Changes of Internal State Are Expressed in Coherent Shifts of Neuromuscular Activity in Aplysia Feeding Behavior

Motivated behaviors comprise appetitive actions whose occurrence results partly from an internally driven incentive to act. Such impulsive behavior can also be regulated by external rewarding stimuli that, through learning processes, can lead to accelerated and seemingly automatic, compulsive-like recurrences of the rewarded act. Here, we explored such behavioral plasticity in Aplysia by analyzing how appetitive reward stimulation in a form of operant conditioning can modify a goal-directed component of the animal's food-seeking behavior. In naive animals, protraction/retraction cycles of the tongue-like radula are expressed sporadically with highly variable interbite intervals. In contrast, animals that were previously given a food-reward stimulus in association with each spontaneous radula bite now expressed movement cycles with an elevated frequency and a stereotyped rhythmic organization. This rate increase and regularization, which was retained for several hours after training, depended on both the reward quality and its contingency because accelerated, stereotyped biting was not induced in animals that had previously received a less-palatable food stimulus or had been subjected to nonassociative reward stimulation. Neuronal correlates of these learning-induced changes were also expressed in the radula motor pattern-generating circuitry of isolated buccal ganglia. In such in vitro preparations, moreover, manipulation of the burst frequency of the bilateral motor pattern-initiating B63 interneurons indicated that the regularization of radula motor pattern generation in contingently trained animals occurred separately from an increase in cycle rate, thereby suggesting independent processes of network plasticity. These data therefore suggest that operant conditioning can induce compulsive-like actions in Aplysia feeding behavior and provide a substrate for a cellular analysis of the underlying mechanisms.

Section: Operant Conditioning and Induction Of Compulsive-like Feedinmentioning

confidence: 64%

Behavioral andIn VitroCorrelates of Compulsive-Like Food Seeking Induced by Operant Conditioning inAplysia

Nargeot¹,

Petrissans²,

Simmers³

2007

“…Repetitive 30-s-ISI (see Materials and Methods) stimulation of CBI-2 promotes the generation of ingestive motor programs, whereas stimulation of EN promotes the generation of egestive motor programs. Notably, in semi-intact preparations, the two CPG inputs CBI-2 and EN, respectively, elicit ingestive and egestive behaviors (Chiel et al, 1988;Jing and Weiss, 2005;Zhurov et al, 2005).…”

Section: B64 Hyperpolarization In Ingestive Versus Egestive Programsmentioning

confidence: 99%

“…If this is the case, it should be possible to experimentally change positive latencies into negative ones, and vice versa, by altering the state of the network. Previous work showed that previous history of network activity produces lasting changes in the state of the system (Proekt et al, , 2007Brezina et al, 2005;Zhurov et al, 2005). We used previously described experimental paradigms (Proekt et al, , 2007 to manipulate the state of the network and characterized the resulting changes in B64 latency.…”

Section: Dynamic Change Of B64 Latency During Program Buildup and Biamentioning

confidence: 99%

State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network

Due²,

Sasaki³

et al. 2007

When sustained firing of a neuron is similar in different types of motor programs, its role in the generation of these programs is often similar. We investigated whether this is also the case for neurons involved in phase transition. In the Aplysia feeding central pattern generator (CPG), identified interneuron B64 starts firing at the transition between the protraction and the retraction phases of all types of motor programs, and its firing is sustained during the retraction phase. It was thought that B64 functions as a protraction terminator as it provides strong inhibitory input to protraction interneurons and motoneurons. Furthermore, premature activation of B64 can lead to premature termination of the protraction phase. Indeed, as we show here, B64 can terminate the protraction phase regardless of the type of motor program. However, B64 actually only functions as a protraction terminator in ingestive-like but not in egestive-like programs. This differential role of B64 results from a differential timing of the initiation of B64 spiking in the two types of programs. In turn, this differential timing of the initiation of B64 firing is determined by the internal state of the CPG. Thus, this study indicates the importance of the timing of initiation of firing in determining the functional role of a neuron and demonstrates that this role depends on the activity-dependent state of the network.

“…B65 actions suggest that inputrepresenting neurons that are themselves elements of the CPG may play a role similar to that attributed to higher-order neurons. In addition, because B65 activity may be further regulated by other inputs, the mechanisms described in here may support additional forms of network and behavior flexibility Lum et al, 2005;Proekt et al, 2005;Zhurov et al, 2005;Jing et al, 2007).…”

Section: Discussionmentioning

confidence: 87%

An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network

Sasaki¹,

Jing²,

Due³

et al. 2008

Despite the importance of spike-timing regulation in network functioning, little is known about this regulation at the cellular level. In the Aplysia feeding network, we show that interneuron B65 regulates the timing of the spike initiation of phase-switch neurons B64 and cerebral-buccal interneuron-5/6 (CBI-5/6), and thereby determines the identity of the neuron that acts as a protraction terminator. Previous work showed that B64 begins to fire before the end of protraction phase and terminates protraction in CBI-2-elicited ingestive, but not in CBI-2-elicited egestive programs, thus indicating that the spike timing and phase-switching function of B64 depend on the type of the central pattern generator (CPG)-elicited response rather than on the input used to activate the CPG. Here, we find that CBI-5/6 is a protraction terminator in egestive programs elicited by the esophageal nerve (EN), but not by CBI-2, thus indicating that, in contrast to B64, the spike timing and protraction-terminating function of CBI-5/6 depends on the input to the CPG rather than the response type. Interestingly, B65 activity also depends on the input in that B65 is highly active in EN-elicited programs, but not in CBI-2-elicited programs independent of whether the programs are ingestive or egestive. Notably, during EN-elicited egestive programs, hyperpolarization of B65 delays the onset of CBI-5/6 firing, whereas in CBI-2-elicited ingestive programs, B65 stimulation simultaneously advances CBI-5/6 firing and delays B64 firing, thereby substituting CBI-5/6 for B64 as the protraction terminator. Thus, we identified a neural mechanism that, in an input-dependent manner, regulates spike timing and thereby the functional role of specific neurons.