Peptidergic motoneurons in the buccal ganglia of Aplysia californica Immunocytochemical, morphological, and physiological characterizations

PaulJ. Church; KevinP. Cohen; MarshaL. Scott; MarkD. Kirk

doi:10.1007/bf00198352

Fast Synaptic Connections From CBIs to Pattern-Generating Neurons in Aplysia: Initiation and Modification of Motor Programs

Journal of Neurophysiology ◽

10.1152/jn.00497.2002 ◽

2003 ◽

Vol 89 (4) ◽

pp. 2120-2136 ◽

Cited By ~ 31

Author(s):

Itay Hurwitz ◽

Irving Kupfermann ◽

Klaudiusz R. Weiss

Keyword(s):

Central Pattern Generator ◽

Motor Pattern ◽

Aplysia Californica ◽

Pattern Generator ◽

Synaptic Connections ◽

Motor Patterns ◽

Motor Programs ◽

Postsynaptic Potentials ◽

Buccal Ganglia ◽

Very High

Consummatory feeding movements in Aplysia californica are organized by a central pattern generator (CPG) in the buccal ganglia. Buccal motor programs similar to those organized by the CPG are also initiated and controlled by the cerebro-buccal interneurons (CBIs), interneurons projecting from the cerebral to the buccal ganglia. To examine the mechanisms by which CBIs affect buccal motor programs, we have explored systematically the synaptic connections from three of the CBIs (CBI-1, CBI-2, CBI-3) to key buccal ganglia CPG neurons (B31/B32, B34, and B63). The CBIs were found to produce monosynaptic excitatory postsynaptic potentials (EPSPs) with both fast and slow components. In this report, we have characterized only the fast component. CBI-2 monosynaptically excites neurons B31/B32, B34, and B63, all of which can initiate motor programs when they are sufficiently stimulated. However, the ability of CBI-2 to initiate a program stems primarily from the excitation of B63. In B31/B32, the size of the EPSPs was relatively small and the threshold for excitation was very high. In addition, preventing firing in either B34 or B63 showed that only a block in B63 firing prevented CBI-2 from initiating programs in response to a brief stimulus. The connections from CBI-2 to the buccal ganglia neurons showed a prominent facilitation. The facilitation contributed to the ability of CBI-2 to initiate a BMP and also led to a change in the form of the BMP. The cholinergic blocker hexamethonium blocked the fast EPSPs induced by CBI-2 in buccal ganglia neurons and also blocked the EPSPs between a number of key CPG neurons within the buccal ganglia. CBI-2 and B63 were able to initiate motor patterns in hexamethonium, although the form of a motor pattern was changed, indicating that non-hexamethonium-sensitive receptors contribute to the ability of these cells to initiate bursts. By contrast to CBI-2, CBI-1 excited B63 but inhibited B34. CBI-3 excited B34 and not B63. The data indicate that CBI-1, -2, and -3 are components of a system that initiates and selects between buccal motor programs. Their behavioral function is likely to depend on which combination of CBIs and CPG elements are activated.

Download Full-text

Compartmentalization of pattern-initiation and motor functions in the B31 and B32 neurons of the buccal ganglia of Aplysia californica

Journal of Neurophysiology ◽

10.1152/jn.1994.71.4.1514 ◽

1994 ◽

Vol 71 (4) ◽

pp. 1514-1527 ◽

Cited By ~ 34

Author(s):

I. Hurwitz ◽

R. S. Goldstein ◽

A. J. Susswein

Keyword(s):

Motor Neurons ◽

Action Potentials ◽

Divalent Cations ◽

Aplysia Californica ◽

Strongly Coupled ◽

Buccal Ganglia ◽

Signaling Mechanisms ◽

Slow Potentials ◽

Coupled Cells ◽

Electrical Signaling

1. The B31 and B32 cells in the buccal ganglia of Aplysia californica have unusual electrophysiological features. The somata of these strongly coupled cells do not sustain conventional action potentials. Brief depolarization of the soma produces a complex, sustained regenerative slow depolarization that is followed by a hyperpolarization. This activity in B31/B32 is correlated with a patterned burst of activity expressed in many of the neurons of the buccal ganglia. 2. Intracellular fills of B31/B32 showed that they have many neurites adjacent to the soma, as well as peripheral axons leaving the buccal ganglia via the radular nerve and innervating the Intrinsic-2 (I2) muscle of the buccal mass. Varicosities of B31/B32 axons are seen within the muscle. Backfills from I2 filled two adjacent B31/B32 cells as well as two newly identified neurons: B61 and B62. 3. Intracellular recording from the B31/B32 axons shows that they sustain conventional action potentials. These are recorded in the soma as approximately 10-mV fast depolarizations. Failed spikes in B31/B32, and conventional spikes in B61/B62, are correlated one for one with end-junction potentials (EJPs) in the I2 muscle. The EJPs are present even when the ganglia and muscles are bathed in high-divalent cations seawater. Thus B31/B32 and B61/B62 are motor neurons to the I2 muscle. 4. To determine whether the ability of B31/B32 to initiate patterned bursts is mediated by spikes in the axon or by slow potentials in the soma, the B31/B32 axon was stimulated directly while recording from the B31/B32 soma. Patterned bursts were never seen in the absence of slow potentials in the soma. Thus the ability of B31/B32 to initiate patterned bursts is localized to the soma and adjacent neurites. Slow potentials influence and cause spiking in adjacent neurons even in the absence of axon spikes. 5. These data show that the B31/B32 cells serve two functions that are compartmentalized in different regions of the cell and are mediated via different electrical signaling mechanisms. The B31/B32 somata utilize slow, sustained potentials as part of a network initiating patterned activity in the buccal ganglia. The B31/B32 axons utilize conventional action potentials, and act as motor neurons to the I2 muscle.

Download Full-text

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

Journal of Neurophysiology ◽

10.1152/jn.1996.75.4.1309 ◽

1996 ◽

Vol 75 (4) ◽

pp. 1309-1326 ◽

Cited By ~ 62

Author(s):

I. Hurwitz ◽

D. Neustadter ◽

D. W. Morton ◽

H. J. Chiel ◽

A. J. Susswein

Keyword(s):

Feeding Behavior ◽

Motor Neurons ◽

Activity Patterns ◽

Aplysia Californica ◽

Motor Programs ◽

Physiological Functions ◽

Rest Position ◽

Buccal Ganglia ◽

Normal Feeding ◽

Protraction Phase

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.

Download Full-text

Transmission Electron Microscopy Studies of Pore Cells in Limax Maximus

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100080705 ◽

1977 ◽

Vol 35 ◽

pp. 656-657

Author(s):

B. S. Beltz

Keyword(s):

Electron Microscopy ◽

Cell Periphery ◽

Salivary Duct ◽

Terrestrial Mollusc ◽

Buccal Ganglia ◽

Transmission Electron ◽

Pore Cells ◽

Gland Tissue ◽

Storage Area ◽

Limax Maximus

The cells which are described in this study surround the salivary nerve of the terrestrial mollusc, Limax maximus. The salivary system of Limax consists of bilateral glands, ducts, and nerves. The salivary nerves originate at the buccal ganglia, which are situated on the posterior face of the buccal mass, and run along the salivary duct to the gland. The salivary nerve branches several times near the gland, and eventually sends processes into the gland.The pore cells begin to appear at the first large branch point of the salivary nerve, near the gland (Figure 1). They follow the nerve distally and eventually accompany the nerve branches into the gland tissue. The cells are 20-50 microns in diameter and contain very small nuclei (1-5 microns) (Figure 2).The cytoplasm of the pore cells is segregated into a storage area of glycogen and an organelle region located in a band around the cell periphery (Figure 3).

Download Full-text

Registered Report: Transcriptional Analysis of Savings Memory Suggests Forgetting Is Due to Retrieval Failure

10.31234/osf.io/h59jv ◽

2020 ◽

Author(s):

Robert Calin-Jageman ◽

Irina Calin-Jageman ◽

Tania Rosiles ◽

Melissa Nguyen ◽

Annette Garcia ◽

...

Keyword(s):

Memory Trace ◽

Aplysia Californica ◽

Transcriptional Response ◽

Transcriptional Analysis ◽

Retrieval Failure ◽

Initial Learning ◽

Rigorous Test ◽

Stage 1 ◽

Induced Changes

[[This is a Stage 2 Registered Report manuscript now accepted for publication at eNeuro. The accepted Stage 1 manuscript is posted here: https://psyarxiv.com/s7dft, and the pre-registration for the project is available here (https://osf.io/fqh8j, 9/11/2019). A link to the final Stage 2 manuscript will be posted after peer review and publication.]] There is fundamental debate about the nature of forgetting: some have argued that it represents the decay of the memory trace, others that the memory trace persists but becomes inaccessible due to retrieval failure. These different accounts of forgetting lead to different predictions about savings memory, the rapid re-learning of seemingly forgotten information. If forgetting is due to decay, then savings requires re-encoding and should thus involve the same mechanisms as initial learning. If forgetting is due to retrieval failure, then savings should be mechanistically distinct from encoding. In this registered report we conducted a pre-registered and rigorous test between these accounts of forgetting. Specifically, we used microarray to characterize the transcriptional correlates of a new memory (1 day after training), a forgotten memory (8 days after training), and a savings memory (8 days after training but with a reminder on day 7 to evoke a long-term savings memory) for sensitization in Aplysia californica (n = 8 samples/group). We found that the re-activation of sensitization during savings does not involve a substantial transcriptional response. Thus, savings is transcriptionally distinct relative to a newer (1-day old) memory, with no co-regulated transcripts, negligible similarity in regulation-ranked ordering of transcripts, and a negligible correlation in training-induced changes in gene expression (r = .04 95% CI [-.12, .20]). Overall, our results suggest that forgetting of sensitization memory represents retrieval failure.

Download Full-text

Stage 1 Registered Report Manuscript - Transcriptional Correlates of Savings Memory: Is Forgetting Due to Decay or Retrieval Failure?

10.31234/osf.io/s7dft ◽

2020 ◽

Author(s):

Robert Calin-Jageman ◽

Irina Calin-Jageman ◽

Tania Rosiles ◽

Melissa Nguyen ◽

Annette Garcia ◽

...

Keyword(s):

Gene Expression ◽

Memory Trace ◽

Aplysia Californica ◽

Retrieval Failure ◽

Initial Learning ◽

Rigorous Test ◽

Regulated Gene Expression ◽

Stage 1 ◽

Weak Similarity

[[This is a Stage 1 Registered Report manuscript. The project was submitted for review to eNeuro. Upon revision and acceptance, this version of the manuscript was pre-registered on the OSF (9/11/2019, https://osf.io/fqh8j) (but due to an oversight not posted as a preprint until July 2020). A Stage 2 manuscript is now posted as a pre-print (https://psyarxiv.com/h59jv) and is under review at eNeuro. A link to the final Stage 2 manuscript will be added when available.]]There is fundamental debate about the nature of forgetting: some have argued that it represents the decay of the memory trace, others that the memory trace persists but becomes inaccessible due to retrieval failure. These different accounts of forgetting make different predictions about savings memory, the rapid re-learning of seemingly forgotten information. If forgetting is due to decay then savings requires re-encoding and should thus involve the same mechanisms as initial learning. If forgetting is due to retrieval-failure then savings should be mechanistically distinct from encoding. In this registered report we conducted a pre-registered and rigorous test between these accounts of forgetting. Specifically, we used microarray to characterize the transcriptional correlates of a new memory (1 day from training), a forgotten memory (8 days from training), and a savings memory (8 days from training but with a reminder on day 7 to evoke a long-term savings memory) for sensitization in Aplysia californica (n = 8 samples/group). We find that the transcriptional correlates of savings are [highly similar / somewhat similar / unique] relative to new (1-day-old) memories. Specifically, savings memory and a new memory share [X] of [Y] regulated transcripts, show [strong / moderate / weak] similarity in sets of regulated transcripts, and show [r] correlation in regulated gene expression, which is [substantially / somewhat / not at all] stronger than at forgetting. Overall, our results suggest that forgetting represents [decay / retrieval-failure / mixed mechanisms].

Download Full-text