Effects of different forms of engagement on the neuronal activity in the monkey's primary auditory cortex

Abstract

The effect of engagement on the neuronal activity in the primary auditory cortex (A1) has been previously shown. However, the experimental designs of previous studies did not consider possible combined influences of separate forms of engagement. We proposed three forms of engagement, including the presence of unconditioned stimuli that may change the meaning of a sound, the sense of agency (subjective awareness of control of one‟s own volitional action), and the level of effort. The aim of the present study was to identify how these forms of engagement influence the neuronal activity in A1. We first analyzed how the individual factors, such as the unconditioned stimuli alone or the acoustical stimuli alone, changed the activity in A1 in monkeys (Macaca fascicularis). We compared the effects of the individual factors with their pairing (the Pavlovian conditioning). The three passive conditions were presented to a group of monkeys that were previously trained to instrumental conditions (well-trained monkeys) and to a group without such training (low-trained monkeys). To separate the individual effects of engagement and to prevent the monkeys from learning to react to temporal cues, two types of the acoustical stimuli were used: “tone only” and “tone followed by noise”. We reported only the results of the comparisons in the case of “tone followed by noise”. To reveal the effects of the sense of agency and level of effort, we compared neuronal activity in A1 recorded while the well-trained monkeys performed three instrumental conditions and were presented one passive condition (the Pavlovian conditioning). Two of these four conditions required self-initiation of the acoustical stimuli with a grasp of a metal bar, whereas the other two conditions were initiated externally by a training computer. To reveal the effect of the level of effort, two of the four conditions required a high effort by requiring the detection of the pure tone, and the other two required a low effort, without such detection. The effects of sound meaning and of unconditioned stimuli were based on 75 and 97 units recorded during a presentation of the three passive conditions to the low- and well-trained monkeys, respectively. We found that the presence of the unconditioned stimuli led to slow modulations in the neuronal activity throughout the entire trial in both groups of monkeys. The fact that the slow modulations were present in both groups indicated that the changes were not related to the previous experience of the monkeys. The acoustical stimuli without meaning led to higher responses to the noise onset in the well-trained monkeys. The effects of agency and level of effort were based on 180 units recorded while the monkeys performed in the three instrumental conditions and were presented with one passive condition. We found that the slow modulations in the three instrumental conditions and the one passive condition were very similar. The neuronal activities differed only in short intervals within the time courses due to variations in the required movements in the conditions. The main effects of the sense of agency were a decrease in neuronal activity after the self-initiation and a smaller neuronal activity during the noise stimulation. The main effect of the level of effort was a higher neuronal activity after detection of the tone in the conditions requiring high effort. These results were consistent with and expanded upon previous studies showing that the neurons in A1 are sensitive to engagement. Moreover, we have shown that different forms of engagement have different effects on the neuronal activity in A1.