Characterization of a radula opener neuromuscular system in Aplysia

Abstract

1. Several lines of evidence suggest that the I7-I10 muscle group contributes to the radula opening phase of behavior in Aplysia; 1) extracellular stimulation of these muscles in reduced preparations causes the halves of the radula to separate, 2) synaptic activity can be recorded from muscles I7-I10 in intact animals when the radula is opening, and 3) motor neurons innervating I7-I10 are activated out of phase with retractor/closer motor neurons during cycles of buccal activity driven by the cerebral-to-buccal interneuron 2 (CBI-2). 2. All of the opener muscles are innervated by the B48 neurons, a bilaterally symmetrical pair of cholinergic motor neurons. B48 neurons produce excitatory junction potentials (EJPs) in opener muscle fibers that summate to produce muscle contractions. Contraction size is determined by the size of depolarization in muscle fibers and/or by action potentials that are triggered by summation of B48-evoked EJPs. 3. In addition to input from B48 neurons, opener muscles also receive excitatory input from the cholinergic multiaction neurons B4/B5. EJPs evoked by stimulation of neurons B4/B5 are 1/10 the size of B48-evoked EJPs. Consequently, changes in muscle tension produced by B4/B5 activity are relatively small. In contrast to B48 neurons, neurons B4/B5 are likely to be active during the closing/retraction phase of behavior. During cycles of buccal activity driven by neuron CBI-2, neurons B4/B5 fire in phase with closer/retractor motor neurons. Thus opener muscles may develop a modest amount of tension during the closing/retraction phase of behavior as a result of synaptic input from neurons B4/B5. 4. Opener muscles may also develop tension during closing/retraction simply by virtue of the fact that they have been stretched. When isolated opener muscles are lengthened, depolarizations are recorded from individual muscle fibers, and muscle tension increases. With sufficient changes in fiber length, action potentials are elicited. These action potentials produce twitchlike muscle contractions that become rhythmic with maintained stretch. Stretch-activated depolarizations are generally first apparent when muscle length is increased by 1 mm. Length changes of 4-5 mm are generally necessary to elicit twitchlike muscle contractions. Changes of 1-2 mm in muscle length are observed when the opener muscle's antagonist, the accessory radula closer, is activated in reduced preparations. 5. Stretch may also modulate B48-induced contractions of the opener muscles. When muscle length is increased, B48-elicited contractions of the I7 muscle are larger. These increases in contraction amplitude are accompanied by decreases in contraction latency. 6. We conclude that muscles I7-I10 contract vigorously in response to strong excitatory input from neuron B48 and contribute to radula opening. Stretch may potentiate this activity. Thus, if radula closer muscles contract vigorously and pull on the opener muscles, the opener muscles will respond by contracting more vigorously themselves. This may be a mechanism fo...

Motor neuronal activity varies least among individuals when it matters most for behavior

“…In particular, it might be useful to include the activity of the motor neurons for the intrinsic muscles of the odontophore such as B15/B16, the motor neurons for the accessory radular closer (ARC) muscle [Cohen et al 1978; the ARC muscle is also known as I5 (Howells 1942)], or B48, the motor neuron for the I7-I10 muscles, which contribute to opening of the radula (Evans et al 1996). Although we were unable to distinguish these motor neurons on BN3, in future studies it might be possible to combine the suspended buccal mass preparation (McManus et al 2012) with voltage-sensitive dyes (Hill et al 2010;Morton et al 1991) to obtain a more complete picture of the full activity of all the motor neurons during feeding.…”

Neuromechanics of Coordination during Swallowing inAplysia californica

“…Opening is mediated by the I7 muscles, which are controlled by motor neuron B48 [I7 is not shown in Fig. 1C because it is internal to the odontophore (see Evans et al, 1996)]. Closing is mediated primarily by the I4 muscles, which are controlled by the B8 motor neurons (Morton and Chiel, 1993b;Church and Lloyd, 1994).…”

“…The feeding apparatus of the animal is a grasping device that the animal uses to manipulate and ingest food (Kupfermann, 1974). Activity of individual nerve cells that control the grasper during feeding has been monitored in intact animals (Warman and Chiel, 1995), movements of the feeding musculature have been visualized in intact animals (Neustadter et al, 2002), and semi-intact preparations have been used to explore the effects of motor neuronal activity on grasper biomechanics (Weiss et al, 1986;Cropper et al, 1990;Morton and Chiel 1993b;Evans et al, 1996;Orekhova et al, 2001).…”

The kinematics of multifunctionality: comparisons of biting and swallowing inAplysia californica

“…The circumferential muscle shown in C2 was designated as such by Starmühlner (Starmühlner, 1956). The nomenclature for the other intrinsic muscles (I1 through I10) follows Howells (Howells, 1942) and Evans et al (Evans et al, 1996), and the nomenclature for the extrinsic muscles (E1-E3 and E6) follows Chiel et al and Howells (Howells, 1942). Compare with fig.·21 of Neustadter et al (Neustadter et al, 2002b).…”

“…Extracellular recordings from I5 (ARC) were taken from Cropper et al (Cropper et al, 1990b), and were aligned with BN3 activity (which carries the axons of the B15/B16 motor neurons). Recordings from I10 (which are representative of activity in 17, I8, I9 and I10) were taken from Evans et al (Evans et al, 1996). The lengths of the scanned recordings were scaled relative to one another using the duration of the opening of the jaws to the closing of the jaws during a bite, and aligned by peak protraction.…”