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ARTICLE

Proprioceptive Input to Feeding Motor Programs inAplysia

Colin G. Evans and Elizabeth C. Cropper
Journal of Neuroscience 1 October 1998, 18 (19) 8016-8031; DOI: https://doi.org/10.1523/JNEUROSCI.18-19-08016.1998
Colin G. Evans
1Department of Physiology and Biophysics and
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Elizabeth C. Cropper
1Department of Physiology and Biophysics and
2The Fishberg Center for Research in Neurobiology, The Mount Sinai Medical Center, New York, New York 10029
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  • Fig. 1.
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    Fig. 1.

    Schematic illustration of the preparation used to transduce movements of the buccal mass. (Ganglia are not shown.) A string was tied to the anterior tip of the radula and attached to a movement transducer. This transducer detects movement of the radula toward the jaws, which is referred to as protraction (arrow 1), and movement of the radula toward esophageal tissue, which is referred to as retraction (arrow 2). Protraction produces a downward deflection in transducer records, and retraction produces an upward movement. The rest position of the radula (the position before movement is elicited) is indicated by thedotted line in the bottom diagram.

  • Fig. 2.
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    Fig. 2.

    Anatomy of B51. A, Camera lucida drawing of two B51 neurons in the same preparation filled with carboxyfluorescein dye. B, Semischematic drawing showing the peripheral projection of a B51 neuron. Note that the B51 process can be traced to the black tissue contiguous with the esophagus overlying the I4 muscle complex.

  • Fig. 3.
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    Fig. 3.

    Brief stretches applied to each I4 leaflet (dorsal, medial, and lateral; see Fig. 4B1) evoke what appear to be centripetal spikes in B51.

  • Fig. 4.
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    Fig. 4.

    B44 innervates the inner leaflets of the I4 muscle complex. A, Camera lucida drawing of B44 is shown.Bn 2 and Bn 3, Buccal nerves 2 and 3. B1, Semischematic drawing of the radula and attached musculature is shown. The I4 muscle complex has been flipped back to expose the inner leaflets. B2, Intracellular stimulation of B44 (bottom) elicits EJPs recorded intracellularly from a fiber of the dorsal inner leaflet (top). More specifically, EJPs were recorded from the posterior side of the dorsal leaflet, i.e., the side that is closest to the outer leaflets. B3, Stimulation of B44 (bottom) also elicits EJPs that can be recorded from the anterior face of the inner leaflets (top), i.e., the side shown in B1. Note that EJPs recorded from the posterior face of the inner leaflets are larger than those recorded from the anterior face. The posterior face of the inner leaflets lies directly under the tissue that contains processes of B51.

  • Fig. 5.
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    Fig. 5.

    B8 innervates the outer leaflets of the I4 muscle complex. A, Semischematic drawing of the radula and some of its attached musculature, including the I4 muscle complex, is shown. The outer leaflets of the I4 complex are visible because they overlie the inner leaflets. B, Intracellular stimulation of B8 (bottom) elicits EJPs recorded intracellularly from fibers of the outer leaflets (top).

  • Fig. 6.
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    Fig. 6.

    Experiment done in an isolated buccal ganglion showing that B44 and B51 are electrically coupled. Current injections are indicated by horizontal bars. When B51 is depolarized (A), it is more effective at driving B44 than vice versa (B). In part this is attributable to the fact that B51 is further from threshold when it is at its resting membrane potential. Consequently, when B51 is activated by injecting current, there is an underlying DC component to evoked activity (arrow in A).

  • Fig. 7.
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    Fig. 7.

    When B44 is stimulated, B51 is activated centripetally. Experiments were conducted in a reduced preparation in which the I4 muscle was attached to a semi-isotonic force transducer, which served as a movement detector. A1, When B44 is stimulated (top), a contraction is elicited in the I4 muscle (middle), and spikes are recorded in B51 (bottom). Note that responses in B51 are not recorded until a contraction has been elicited and that activity in B51 outlasts the B44 stimulation. A2, The same preparation is shown after the buccal nerves have been cut. Note that B44 stimulation no longer triggers responses in B51. B, An experiment in a preparation in which the periphery and buccal ganglion are pharmacologically isolated is shown. In B1 andB3, the periphery and buccal ganglion are both in normal ASW. In B2, the ganglion is in a solution that blocks synaptic transmission. Note that responses in B51 are recorded even when transmission in the buccal ganglion does not occur.C, Hyperpolarization reduces the size of spikes evoked in B51 in response to stimulation of B44 (C2 vsC1 or C2 vs C3).

  • Fig. 8.
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    Fig. 8.

    B51 is a proprioceptor. A, Experiment conducted in a reduced preparation in which the I4 muscle is attached to a movement transducer. Increases in the firing frequency of B44 (top) evoke bigger I4 contractions (bottom) and more centripetal spikes in B51 (middle). B, Experiment conducted in an intact buccal mass preparation. When the radula is restrained, more centripetal responses are recorded in B51. C, Experiment conducted in a reduced preparation in which the I4 muscle is counterweighted, i.e., a washer is placed on the free end of the transducer arm. Increasing the counterweight increases the number of centripetal spikes in B51 (middle vs left ormiddle vs right panels).

  • Fig. 9.
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    Fig. 9.

    A1, Experiment performed in an isolated buccal ganglion shows that PSPs in B8 are evoked by injection of current into the soma of B51. A2, PSPs are abolished when the buccal ganglion is placed in a solution that abolishes synaptic transmission (i.e., 0 Ca+2 and 10 mm Co+2). B, Experiment conducted in an intact buccal mass preparation is shown. In this experiment B8 activity did not elicit centripetal responses in B51 unless an object was placed between the radula halves.

  • Fig. 10.
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    Fig. 10.

    Central depolarization gates afferent activity in B51. Horizontal bars indicate current injection into B44. A, Centripetal spikes in B51 do not elicit PSPs in B8 when B8 is at its resting membrane potential. B, Current has been injected into the soma of B51, which has been depolarized by 15 mV. Centripetal spikes now elicit PSPs in B8.C, B51 is again at its resting membrane potential. The size of the current pulse injected into B44 is decreased inB so that the B44 firing frequency will remain relatively unchanged; i.e., because B51 and B44 are electrically coupled, some of the current injected into B51 in B is seen by B44. A smaller current pulse is, therefore, used to drive B44 when B51 is depolarized.

  • Fig. 11.
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    Fig. 11.

    A, Experiment conducted in a semi-intact buccal mass preparation. B44 is depolarized (as indicated by the horizontal bars), and centripetal spikes are elicited in B51. When B51 is at its resting potential (left), these centripetal spikes are not effective at triggering retractions [as shown by the transducer recording (bottom trace on the left)]. When B51 is depolarized (middle, right), however, afferent activity is effective at triggering retractions (bottom traces on the middle and right) and plateau potentials in B51 (middle trace on theright). The increased activity in B51 is effective at driving other neurons. Thus, bracketed action potentials in B44 occur when B44 is no longer being stimulated (top trace in the middle). B, Similar experiment except that B51 is depolarized by 20 mV long before afferent activity is elicited. Although this is a less physiologically relevant manipulation, inward currents activated by the depolarization itself are less likely to be changing when afferent activity is elicited. Under these conditions, depolarization is still effective at “gating” centripetal activity; i.e., when B51 is depolarized, afferent spikes trigger activity in B51 that is more long lasting (bottom trace on right) and is effective at driving other neurons [again bracketed action potentials in B44 occur when current is no longer being injected (top trace on right)].

  • Fig. 12.
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    Fig. 12.

    Radula movements and intracellular recordings from B15 and B51 during a carbachol-elicited motor program. The fact that B15 is active suggests that these programs are ingestive. In intact animals, B15 does not fire when animals make rejection responses (Cropper et al., 1990). Left, Activity of B15 and B51 without current injection in either neuron. Right, Depolarizing current injected into B51. Note that radula retractions are more vigorous and that activity in B15 remains phase-locked to B51 activity.

  • Fig. 13.
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    Fig. 13.

    Radula movements and intracellular recordings from left and right B51s during a carbachol-elicited motor program. In this experiment, depolarizing current is periodically injected into both B51s (e.g., left and right panels). The B51s are then returned to the resting membrane potential (e.g.,middle panel). Note that when the B51s are depolarized by current injection, CPG-elicited depolarizations are also larger in amplitude and longer in duration. Additionally, radula retractions become more vigorous. Changes in B51 activity and changes in radula movements occur in parallel. Thus, when B51 is no longer depolarized, radula retraction immediately becomes less vigorous. When B51 is depolarized, again radula movements immediately become enhanced.

  • Fig. 14.
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    Fig. 14.

    Schematic diagram that illustrates current conceptualizations of how radula movements are thought to change as food is ingested (Weiss et al., 1986). A, When food is not ingested, it has been suggested that opening/protraction occurs as the radula moves from a neutral position to a point where it is extended through the animal’s open jaws (arrow 1). It has been suggested that the radula then returns to a neutral state (arrow 2). B, When animals make swallowing responses, the radula moves from a rest position to a hyper-retracted position so that food can be deposited in the esophagus (arrow 1). The radula then returns to the rest position (arrow 2).

  • Fig. 15.
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    Fig. 15.

    Radula movements and intracellular recordings from B51 and B8 during a carbachol-elicited motor program in which radula retractions were relatively vigorous. The B51 neuron was hyperpolarized during the time indicated by the horizontal bar. Note that radula retractions immediately became less vigorous.

  • Fig. 16.
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    Fig. 16.

    Radula movements and intracellular recordings from B51 and B44 during a carbachol-elicited motor program. At the point indicated by the bar above the top trace, a piece of PE tubing was inserted between the radula halves. Radula retraction became more vigorous, and the piece of PE tubing was pulled through the buccal mass. Activity in B44 and B51 was enhanced in parallel to changes in radula movements. At least some of the increased activity in B51 was likely to have been peripherally generated because spikes are recorded when B51 is no longer centrally depolarized (arrow in record of B51 activity, ininset). Also note that spikes in B51 are of different sizes, which also suggests that they are generated at different sites.

  • Fig. 17.
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    Fig. 17.

    Schematic representation of neural activity during a bite (left) and a swallow (right). When bites are converted to swallows, activity in radula closing/retraction motor neurons is enhanced and prolonged (top). These changes in motor neuron activity result, at least partially, from the activation of buccal sensory neurons. Activity is likely to be initiated in radula mechanoafferents at the end of protraction/opening, as food contacts the maximally extended radula (middle). Radula mechanoafferents are likely to remain active as the radula closes on food and may accommodate with maintained stimulation (Miller et al., 1994). Centripetal activity in B51 is likely to occur relatively late during closing/retraction (bottom). Although B44 starts firing as closing/retraction is initiated, it takes time for the I4 muscle to contract. Radula mechanoafferents may, therefore, trigger bite to bite–swallow conversions, whereas centripetal activity in B51 may be more important as swallows are executed.

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The Journal of Neuroscience: 18 (19)
Journal of Neuroscience
Vol. 18, Issue 19
1 Oct 1998
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Proprioceptive Input to Feeding Motor Programs inAplysia
Colin G. Evans, Elizabeth C. Cropper
Journal of Neuroscience 1 October 1998, 18 (19) 8016-8031; DOI: 10.1523/JNEUROSCI.18-19-08016.1998

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Proprioceptive Input to Feeding Motor Programs inAplysia
Colin G. Evans, Elizabeth C. Cropper
Journal of Neuroscience 1 October 1998, 18 (19) 8016-8031; DOI: 10.1523/JNEUROSCI.18-19-08016.1998
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Keywords

  • proprioceptive input
  • Aplysia
  • central pattern generator
  • load compensation
  • plateau potentials
  • feeding behavior

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