Effect anticipation modulates deviance processing in the brain

Abstract

Humans constantly perform actions to achieve desired goals in the environment. However, only very little is known about how actions influence stimulus processing. The present study addresses the question as to how performing an action that is associated with a particular auditory effect influences deviance processing in the brain. In the first part of the experiment, subjects performed left and right keypresses that were always followed by one of two tones, establishing an association between the particular action and the perceptual code of the effect tone. In the second part subjects were required to perform random series of left and right keypresses. The action triggered randomly one of the experimental stimuli of a typical oddball task (i.e., most of the time a standard tone and, rarely, a perceptually deviant tone). Deviant and standard stimuli were the same tones used as effect tones in the first phase of the experiment. Deviant stimuli elicited a larger P3a when the action that triggered stimulus presentation was associated with the standard tone than when it was associated with the deviant tone. This indicates a larger orienting response in the former case. The findings suggest that the context to which incoming sensory information is compared in order to detect deviant stimuli is codetermined by the sensory effects humans anticipate their actions to have.

Introduction

People are almost constantly exposed to a multitude of external stimuli. Since the brain cannot analyse all of the incoming information to the same extent, humans select the most important aspects of their environment for in-depth processing. Yet, humans are not in danger to miss important or potentially perilous events in the surroundings, because novel or salient stimuli elicit an orienting response, i.e., an involuntary shift of attention to the new or unexpected stimulus (e.g., Sokolov, 1963). For example, when driving a car people might well attend to the radio but a sudden change in the background noise nonetheless triggers an orienting response towards the potential danger.

Hence, humans distinguish between events that are novel or unexpected and events that have already been experienced or were to be expected. Evidently, whether or not a stimulus is considered novel or unexpected depends heavily upon the context in which it is embedded. In most experimental paradigms investigating the orienting response, the subject takes the role of a passive observer who is presented with a series of stimuli, some of which are deviant with respect to the stimulus context. However, humans are hardly ever mere passive observers. Rather, they act on their surroundings in order to achieve desired goals and the stimulus context is strongly modulated by their actions.

The ideomotor theory addresses this kind of “intention-based” action that is meant to produce some internally pre-specified effect (see for example Prinz, 1997). The ideomotor approach claims that performing an action leaves behind an association between the action's motor code and the sensory effects the action produces (“action-effect bindings”). These associations are bi-directional and can, therefore, be used to retrieve an action by “anticipating” its effects (e.g., Elsner and Hommel, 2001, Herwig et al., in press, Kunde, 2001). Actually, the common coding approach (e.g., Prinz, 1990, Prinz, 1997) assumes that perceived and to-be-produced events share a common representational medium. In this medium, both actions and perceptual events are represented in an abstract format. As a consequence, perceived events and actions destined to produce a sensory effect can interact with each other directly (for a review see Hommel et al., 2001).

From this point of view, humans need not only monitor the input for stimuli that are deviant with respect to the context of perceived stimuli, but also for unexpected action effects. If they do so, then the “context”, to which the effect stimulus is compared, is not only defined by the perceived stimuli of the stimulus context. It is also defined by the anticipated consequences of the agent's actions (which, according to the common coding principle, have the same representational format as perceived stimuli).

In the present study, we adopt an ideomotor/common-coding perspective to investigate the effect of intention-based action production (or rather effect production) on deviance processing in the brain. In one of the most prominent paradigms for the study of the orienting response, two classes of stimuli are presented, a frequently occurring stimulus that defines the context – the standard stimulus – and an infrequently occurring stimulus that is meant to elicit the orienting response – the deviant stimulus. There are several variants of this “oddball task”, differing primarily in the task the subjects are required to perform, e.g., whether they have to react to the oddballs, to count them silently, or to watch a silent movie and, thus, to ignore the stimuli (see, for example, Friedman et al., 2001).

The majority of studies have used the auditory modality, such that we know a lot about electrophysiological correlates of orienting to deviant auditory events (see Näätänen, 1990, Friedman et al., 2001). The earliest event-related potential (ERP) indicating the detection of a change in an otherwise invariant context of stimulus events is the mismatch negativity (MMN; see Alho, 1995, Näätänen, 1992). The MMN has a fronto-central topography and a latency of 120–250 ms post-stimulus. It is probably generated in and around the primary auditory cortex (Alho, 1995) and, as a secondary source, in the frontal cortex (e.g., Giard et al., 1990). It has been proposed that the frontal cortex receives input from the sensory-specific MMN generator indicating a potentially relevant event and calling for an involuntary orienting response.

If the stimulus is sufficiently deviant, the MMN gives rise to a P300. The P300 is considered to consist of two different components that are probably mutually related and may be elicited in tandem, the P3a and P3b (Courchesne et al., 1975, Friedman et al., 2001, Polich, 2003). The P3a has a fronto-central distribution and peaks at about 300 ms post-stimulus. It is elicited by contextually deviant or novel stimuli, and is considered to reflect the frontal lobe function related to orienting of attention (see Posner and Petersen, 1990). The P3b has a more posterior distribution and peaks later. It is elicited by infrequently occurring stimuli that are task-relevant, or involve a decision. It has been proposed that the P3b results from memory updating operations involving the hippocampal formation and the parietal cortex (e.g., Knight, 1996).

In the present study, we used the three-tone oddball paradigm, which elicits the P3a and P3b components relatively independently (Comerchero and Polich, 1999, Katayama and Polich, 1998). In this paradigm, subjects are presented with a series of stimuli of either of three classes, a high-probability stimulus – the standard – and two different low-probability stimuli – the target and the deviant. The subjects' task was to silently count the target stimuli. The perceptual difference between standard and target stimuli was small (1940 Hz vs. 2000 Hz), whereas the difference between standard and task-irrelevant deviant stimuli was large (1940 Hz vs. 500 Hz). The P300 to high-deviant (but task-irrelevant) stimuli consists mainly of the P3a component; whereas the P300 to task-relevant (but low-deviant) stimuli consists mainly of the P3b component (see Comerchero and Polich, 1999, Katayama and Polich, 1998).

Importantly, Nittono (2006) made subjects perform a three-tone oddball task in two conditions that already shed some light on the question as to whether action production affects deviance processing (see also Nittono and Ullsperger, 2000, Nittono et al., 2003). In the self condition, the stimuli were presented in response to subjects' voluntary key presses. In this condition, subjects were instructed to press a pre-specified key with the index finger not faster than once every 2 s. Each keypress triggered one of the three stimuli. In the auto condition, the stimuli were presented automatically at the same inter-stimulus intervals as those recorded in the preceding self condition. Nittono (2006) showed that the P3a elicited by high-deviant task-irrelevant stimuli were enhanced in the self condition compared to the auto condition. By contrast, the P3b to low-deviant task-relevant stimuli was the same in both conditions. This was also true for the MMN.

As Nittono (2006) pointed out, the enhanced P3a he observed in the self condition is not necessarily due to an effect of voluntary effect production. Rather, it might be that voluntary effect production merely serves to increase the allocation of attention to the oddball task. However, Nittono also points out that the results may indicate (but not prove beyond doubt) that the neural context to which a stimulus is compared is partially defined by the anticipated effect of the action that triggers the stimulus. According to the ideomotor principle, the perceptual representation of a forthcoming action effect is activated when people intend to produce it by voluntary action. It has been shown that when people frequently experience a perceptual event after a particular action a bidirectional link between action and effect is formed through associative learning mechanisms (Elsner and Hommel, 2001, Elsner and Hommel, 2004, Herwig et al., in press). It is plausible to assume that an action is associated to the stimulus event that the subject most often experiences after the execution of the action and that the action, therefore, at some point activates the representation of that stimulus. If so, the action subjects performed in the self condition of Nittono's (2006) experiment would have activated the representation of the high-probability standard stimulus. This anticipatory activation of the standard stimulus, in turn, would have made a deviant stimulus more salient, resulting in a larger orienting response and, therefore, an enhanced P3a.

The present study addresses the question as to how performing an action associated to a particular auditory effect affects deviance processing in the brain as reflected by P3a and MMN. Our experiment comprised two phases. First, subjects undergo an acquisition phase, in which subjects performed self-selected keypresses that were always followed by a certain tone (e.g. left keypress → high pitch tone [1940 Hz, later used as the standard stimulus]; right keypress → low pitch tone [500 Hz, later used as the deviant stimulus]). This acquisition phase was meant to establish an association between the particular action code and the perceptual code of the effect stimulus, as demonstrated for example by Elsner and Hommel, 2001, Elsner and Hommel, 2004 and Herwig et al. (in press). In the second phase, subjects performed a three-tone oddball task, as described above. Importantly, in our paradigm, stimulus presentation was triggered by the subjects' voluntary keypresses. As in the first phase, subjects were required on each trial to choose between a left and a right keypress. The action triggered randomly one of the three types of stimulus. The standard stimulus (1940 Hz) was presented with a probability of .75, target (2000 Hz) and deviant (500 Hz) stimuli were presented with a probability of .125 each. Subjects were required to silently count the target stimuli. Fig. 1 illustrates the experiment.

Importantly, depending on the action performed on the given trial, the subject anticipated either the standard or the deviant stimulus. Depending on the stimulus that was actually presented, the subject's anticipation could or could not be fulfilled. Our reasoning is the following. According to the common coding approach, effect anticipations are represented in the same domain as perceived stimuli. As a consequence, the anticipation of an action effect constitutes one component of the neural context incoming stimulation is compared to, just as the perceived stimuli that constitute the stimulus context. If the subject anticipates the standard stimulus, then the occurrence of a deviant stimulus should be all the more unexpected and, thus, elicit a larger orienting response. Likewise, if the subject anticipates the deviant stimulus, then the occurrence of a deviant stimulus should be less unexpected. As a consequence, ERPs indicating deviance processing in the brain should be larger in the former case than in the latter. To be precise, on the basis of the findings from Nittono (2006) we expected to find an increased P3a for deviant stimuli when the “anticipated” action outcome is the standard stimulus than when the anticipated action outcome is the deviant stimulus. By contrast, since Nittono failed to find a modulation of the MMN by voluntary action production in the experiment described above, we predicted that the MMN does not interact with the “anticipated” action outcome.

Notice that our paradigm does not confound effect anticipation and allocation of attention, since all stimuli in the oddball phase are triggered by voluntary keypresses.