Predicting Adaptive Behavior in the Environment from Central Nervous System Dynamics

To generate adaptive behavior, the nervous system is coupled to the environment. The coupling constrains the dynamical properties that the nervous system and the environment must have relative to each other if adaptive behavior is to be produced. In previous computational studies, such constraints have been used to evolve controllers or artificial agents to perform a behavioral task in a given environment. Often, however, we already know the controller, the real nervous system, and its dynamics. Here we propose that the constraints can also be used to solve the inverse problem—to predict from the dynamics of the nervous system the environment to which they are adapted, and so reconstruct the production of the adaptive behavior by the entire coupled system. We illustrate how this can be done in the feeding system of the sea slug Aplysia. At the core of this system is a central pattern generator (CPG) that, with dynamics on both fast and slow time scales, integrates incoming sensory stimuli to produce ingestive and egestive motor programs. We run models embodying these CPG dynamics—in effect, autonomous Aplysia agents—in various feeding environments and analyze the performance of the entire system in a realistic feeding task. We find that the dynamics of the system are tuned for optimal performance in a narrow range of environments that correspond well to those that Aplysia encounter in the wild. In these environments, the slow CPG dynamics implement efficient ingestion of edible seaweed strips with minimal sensory information about them. The fast dynamics then implement a switch to a different behavioral mode in which the system ignores the sensory information completely and follows an internal “goal,” emergent from the dynamics, to egest again a strip that proves to be inedible. Key predictions of this reconstruction are confirmed in real feeding animals.

[1]  C. Campbell,et al.  On Being There , 1965 .

[2]  I. Kupfermann Feeding behavior in Aplysia: a simple system for the study of motivation. , 1974, Behavioral biology.

[3]  I Kupfermann,et al.  Behavior patterns of Aplysia californica in its natural environment. , 1974, Behavioral biology.

[4]  E. Kandel Behavioral Biology Of Aplysia , 1979 .

[5]  Cross-modality sensory integration in the control of feeding Aplysia. , 1982, Behavioral and neural biology.

[6]  A. McClellan,et al.  MOVEMENTS AND MOTOR PATTERNS OF THE BUCCAL MASS OF PLEUROBRANCHAEA DURING FEEDING, REGURGITATION AND REJECTION , 1982 .

[7]  H. Chiel,et al.  An identified histaminergic neuron modulates feeding motor circuitry in Aplysia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  H. Chiel,et al.  Activity of an identified histaminergic neuron, and its possible role in arousal of feeding behavior in semi-intact Aplysia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Abraham J Susswein,et al.  Identification of the neural pathway for reinforcement of feeding when Aplysia learn that food is inedible , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  P. Andrews,et al.  The neurophysiology of vomiting. , 1988, Bailliere's clinical gastroenterology.

[11]  P. Andrews,et al.  8 The neurophysiology of vomiting , 1988 .

[12]  I Kupfermann,et al.  The role of a modulatory neuron in feeding and satiation in Aplysia: effects of lesioning of the serotonergic metacerebral cells , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Randall Beer,et al.  Intelligence as Adaptive Behavior , 1990 .

[14]  I Kupfermann,et al.  Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Randall D. Beer,et al.  Evolving Dynamical Neural Networks for Adaptive Behavior , 1992, Adapt. Behav..

[16]  I. Hurwitz,et al.  Adaptation of Feeding Sequences in Aplysia Oculifera to Changes in the Load and Width of Food , 1992 .

[17]  D. Bray Protein molecules as computational elements in living cells , 1995, Nature.

[18]  E. Marder,et al.  Principles of rhythmic motor pattern generation. , 1996, Physiological reviews.

[19]  Mark A. Willis,et al.  Adaptive Control of Odor-Guided Locomotion: Behavioral Flexibility as an Antidote to Environmental Unpredictability1 , 1996, Adapt. Behav..

[20]  Stephen Wolfram,et al.  The Mathematica Book , 1996 .

[21]  H. Chiel,et al.  Activity patterns of the B31/B32 pattern initiators innervating the I2 muscle of the buccal mass during normal feeding movements in Aplysia californica. , 1996, Journal of neurophysiology.

[22]  D. A. Baxter,et al.  Contingent-Dependent Enhancement of Rhythmic Motor Patterns: AnIn Vitro Analog of Operant Conditioning , 1997, The Journal of Neuroscience.

[23]  Randall D. Beer,et al.  The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment , 1997, Trends in Neurosciences.

[24]  Randall D. Beer,et al.  The dynamics of adaptive behavior: A research program , 1997, Robotics Auton. Syst..

[25]  I. V. Orekhova,et al.  Control of time-dependent biological processes by temporally patterned input. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Hooper,et al.  Muscle Response to Changing Neuronal Input in the Lobster (Panulirus interruptus) Stomatogastric System: Spike Number- versus Spike Frequency-Dependent Domains , 1997, The Journal of Neuroscience.

[27]  D. A. Baxter,et al.  Identification and characterization of catecholaminergic neuron B65, which initiates and modifies patterned activity in the buccal ganglia of Aplysia. , 1998, Journal of neurophysiology.

[28]  T. Gelder,et al.  The dynamical hypothesis in cognitive science , 1998, Behavioral and Brain Sciences.

[29]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[30]  Irving Kupfermann,et al.  Studies of Neuromodulation of Oscillatory Systems in Aplysia, by Means of Genetic Algorithms , 2000, Adapt. Behav..

[31]  I. V. Orekhova,et al.  Optimization of rhythmic behaviors by modulation of the neuromuscular transform. , 2000, Journal of neurophysiology.

[32]  I. V. Orekhova,et al.  The neuromuscular transform: the dynamic, nonlinear link between motor neuron firing patterns and muscle contraction in rhythmic behaviors. , 2000, Journal of neurophysiology.

[33]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

[34]  R. Beer Dynamical approaches to cognitive science , 2000, Trends in Cognitive Sciences.

[35]  V Brezina,et al.  The neuromuscular transform constrains the production of functional rhythmic behaviors. , 2000, Journal of neurophysiology.

[36]  J. Jing,et al.  Neural Mechanisms of Motor Program Switching inAplysia , 2001, The Journal of Neuroscience.

[37]  Eytan Ruppin,et al.  Emergence of Memory-Driven Command Neurons in Evolved Artificial Agents , 2001, Neural Computation.

[38]  I. V. Orekhova,et al.  Sonometric measurements of motor-neuron-evoked movements of an internal feeding structure (the radula) in Aplysia. , 2001, Journal of neurophysiology.

[39]  P J Hornby,et al.  Central neurocircuitry associated with emesis. , 2001, The American journal of medicine.

[40]  M. P. Nusbaum,et al.  A small-systems approach to motor pattern generation , 2002, Nature.

[41]  J. Jing,et al.  Interneuronal and peptidergic control of motor pattern switching in Aplysia. , 2002, Journal of neurophysiology.

[42]  Jan Treur,et al.  Putting intentions into cell biochemistry: an artificial intelligence perspective. , 2002, Journal of theoretical biology.

[43]  D. A. Baxter,et al.  Operant Reward Learning in Aplysia: Neuronal Correlates and Mechanisms , 2002, Science.

[44]  J. Jing,et al.  Interneuronal Basis of the Generation of Related but Distinct Motor Programs in Aplysia: Implications for Current Neuronal Models of Vertebrate Intralimb Coordination , 2002, The Journal of Neuroscience.

[45]  Abraham J Susswein,et al.  Comparative neuroethology of feeding control in molluscs. , 2002, The Journal of experimental biology.

[46]  E. Ruppin Evolutionary autonomous agents: A neuroscience perspective , 2002, Nature Reviews Neuroscience.

[47]  Randall D. Beer,et al.  The Dynamics of Active Categorical Perception in an Evolved Model Agent , 2003, Adapt. Behav..

[48]  Valentin A. Nepomnyashchikh,et al.  Emergence of Adaptive Searching Rules from the Dynamics of a Simple Nonlinear System , 2003, Adapt. Behav..

[49]  I. V. Orekhova,et al.  Neuromuscular modulation in Aplysia. I. Dynamic model. , 2003, Journal of neurophysiology.

[50]  Vladimir Brezina,et al.  Neuromuscular modulation in Aplysia. II. Modulation of the neuromuscular transform in behavior. , 2003, Journal of neurophysiology.

[51]  K. R. Weiss,et al.  The effects of food arousal on the latency of biting inAplysia , 1978, Journal of comparative physiology.

[52]  Randall D. Beer,et al.  Evolution and Analysis of Model CPGs for Walking: II. General Principles and Individual Variability , 1999, Journal of Computational Neuroscience.

[53]  H. Chiel,et al.  In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia , 1993, Journal of Comparative Physiology A.

[54]  Jian Jing,et al.  Feeding Neural Networks in the Mollusc Aplysia , 2004, Neurosignals.

[55]  H. Chiel,et al.  The timing of activity in motor neurons that produce radula movements distinguishes ingestion from rejection in Aplysia , 1993, Journal of Comparative Physiology A.

[56]  I. V. Orekhova,et al.  Cycle-to-cycle variability of neuromuscular activity in Aplysia feeding behavior. , 2004, Journal of neurophysiology.

[57]  Irving Kupfermann,et al.  The stimulus control of biting inAplysia , 2004, Journal of comparative physiology.

[58]  Y. Arshavsky,et al.  Dual sensory-motor function for a molluskan statocyst network. , 2004, Journal of neurophysiology.

[59]  K. R. Weiss,et al.  Dynamical basis of intentions and expectations in a simple neuronal network. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[60]  B. Webb Neural mechanisms for prediction: do insects have forward models? , 2004, Trends in Neurosciences.

[61]  Y. Arshavsky,et al.  The Role of Sensory Network Dynamics in Generating a Motor Program , 2005, The Journal of Neuroscience.

[62]  Vladimir Brezina,et al.  Modeling neuromuscular modulation in Aplysia. III. Interaction of central motor commands and peripheral modulatory state for optimal behavior. , 2005, Journal of neurophysiology.

[63]  Catalin V. Buhusi,et al.  What makes us tick? Functional and neural mechanisms of interval timing , 2005, Nature Reviews Neuroscience.

[64]  K. R. Weiss,et al.  Changes of Internal State Are Expressed in Coherent Shifts of Neuromuscular Activity in Aplysia Feeding Behavior , 2005, The Journal of Neuroscience.

[65]  J. Staddon Interval timing: memory, not a clock , 2005, Trends in Cognitive Sciences.

[66]  J. Jing,et al.  Generation of Variants of a Motor Act in a Modular and Hierarchical Motor Network , 2005, Current Biology.

[67]  K. R. Weiss,et al.  Tight or loose coupling between components of the feeding neuromusculature of Aplysia? , 2005, Journal of neurophysiology.

[68]  K. R. Weiss,et al.  Variability of swallowing performance in intact, freely feeding aplysia. , 2005, Journal of neurophysiology.

[69]  U. Dieckmann,et al.  Adaptive Dynamics , 2020, Mathematical Population Genetics and Evolution of Bacterial Cooperation.

[70]  L. Abbott,et al.  Neural network dynamics. , 2005, Annual review of neuroscience.

[71]  Alain Destexhe,et al.  Neuronal Computations with Stochastic Network States , 2006, Science.

[72]  H. Chiel,et al.  Neuromechanics of Coordination during Swallowing in Aplysia californica , 2006, The Journal of Neuroscience.

[73]  A. Bastian Learning to predict the future: the cerebellum adapts feedforward movement control , 2006, Current Opinion in Neurobiology.

[74]  H. Chiel,et al.  Neuromechanics of Multifunctionality during Rejection in Aplysia californica , 2006, The Journal of Neuroscience.

[75]  Xabier E. Barandiaran,et al.  On What Makes Certain Dynamical Systems Cognitive: A Minimally Cognitive Organization Program , 2006, Adapt. Behav..

[76]  J. Jing,et al.  State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network , 2007, The Journal of Neuroscience.

[77]  J. Jing,et al.  Multiple contributions of an input-representing neuron to the dynamics of the aplysia feeding network. , 2007, Journal of neurophysiology.

[78]  J. Jing,et al.  From Hunger to Satiety: Reconfiguration of a Feeding Network by Aplysia Neuropeptide Y , 2007, The Journal of Neuroscience.

[79]  Saeed Tavazoie,et al.  Predictive Behavior Within Microbial Genetic Networks , 2008, Science.

[80]  J. Jing,et al.  An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network , 2008, The Journal of Neuroscience.

[81]  Charles C. Horn,et al.  Why is the neurobiology of nausea and vomiting so important? , 2008, Appetite.

[82]  Barnett,et al.  Supplementary References , 2022 .