Diverse synaptic connections between peptidergic radula mechanoafferent neurons and neurons in the feeding system of Aplysia.

The buccal ganglion of Aplysia contains a heterogeneous population of peptidergic, radula mechanoafferent (RM) neurons. To investigate their function, two of the larger RM cells (B21, B22) were identified by morphological and electrophysiological criteria. Both are low-threshold, rapidly adapting, mechanoafferent neurons that responded to touch of the radula, the structure that grasps food during ingestive and egestive feeding movements. Sensory responses of the cells consisted of spike bursts at frequencies of 8-35 Hz. Each cell was found to make chemical, electrical, or combined synapses with other sensory neurons, motor neurons and interneurons involved in radula closure and/or protraction-retraction movements of the odontophore. Motor neurons receiving input included the following: B8a/b, B15, and B16, which innervate muscles contributing to radula closing; and B82, a newly identified neuron that innervates the anterodorsal region of the I1/I3 muscles of the buccal mass. B21 and B22 can affect buccal motor programs by way of their connections to interneurons such as B19 and B64. Fast, chemical, excitatory postsynaptic potentials (EPSPs) produced by RM neurons, such as B21, exhibited strong, frequency-dependent facilitation, a form of homosynaptic plasticity. Firing B21 also produced a slow EPSP in B15 that increased the excitability of the cell. Thus a sensory neuron mediating a behavioral response may have modulatory effects. The data suggest multiple functions for RM neurons including 1) triggering of phase transitions in rhythmic motor programs, 2) adjusting the force of radula closure, 3) switching from biting to swallowing or swallowing to rejection, and 4) enhancing food-induced arousal.

[1]  I Kupfermann,et al.  Outputs of radula mechanoafferent neurons in Aplysia are modulated by motor neurons, interneurons, and sensory neurons. , 2000, Journal of neurophysiology.

[2]  P. Meyrand,et al.  Dynamic Restructuring of a Rhythmic Motor Program by a Single Mechanoreceptor Neuron in Lobster , 1999, The Journal of Neuroscience.

[3]  S. Baccus,et al.  Synaptic facilitation by reflected action potentials: enhancement of transmission when nerve impulses reverse direction at axon branch points. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  I. Hurwitz,et al.  Different roles of neurons B63 and B34 that are active during the protraction phase of buccal motor programs in Aplysia californica. , 1997, Journal of neurophysiology.

[5]  P E Crago,et al.  The kinematics of swallowing in the buccal mass of Aplysia californica. , 1997, The Journal of experimental biology.

[6]  D A Price,et al.  Release of Peptide Cotransmitters in Aplysia: Regulation and Functional Implications , 1996, The Journal of Neuroscience.

[7]  E. Cropper,et al.  Multiple mechanisms for peripheral activation of the peptide-containing radula mechanoafferent neurons B21 and B22 of Aplysia. , 1996, Journal of neurophysiology.

[8]  C G Evans,et al.  Characterization of a radula opener neuromuscular system in Aplysia. , 1996, Journal of neurophysiology.

[9]  A. Mar,et al.  Modulation of Conduction Block in Leech Mechanosensory Neurons , 1996, The Journal of Neuroscience.

[10]  I. Hurwitz,et al.  B64, a newly identified central pattern generator element producing a phase switch from protraction to retraction in buccal motor programs of Aplysia californica. , 1996, Journal of neurophysiology.

[11]  I. Kupfermann,et al.  Evidence for transmitter similarity of two classes of mechanoreceptor neurons in the cerebral ganglion of Aplysia , 1996, Neuroscience Letters.

[12]  Paul S. Katz,et al.  Intrinsic neuromodulation: altering neuronal circuits from within , 1996, Trends in Neurosciences.

[13]  E R Kandel,et al.  Presynaptic facilitation revisited: state and time dependence , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  H. Chiel,et al.  A new technique for chronic single-unit extracellular recording in freely behaving animals using pipette electrodes , 1995, Journal of Neuroscience Methods.

[15]  I. Kupfermann,et al.  A population of SCP-containing neurons in the buccal ganglion of Aplysia are radula mechanoafferents and receive excitation of central origin , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  P. Church,et al.  Activity of multiple identified motor neurons recorded intracellularly during evoked feedinglike motor programs in Aplysia. , 1994, Journal of neurophysiology.

[17]  K. R. Weiss,et al.  cAMP-dependent phosphorylation of Aplysia twitchin may mediate modulation of muscle contractions by neuropeptide cotransmitters. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  K. Weiss,et al.  Characterization of the membrane ion currents of a model molluscan muscle, the accessory radula closer muscle of Aplysia california. I. Hyperpolarization-activated currents. , 1994, Journal of neurophysiology.

[19]  M. Burrows,et al.  A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  S. L. Hooper,et al.  Physiology and biochemistry of peptidergic cotransmission in Aplysia , 1993, Journal of Physiology-Paris.

[21]  K. R. Weiss,et al.  Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry ofAplysia , 1993, Brain Research.

[22]  K. R. Weiss,et al.  Localization of myomodulin‐like immunoreactivity in the central nervous system and peripheral tissues of Aplysia californica , 1991, The Journal of comparative neurology.

[23]  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.

[24]  C. Govind,et al.  Neuromuscular organization of the buccal system in Aplysia californica , 1991, The Journal of comparative neurology.

[25]  E. Shapiro,et al.  Identification of a peptide specific for Aplysia sensory neurons by PCR-based differential screening , 1991, Science.

[26]  P. Lloyd,et al.  Expression of diverse neuropeptide cotransmitters by identified motor neurons in Aplysia , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  V. Castellucci,et al.  Receptive fields and properties of a new cluster of mechanoreceptor neurons innervating the mantle region and the branchial cavity of the marine mollusk Aplysia californica. , 1991, The Journal of experimental biology.

[28]  P. Lloyd,et al.  Neuropeptide cotransmitters released from an identified cholinergic motor neuron modulate neuromuscular efficacy in Aplysia , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  K. R. Weiss,et al.  Differential firing patterns of the peptide-containing cholinergic motor neurons B15 and B16 during feeding behavior inAplysia , 1990, Brain Research.

[30]  H. Chiel,et al.  Multiple roles of a histaminergic afferent neuron in the feeding behavior of Aplysia , 1990, Trends in Neurosciences.

[31]  R. Harris-Warrick,et al.  Neuromodulation of the crab pyloric central pattern generator by serotonergic/cholinergic proprioceptive afferents , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  M. Kirk,et al.  Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: synaptic connections, effects on ongoing motor rhythms, and peptide modulation. , 1990, Journal of neurophysiology.

[33]  A. Sweet-Cordero,et al.  Modulation of ionic currents in Aplysia motor neuron B15 by serotonin, neuropeptides, and second messengers , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  I Kupfermann,et al.  Selective modulation of spike duration by serotonin and the neuropeptides, FMRFamide, SCPB, buccalin and myomodulin in different classes of mechanoafferent neurons in the cerebral ganglion of Aplysia , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  AJ Susswein,et al.  Identification and characterization of neurons initiating patterned neural activity in the buccal ganglia of Aplysia , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  J. Swanson,et al.  Macrophages possess probenecid-inhibitable organic anion transporters that remove fluorescent dyes from the cytoplasmic matrix , 1987, The Journal of cell biology.

[37]  I Kupfermann,et al.  Multiple neuropeptides in cholinergic motor neurons of Aplysia: evidence for modulation intrinsic to the motor circuit. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[38]  W. Sossin,et al.  Peptidergic modulation of neuronal circuitry controlling feeding in Aplysia , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  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.

[40]  H. Chiel,et al.  Sensory function and gating of histaminergic neuron C2 in Aplysia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  Alison J. Longley,et al.  Serotonin immunoreactivity of neurons in the gastropod Aplysia californica. , 1986, Journal of neurobiology.

[42]  B. McNaughton,et al.  Intracellular fluorescent staining with carboxyfluorescein: a rapid and reliable method for quantifying dye-coupling in mammalian central nervous system , 1986, Journal of Neuroscience Methods.

[43]  I. Kupfermann,et al.  Biochemical and immunocytological localization of molluscan small cardioactive peptides in the nervous system of Aplysia californica , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  J. Byrne,et al.  Post-tetanic potentiation inAplysia sensory neurons , 1984, Brain Research.

[45]  E. Kandel,et al.  Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. , 1983, Journal of neurophysiology.

[46]  A. Wilson,et al.  Role of proprioceptive reflexes in control of feeding muscles of Aplysia. , 1983, Journal of neurophysiology.

[47]  I Kupfermann,et al.  Interganglionic cerebral-buccal mechanoafferents of Aplysia: receptive fields and synaptic connections to different classes of neurons involved in feeding behavior. , 1982, Journal of neurophysiology.

[48]  I. Kupfermann,et al.  Response properties and synaptic connections of mechanoafferent neurons in cerebral ganglion of Aplysia. , 1979, Journal of neurophysiology.

[49]  H. Lorković Cellular Basis of Behavior: An Introduction to Behavioral Neurology , 1977 .

[50]  D. Gardner Interconnections of identified multiaction interneurons in buccal ganglia of Aplysia. , 1977, Journal of neurophysiology.

[51]  E. Kandel,et al.  Receptive fields and response properties of mechanoreceptor neurons innervating siphon skin and mantle shelf in Aplysia. , 1974, Journal of neurophysiology.

[52]  D. V. Essen,et al.  The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech. , 1973 .

[53]  B. Jahan-Parwar Behavioral and Electrophysiological Studies on Chemoreception in Aplysia , 1972 .

[54]  D. Gardner,et al.  Bilateral Symmetry and Interneuronal Organization in the Buccal Ganglia of Aplysia , 1971, Science.

[55]  H. H. Howells,et al.  The Structure and Function of the Alimentary Canal of Aplysia Punctata , 1942 .

[56]  K. Abromeit Music Received , 2023, Notes.

[57]  K. Weiss,et al.  Characterization of the membrane ion currents of a model molluscan muscle, the accessory radula closer muscle of Aplysia californica. III. Depolarization-activated Ca current. , 1994, Journal of neurophysiology.

[58]  I Kupfermann,et al.  Motor control of buccal muscles in Aplysia. , 1978, Journal of neurophysiology.

[59]  E. Kandel Cellular basis of behavior: An introduction to behavioral neurobiology. , 1976 .

[60]  D. van Essen The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech , 1973, The Journal of physiology.