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H J Chiel

Publications and source records attributed to H J Chiel.

At least 19 recordsLinked to original sources

Passive hinge forces in the feeding apparatus of Aplysia aid retraction during biting but not during swallowing.

Swallowing and biting responses in the marine mollusk Aplysia are both mediated by a cyclical alternation of protraction and retraction movements of the grasping structure, the radula and underlying odontophore, within the feeding apparatus of the animal, the buccal mass. In vivo observations demonstrate that Aplysia biting is associated with strong protractions and rapid initial retractions, whereas Aplysia swallowing is associated with weaker protractions and slower initial retractions. During biting, the musculature joining the radula/odontophore to the buccal mass (termed the "hinge") is stretched more than in swallowing. To test the hypothesis that stretch of the hinge might contribute to rapid retractions observed in biting, we analyzed the hinge's passive properties. During biting, the hinge is stretched sufficiently to assist retraction. In contrast, during swallowing, the hinge is not stretched sufficiently for its passive forces to assist retraction, because the odontophore's anterior movement is smaller than during biting. A quantitative model demonstrated that steady-state passive forces were sufficient to generate the retraction movements observed during biting. Experimental measures of the relative magnitude of the hinge's active and passive forces at the protraction displacements of biting suggest that passive forces are at least a third of the total force.

Animals↗

Biomechanical properties and a kinetic simulation model of the smooth muscle I2 in the buccal mass of Aplysia.

The muscle I2 is a smooth muscle from the buccal mass of the marine mollusc Aplysia californica whose neural control, in vivo kinematics, and behavioral role have been extensively analyzed. In this study, we measured the activation and contractile dynamics of the muscle in order to construct a Hill-type kinetic model of the muscle. This is the first study to our knowledge, of Aplysia muscle contractile dynamics. The isometric force-frequency relationship of I2 had a frequency threshold of about 6-8 Hz, and its force output saturated at 20-25 Hz, properties that match the high frequency (20 Hz) bursts generated by the B31/B32 neurons that innervate it. Peak isometric force was generated at about 118% of the in situ relaxed length. These results and I2's estimated in vivo kinematics suggest that it generates maximum force at the onset of protraction. The muscle tension during iso-velocity lengthening and shortening was an asymmetric function of velocity. Short range stiffness and yielding responses were observed in lengthening, whereas muscle tension decreased smoothly in shortening. These visco-elastic properties suggest that the I2 muscle can serve to brake forceful retraction movements. A Hill-type model, parameterized from the measurements, captured many of the mechanical properties of I2. Our results provide a quantitative understanding of the biomechanical significance of the muscle's neural control and provide a basis for simulation studies of the control of feeding behavior.

Animals↗

Biorobotic approaches to the study of motor systems.

Biorobotics is a promising new area of research at the interface between biology and robotics. Robots can either be used as physical models of biological systems or be directly inspired by biological studies. A great deal of progress has recently been made in biorobotic studies of locomotion, orientation, and vertebrate arm control.

Animals↗

Kinematic models of the buccal mass of Aplysia californica.

The feeding behavior of the marine mollusc Aplysia californica is an intensively studied model system for understanding the neural control of behavior. Feeding movements are generated by contractions of the muscles of the buccal mass. These muscles are internal and cannot be visualized during behavior. In order to infer the movements of the muscles of the buccal mass, two kinematic models were constructed. The first kinematic model assumed that the complex consisting of the pincer-like radula and the underlying odontophore was spherical in shape. In this model, the radula/odontophore was moved anteriorly or posteriorly and the more superficial buccal muscles (I1/I3 and I2) were fitted around it. Although the overall buccal mass shapes predicted by this model were similar to those observed in vivo during protraction, the shapes predicted during retraction were very different. We therefore constructed a second kinematic model in which the shape of the radula/odontophore was based on the shapes assumed by those structures in vitro when they were passively forced into protraction, rest or retraction positions. As each of these shapes was rotated, the second kinematic model generated overall shapes of the buccal mass that were similar to those observed in vivo during swallowing and tearing, and made predictions about the antero-posterior length of the buccal mass and the relative location of the lateral groove. These predictions were consistent with observations made in vivo and in vitro. The kinematic patterns of intrinsic buccal muscles I1 and I2 in vivo were estimated using the second model. Both models make testable predictions with regard to the functions and neural control of intrinsic buccal muscles I2 and I3.

Animals↗

The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment.

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.

Adaptation, Psychological↗

A nonisometric kinetic model for smooth muscle.

We have modeled the nonisometric contractile dynamics of smooth muscle by modifying a four-state model of actin and myosin bonds originally proposed by Hai and Murphy to simulate the isometric contractions of vertebrate smooth muscle. The model includes a latch bridge, which cycles more slowly than regular cross bridges. We generalized this model to represent the calcium-regulated processes of vertebrate and invertebrate smooth muscles. We added length dynamics by assuming length-dependent bonding and unbonding rates for the cross bridges. The calculation of the cross-bridge length distribution was simplified by assuming a Gaussian distribution, as first done by Zahalak for skeletal muscle. To test the performance of this model, we simulated isometric and nonisometric responses of different kinds of smooth muscle, including vascular smooth muscle, airway smooth muscle, molluscan catch muscle (anterior byssus retractor muscle), and Aplysia I(2) muscle. The model captures the economical force maintenance property at the later stages of isometric muscle contraction and responses to imposed lengthening and shortening movements.

Actomyosin↗

The kinematics of swallowing in the buccal mass of Aplysia californica.

Changes in the positions, shapes and movements of the feeding apparatus (buccal mass) of the marine mollusc Aplysia californica were studied in intact, transilluminated juveniles. The buccal mass assumes characteristic shapes as its internal structure, the radula/odontophore, moves anteriorly (protracts) or posteriorly (retracts). These shapes are especially distinctive when the radula/odontophore has protracted forwards fully, is close to its resting or neutral position, or has retracted backwards fully. We refer to the shapes that occur at full protraction, transition and full retraction as shape 1 (spherical), shape 2 (ovoid) and shape 3 (gamma-shaped), respectively. We introduce this shape nomenclature in order to avoid confusion with the existing terms protraction and retraction, which we reserve exclusively to describe the direction of movement of the radula/odontophore. The observed shape changes do not agree with those predicted on the basis of in vitro observations of a feeding head preparation, but are similar to shapes observed in vitro in the snail Lymnaea stagnalis. The buccal mass also rotates approximately 10 degrees dorsally during retraction, pivoting on the attachment to the mouth, before the subsequent protraction and return of the buccal mass to the transition shape. This rotation may be due to activation of the extrinsic muscles of the buccal mass. Plots of the buccal mass shape parameters eccentricity versus ellipticity create a two-dimensional shape space, which accurately quantifies the subtle transitions of shape between the different phases of the feeding cycle. Quantitative differences are observed between pure swallows and swallows with tearing behavior, but the qualitative shapes are similar. Hysteresis in the shape space plots of most swallows provides evidence for the hypothesis that protraction and retraction each have distinct 'active' and 'return' phases. The observed kinematic pattern imposes constraints on the internal structures of the buccal mass and may be used to infer the shape and positions of the radula and odontophore.

Animals↗

Activity patterns of the B31/B32 pattern initiators innervating the I2 muscle of the buccal mass during normal feeding movements in Aplysia californica.

1. B31 and B32 are pattern-initiator neurons in the buccal ganglia of Aplysia. Along with the B61/B62 neurons, B31/B32 are also motor neurons that innervate the 12 buccal muscle via the I2 nerve. This research was aimed at determining the physiological functions of the B31/B32 and B61/B62 neurons, and of the I2 muscle. 2. Stimulating the I2 muscle in the radula rest position produces radula protraction. In addition, in behaving animals lesioning either the muscle or the I2 nerve greatly reduces radula protraction. 3. During buccal motor programs in reduced preparations, B31/B32 and B61/62 fire preceding activity in neuron B4, whose firing indicates the onset of radula retraction. In addition, during both ingestion-like and rejection-like patterns the activity in the I2 nerve is correlated with protraction. 4. B31/B32 fire at frequencies of 15-25 Hz. Neither B31/B32 nor B61/B62 elicit facilitating end-junction potentials (EJPs) and electromyograms (EMGs) in the I2 muscle. EMGs from B31/B32 are smaller than those from B61/B62. B31/B32 and B61/B62 innervate all areas of the muscle approximately uniformly. 5. In behaving animals, EMGs consistent with B31/B32 activity are seen in the I2 muscle during the protraction phase of biting, swallowing, and rejection movements. In addition, the I2 muscle receives inputs that cannot be attributed to either the B31/B32 or B61/B62 neurons, either because the potentials are too large, firing frequencies are too low, or a prominent facilitation is seen. Such potentials are associated with lip movements, and also with radula retraction. 6. EMGs were recorded from the I2 muscle during feeding behavior after a lesion of the I2 nerve. Animals that had severe deficits in protraction showed no activity consistent with B31/B32 or B61/B62, but did show activity during retraction. 7. Our data indicate that the I2 muscle and the B31/B32 motor neurons are essential constituents contributing to protraction movements. Activity in these neurons is associated with radula protraction, which occurs as a component of a number of different feeding movements. The I2 muscle may also contribute to retraction, via activation by other motor neurons.

Action Potentials↗

A new technique for chronic single-unit extracellular recording in freely behaving animals using pipette electrodes.

Using extracellular pipette electrodes made of glass or plastic whose tip diameters ranged from 60 to 100 microns, it was possible to record the activity of single identified neurons in freely behaving animals. Multiple pipettes can be reliably positioned and attached to the sheath. Large signals can be obtained from neurons having soma diameters as small as 70 microns. We have used this technique to monitor the activity of an identified interneuron (B4/B5) during feeding behavior in the marine mollusk Aplysia californica. The technique can also be used in reduced or in vitro preparations for rapidly mapping the neural activity of a ganglion without removing its sheath.

Animals↗

Neural architectures for adaptive behavior.

How do animals use the same peripheral structures to generate different behavioral responses? Three different neuronal architectures have been proposed to mediate this task: dedicated circuitry; distributed circuitry; and reorganizing circuitry. This review will critically examine the evidence for these different architectures in invertebrate circuits, and then examine the evidence for them in more complex vertebrate circuits. The evidence suggests that these different architectures are unlikely to be found in pure form in most neural circuits, but are useful for guiding the experimental analysis of circuitry.

Adaptation, Psychological↗

The timing of activity in motor neurons that produce radula movements distinguishes ingestion from rejection in Aplysia.

1. We have studied the neural circuitry mediating ingestion and rejection in Aplysia using a reduced preparation that produces ingestion-like and rejection-like motor patterns in response to physiological stimuli. 2. We have characterized 3 buccal ganglion motor neurons that produce specific movements of the radula and buccal mass. B8a and B8b act to close the radula. B10 acts to close the jaws and retract the radula. 3. The patterns of activity in these neurons can be used to distinguish the ingestion-like and rejection-like motor patterns. B8a, B8b and B10 are active together during the ingestion-like pattern. Activity in B8a and B8b ends prior to the onset of activity in B10 during the rejection-like pattern. 4. Our data suggest that these neurons undergo similar patterns of activity in vivo. During both feeding-like patterns, the activity and peripheral actions of B8a, B8b, and B10 are consistent with radula movements observed during ingestion and rejection. In addition, the extracellular activity produced by these neurons is consistent with neural activity observed in vivo during ingestion and rejection. 5. Our data suggest that the different activity patterns observed in these motor neurons contribute to the different radula movements that distinguish ingestion from rejection.

Animals↗

In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia.

1. We are studying the neural basis of consummatory feeding behavior in Aplysia using intact, freely moving animals. 2. Video records show that the timing of radula closure during the radula protraction-retraction cycle constitutes a major difference between ingestion (biting or swallowing) and rejection. During ingestion, the radula is closed as it retracts. During rejection, the radula is closed as it protracts. 3. We observed two patterns of activity in nerves which are likely to mediate these radula movements. Patterns I and II are associated with ingestion and rejection, respectively, and are distinguished by the timing of radula nerve activity with respect to the onset of buccal nerve 2 activity. 4. The association of ingestion with pattern I is maintained when the animal feeds on a polyethylene tube, the same food substrate used to elicit rejection responses. Under these conditions, pattern I is associated with either swallowing or no net tube movement. 5. Most transitions from swallowing to rejection were preceded by one or more occurrences of pattern I in which there was no net tube movement, suggesting that these transitions can be predicted. 6. Our data suggest that these two patterns can be used to distinguish ingestion from rejection.

Animals↗

Learning that food is inedible in freely behaving Aplysia californica.

Freely behaving Aplysia californica can learn that food is inedible. Animals were given access to seaweed tied into canvas and attached to a force transducer. Animals repeatedly found the stimulus, attempted to ingest it, and failed. The force transducer provided an objective record of the number of attempts made by the animal to ingest the stimulus, the length of each attempt, and its intensity (i.e., peak force exerted). Within 2.5 hr, animals showed significant declines in these 3 measures of response to the stimulus. When exposed to the same stimulus the next day, animals showed more rapid declines in responsiveness, which indicate a retention of learning. Training appeared to be specific: Responses to the seaweed Laurencia of animals previously trained on the seaweed Ulva do not differ from the responses of naive animals to Laurencia.

Animals↗

Optical methods can be utilized to map the location and activity of putative motor neurons and interneurons during rhythmic patterns of activity in the buccal ganglion of Aplysia.

We sought to develop a map of the locations of neurons that are active during patterned activity in the buccal ganglion of Aplysia using optical techniques. Staining ganglia with a voltage-sensitive absorbance dye (JPW 1124) did not prevent them from generating patterned activity similar to that observed before staining, in response to shock of the esophageal nerve. Absorbance changes were monitored with a 124-element photodiode array, while extracellular electrodes monitored activity of the 6 buccal nerves. Optical and extracellular spikes were grouped with the aid of a template matching program; a total of 120 distinct units were detected in one 15 s recording. Optical signals (83 units) were found in the region of the ganglion containing mainly large neurons. Of these, 13 were detected on both optical and extracellular electrode recordings, suggesting that they might be motor neurons, while 25 of the optically detected neurons appeared not to be correlated with extracellular activity, suggesting that they might be interneurons. It was not possible to determine whether the remaining 45 optically identified units did or did not have correlated nerve activity. The ganglionic locations of putative motor neurons corresponded to the locations of large neurons identified by backfilling nerves of other buccal ganglia, and were consistent with the locations of putative motor neurons found in two other ganglia studied using optical methods. Thus, optical methods have generated a map of the locations and activity patterns of putative motor neurons and interneurons in the buccal ganglion that may be involved in the generation of rhythmic patterns.

Animals↗

Simulation of adaptive behavior.

Behaviors as diverse as swimming, withdrawal, escape, locomotion and feeding have been simulated using neuroethological and neurophysiological data obtained from a variety of animals. These simulations are providing new insights into the neural circuitry that generates adaptive behavior, as well as new ideas for the design of artificial autonomous devices.

Adaptation, Psychological↗

Multiple roles of a histaminergic afferent neuron in the feeding behavior of Aplysia.

The cellular and circuit properties of individual identified neurons in invertebrates can be readily studied; hence it is possible to determine how the complex properties of nerve cells function in the generation of behavior. Recent studies of the cellular basis of feeding behavior in the marine mollusc Aplysia have focused on a neuron, C2, that has a variety of complex properties that determine the behavioral functions of the neuron. C2 conveys mechanosensory information from the mouth of the animal. It receives a complex pattern of inputs during feeding behavior, and generates diverse outputs that may shape behavior. It can act to filter out slow or sporadic sensory inputs, and its own outputs can be 'gated' by synaptic input. C2 uses histamine as its transmitter, and some of its synaptic outputs are modulatory and contribute to the expression of an arousal state induced by food. Other outputs shape feeding behavior directly by affecting motor neurons, as well as presynaptically inhibiting the outputs of feeding motor programs. Thus, the complex properties of this neuron may contribute to the flexibility and adaptability of feeding in Aplysia. Studies of C2 have expanded our concepts of the properties of sensory neurons.

Action Potentials↗

Circuits constructed from identified Aplysia neurons exhibit multiple patterns of persistent activity.

We have used identified neurons from the abdominal ganglion of the mollusc Aplysia to construct and analyze two circuits in vitro. Each of these circuits was capable of producing two patterns of persistent activity; that is, they had bistable output states. The output could be switched between the stable states by a brief, external input. One circuit consisted of cocultured L10 and left upper quadrant (LUQ) neurons that formed reciprocal, inhibitory connections. In one stable state L10 was active and the LUQ was quiescent, whereas in the other stable state L10 was quiescent and the LUQ was active. A second circuit consisted of co-cultured L7 and L12 neurons that formed reciprocal, excitatory connections. In this circuit, both cells were quiescent in one stable state and both cells fired continuously in the other state. Bistable output in both circuits resulted from the nonlinear firing characteristics of each neuron and the feedback between the two neurons. We explored how the stability of the neuronal output could be controlled by the background currents injected into each neuron. We observed a relatively well-defined range of currents for which bistability occurred, consistent with the values expected from the measured strengths of the connections and a simple model. Outside of the range, the output was stable in only a single state. These results suggest how stable patterns of output are produced by some in vivo circuits and how command neurons from higher neural centers may control the activity of these circuits. The criteria that guided us in forming our circuits in culture were derived from theoretical studies on the properties of certain neuronal network models (e.g., Hopfield, J. J. 1984. Proc. Natl. Acad. Sci. USA. 81:3088-3092). Our results show that circuits consisting of only two co-cultured neurons can exhibit bistable output states of the form hypothesized to occur in populations of neurons.

Animals↗

An identified histaminergic neuron can modulate the outputs of buccal-cerebral interneurons in Aplysia via presynaptic inhibition.

We have identified 2 buccal-cerebral interneurons (BCIs), B17 and B18, that appear to be involved in the coordination of feeding behavior in Aplysia. The BCIs have their cell bodies in the buccal ganglion, but send axons to the cerebral ganglion via the cerebral-buccal connectives. The BCIs appear to make monosynaptic connections with neurons in the cerebral ganglion that modulate extrinsic muscles involved in feeding behavior. B17 and B18 are activated antiphasically during a motor program induced by stimulating the esophageal nerve and appear to "read out" different phases of the buccal program to different cells in the cerebral ganglion. B17 and B18 are not necessary, and probably not sufficient, to generate the buccal program. These BCIs, and other cells like them in the buccal ganglion, may be capable of coordinating the activity of the intrinsic muscles of the buccal mass with the activity of its extrinsic muscles, and perhaps with those of the lips, mouth, and tentacles. Identified histaminergic neuron, C2, can modulate the outputs of the BCIs onto their synaptic followers in the cerebral ganglion. Firing of C2 inhibits spiking of the BCIs, probably via cerebral-buccal interneurons. C2 also decreases the size of the EPSP that B17 and B18 evoke in cerebral neuron C4. C2 appears to do so monosynaptically, and it decreases the conductance of C4, ruling out one possible postsynaptic mechanism of action. Variance analysis of the EPSPs evoked by B18 supports the hypothesis that C2 acts presynaptically to decrease the release of transmitter. Applications of histamine to the solution bathing the neuron mimic the effect of firing C2 and reduce the size of the EPSPs B18 induces in C4. The bath-applied histamine appears to act directly on B18, since it elicits a voltage-dependent increased conductance hyperpolarization recorded in the soma of B18, and the hyperpolarization persists in a solution in which synaptic transmission has been blocked. Histamine did not produce any marked changes of the duration of a TEA-broadened somatic action potential of B18. To the extent that the soma of B18 reflects the membrane properties of its synaptic terminal region, the data suggest that histamine may produce presynaptic inhibition by hyperpolarizing the synaptic terminal region.

Analysis of Variance↗