Removal of Default State-Associated Inhibition during Repetition Priming Improves Response Articulation

Abstract

Behavior is a product of both the stimuli encountered and the current internal state. At the level of the nervous system, the internal state alters the biophysical properties of, and connections between, neurons establishing a “network state”. To establish a network state, the nervous system must be altered from an initial default/resting state, but what remains unclear is the extent to which this process represents induction from a passive default state or the removal of suppression by an active default state. We use repetition priming (a history-dependent improvement of behavioral responses to repeatedly encountered stimuli) to determine the cellular mechanisms underlying the transition from the default to the primed network state. We demonstrate that both removal of active suppression and induction of neuron excitability changes each contribute separately to the production of a primed state. The feeding system of Aplysia californica displays repetition priming via an increase in the activity of the radula closure neuron B8, which results in increased bite strength with each motor program. We found that during priming, B8 received progressively less inhibitory input from the multi-functional neurons B4/5. Additionally, priming enhanced the excitability of B8, but the rate at which B8 activity increased as a result of these changes was regulated by the progressive removal of inhibitory input. Thus, the establishment of the network state involves the induction of processes from a rested state, yet the consequences of these processes are conditional upon critical gating mechanisms actively enforced by the default state.

Latent Modulation: A Basis for Non-Disruptive Promotion of Two Incompatible Behaviors by a Single Network State

“…3 B ; t =1.716; df=5; p =0.1468; n =6). However, as reported previously (Dacks et al, 2012), CBI-2 stimulation in HiDi did increase B8 excitability ( t = 12.31; df = 5; p < 0.001; n =6), indicating that in these preparations CBI-2 was capable of modulating neuronal excitability. The decrease in B4/5 excitability was likely due to their activity during motor programs as we found that B4/5 excitability decreased after repeated EN programs (Fig.…”

“…CBI-2 priming increases B8 excitability (Dacks et al, 2012) which could serve as an additional contributing factor to the increased B8 protraction firing rate in EN programs. Consistent with this, the number of spikes elicited from B8 during 10 s of 5 Hz B65 spiking increased post-CBI-2 priming (Fig.…”

“…When motor programs are triggered by the command neuron CBI-2, subsequent responses to CBI-2 stimulation become increasingly ingestive (Proekt et al, 2004; Friedman and Weiss, 2010; Dacks et al, 2012). However, subsequent responses to esophageal nerve (EN) stimulation, which signals inedible food stimuli, become increasingly egestive (Proekt et al, 2008).…”

An Activation Threshold Model for Response Inhibition

“…An assumption is that a response is not initiated until facilitatory inputs to the alpha motoneuron pool exceed inhibitory levels. In the lead up to a response, impulse control mechanisms [20–22] keep the motoneurons below threshold until a movement is appropriate. This framework is consistent with models of saccades whereby the growth of activity in neurons predicts saccade initiation time [23].…”

Consequences of degeneracy in network function

“…For egestion they are closed during protraction and open during retraction. However, when a single cycle of a motor program is triggered in a rested preparation neither ingestion, nor egestion is observed [42–46]. Instead motor programs are not well articulated, and are referred to as having ‘intermediate’ characteristics.…”