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

Abstract

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.

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

“…Previous studies in this system have demonstrated that the durations of spike trains from identified motor neurons Chiel 1993a, 1993b), and durations of EMG from the I2 muscle (reflecting the activity of the B31/B32 and B61/B62 motor neurons; Hurwitz et al 1996), can be related to behavior. The times that were measured are indicated in Fig.…”

“…Previous studies have demonstrated that all critical motor neuronal elements for controlling the feeding apparatus (the buccal mass) can be monitored by recording directly from 1) the protractor muscle (I2), whose activation is an obligatory first step for effective feeding movements and whose EMG patterns represent the activity of interneurons/motor neurons B31/B32 and motor neurons B61/B62 (Hurwitz et al 1996); 2) the radular nerve (RN), which contains axons of the motor neurons B8a/B8b controlling closure of the grasper Chiel 1993a, 1993b); 3) buccal nerve 2 (BN2), which contains axons of the motor neurons controlling the jaw musculature, B10, B6, B9, B3, B38, and B43 (Church and Lloyd 1994;Lu et al 2013;Morton and Chiel 1993b); and 4) buccal nerve 3 (BN3), which contains axons of motor neurons controlling some of the intrinsic muscles of the grasper (e.g., B15/B16; Church and Lloyd 1994;Cohen et al 1978) and a multiaction neuron, B4/B5 (Church and Lloyd 1994;Warman and Chiel 1995;Ye et al 2006b). Nerves RN, BN2, and BN3 are referred to as n1, n5, and n4 in Scott et al (1991).…”

“…1, and the criteria used to define the starts and ends of bursts are listed in Table 1. To characterize the key motor features, we determined the start and stop times of the I2 EMG during the protraction phase by measuring both the time of the first spike and the time at which the muscle EMG reached 10 Hz and the stop time when it fell below 5 Hz (Hurwitz et al 1996; 3 measures), the start and stop times of the largest units on RN (corresponding to activity in the B8a/b neurons; Chiel 1993a, 1993b; 2 measures), the start and stop times of the B4/B5 units on BN3 [largest units on BN3 (Warman and Chiel 1995) from the first to the last spike; 2 measures], and the start and stop times of identified motor neurons B6/B9 and B43 (Lu et al 2013;4 measures). Finally, we measured the third-largest units on BN2 (Church and Lloyd 1994;Morton and Chiel 1993b;Ye et al 2006a), focusing on when they began in retraction (1 measure), for a total of 12 different measures of the motor program.…”

“…To characterize motor programs as completely as possible, the activity of many of the key identified motor neurons for feeding behavior were quantified from in vivo bites (A) and swallows (B), in which all of the essential motor outputs of the feeding system were simultaneously recorded. In each recording, the top channel shows EMG recorded from I2, the protractor muscle (Hurwitz et al 1996). The 2nd channel shows ENG recorded from the radular nerve (RN; large units: activity in neurons B8a/b, grasper closers).…”

Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

“…Single twophase cycles of motor programs consisting of protraction and retraction phases were induced every 2 min by stimulating CBI-2 at 8 -10 Hz with 10 msec current pulses. Electrical activity in nerve I2 was used to monitor protraction because this nerve contains axons of protraction phase motor neurons B31/32 and B61/62 (Hurwitz et al, 1996). Sustained depolarization in B4/5 was used to monitor retraction (Church and Lloyd, 1994;Jing and Weiss, 2001).…”