
control35. These observations can be summarized using two
contrasting musical metaphors. The nervous system is
Continuous feedback from the body and the
often seen as the conductor of the body, choosing the
environment
program for the players and directing exactly how
The most important evidence suggesting that the they play. The results reviewed above suggest a differ-
nervous system cannot be the exclusive focus for ent metaphor: the nervous system is one of a group of
understanding adaptive behavior is that it continu- players engaged in jazz improvization, and the final
ously receives and responds to feedback both from the result emerges from the continued give and take
movements that it induces in its own periphery and between them. In other words, adaptive behavior is
from the surrounding environment (Fig. 1D). the result of the continuous interaction between the
Feedback plays vital roles in normal developmental nervous system, the body and the environment, each
processes. In rats, locomotion takes on its adult form of which have rich, complicated, highly structured
after postnatal day 15 (P15). Immobilizing one leg dynamics. The role of the nervous system is not so
from P1 to P13 does not prevent the development of much to direct or to program behavior as to shape it
a normal locomotor pattern 1–2 weeks after the leg is and evoke the appropriate patterns of dynamics from
freed from restriction; but it does cause a persistent the entire coupled system (see Fig. 1E; Ref. 42). As a
deficit in the duration and timing of electromyogram consequence, one cannot assign credit for adaptive
(EMG) to leg muscles of the restricted side, suggesting behavior to any one piece of this coupled system.
that feedback from movement contributes to normal There are several important implications of this
neural development36. Thelen and associates have broader viewpoint. New behaviors might emerge that
obtained data suggesting that the development of are properties only of the coupled system. For exam-
reaching movements in infants is related to the ability ple, as a predator and prey interact, their unfolding
of the infants to adjust for the dynamics of the reach- behavior depends both on their own actions and the
ing movements that they spontaneously generate changing behavior of the other animal. Furthermore,
(that is, fast or slow, weak or strong movements) by each system cannot control all aspects of the behavior
feedback from their success in reaching their goals37. of the system to which it is coupled. Rather, each
In adult animals, proprioceptive feedback plays a system’s response depends on its own internal state
fundamental role in the generation of normal patterns as well as the perturbations it receives from the other
of motor activity. Pearson and his colleagues demon- system. Instead of asking ‘What is the neural basis of
strated that phasic feedback from stretch receptors was adaptive behavior?’, one should ask ‘What are the
essential for maintaining the frequency and duration contributions of all components of the coupled
of normal flying movements in the locust38. These system and their interactions to adaptive behavior?’
results led Pearson to suggest that there was no such Versions of this viewpoint have been previously
thing as a pure central pattern generator, since all articulated by others. The view of behavior espoused by
pattern generators need sensory feedback to generate cybernetics, the theoretical study of control in animals
and machines43, and, in particular, Ashby’s view of with neural activity, and the primary focus is relating
the brain as a dynamical system that generates appro- neural activity to behavior.
priate behavior44, is consonant with this viewpoint. Three broad approaches can be distinguished
Maturana and Varela’s views on the nature of bio- within computational neuroethology, each of which
logical organization and its consequences for adaptive has benefits and drawbacks. First, one can construct
behavior also emphasize the ongoing interactions biologically realistic models motivated by experi-
between the organism and the environment as essen- mental questions. Drawbacks of these models are the
tial for maintaining the self-organizing integrity of the extensive experimental work required to set the model
organism45,46. Ecological psychology has long empha- parameters, and the complexity of the models, which
sized such a dynamical perspective on perception and are difficult to analyze theoretically. The advantage
action, and the importance of organism/environment is that one can make quantitative, experimentally
mutuality47–50. Altman and Kien have emphasized testable predictions. Examples of this approach are
that the sensory and biomechanical contexts in which realistic models of neural control and biomechanics
neural activity occurs, as well as the contexts created of reptilian tongue-lapping31, leech crawling61 and
by the activity within and between different neural lamprey swimming41,62.
networks, are crucial for the flexibility and richness Second, one can construct more abstract models
of behavior51,52. Within cognitive science, there is a motivated by theoretical questions. Drawbacks of
growing awareness that one must take into account these models are that they may not make quantitative,
the embeddedness of the brain in the body and world experimentally testable predictions. The advantages
to understand aspects of cognition53. are that they highlight key features of a problem, can
Recent work in the field of autonomous robotics has determine what is or is not essential, have few param-
emphasized that intelligent behavior is an emergent eters to set and are tractable to theoretical analysis.
property of an agent embedded in an environment Examples of this approach are the creation of simpli-
with which it must continuously interact54. Raibert fied models of insects58,63, nematode worms64, hover-
and Hodgins, who have built robots that hop, run, flies65, frogs66, and more abstract ‘agents’ capable of
and jump, have made this argument: ‘Many re- locomotion, chemotaxis, learning and visually guided
searchers in neural motor control think of the nerv- behaviors67–69. A coupled model of an oscillator and
ous system as a source of commands that are issued to a pendular limb demonstrated that motor behavior
the body as “direct orders”. We believe that the emerges from interactions between neural and physi-
mechanical system has a mind of its own, governed by cal dynamics70. Mathematical tools of dynamic sys-
the physical structure and the laws of physics. Rather tems analysis have been applied to understanding
than issuing commands, the nervous system can only some of these simpler models42.
make “suggestions” which are reconciled with the Third, one can create physical models by building
physics of the system and the task’55. In our own work devices that exhibit properties of the system under
on biologically-inspired robotics, done in collabor- study. Drawbacks of this approach are that building
ation with Roger Quinn and Roy Ritzmann, we have an actual device can be difficult, slow, and expensive,
demonstrated that incorporating biomechanical prop- and it may fail to work for reasons that have nothing
erties similar to those of insects into hexapod robots to do with one’s understanding of the biological sys-
can simplify their control, allowing them to traverse tem. There are great advantages for engineering, since
irregular terrain and making them robust to it would be a major advance to create robots with the
lesions56,57. flexibility and adaptiveness of animals. There are also
Adopting this broader viewpoint poses difficulties scientific advantages. Building an ‘animal’ provides a
for an experimentalist: it is already a daunting task to unique perspective on how it works. What aspects of
understand the neurons and neural circuits in iso- biomechanics, neural control, or environment are
lation; taking into account the periphery and the en- important for a behavior, and which can be safely
vironment only makes a hard problem even harder. ignored? What are possible solutions that generate
To cope with the challenges of this broader viewpoint, equivalent results? Will one’s ideas about how a sys-
we and others have begun to utilize a promising tem works actually succeed in interaction with the real
methodology termed computational neuroethology58,59. world? Examples of this approach are insect-like hexa-
Computational neuroethology involves creating pod robots57,71–73, robot crickets that can respond to
joint models of the relevant parts of an animal’s mating calls74, and robots guided by insect-like com-
nervous system, body and environment. This requires pound eyes75.
experimental investigation not only of neural cir- In summary, several lines of converging experimen-
cuitry, but also of the relevant aspects of an animal’s tal evidence suggest a broader viewpoint in which the
biomechanics and ecological niche, and then con- roles of the brain, body and environment are fully
struction of models that incorporate these compo- appreciated. The emerging methodology of compu-
nents. Using these models, one can study the contri- tational neuroethology, in which joint models of
butions of the components to adaptive behavior, and neural circuitry, biomechanics and environment can
the new phenomena that may emerge from their be studied, provides an effective means to progress.
interactions. Adopting this methodology has conse-
quences for experimental neuroscience. For example, Selected references
1 Selverston, A.I. (1985) Model Neural Networks and Behavior,
assessing the importance of changes in a motor pro- Plenum Press
gram can only be done by ‘playing it’ through the 2 Harris-Warrick, R.M. et al. (1992) Dynamic Biological Networks:
body, or a model of the body, and observing the The Stomatogastric Nervous System, MIT Press
3 Morton, D.W. and Chiel, H.J. (1994) Trends Neurosci. 17,
behavioral consequences. This approach is distinctive
413–420
from that of computational neuroscience60, in that 4 Michelsen, A., Popov, A.V. and Lewis, B. (1994) J. Comp.
biomechanics and ecology are on an equal footing Physiol. A 175, 153–164