Elsevier

NeuroImage

Volume 28, Issue 4, December 2005, Pages 1007-1013
NeuroImage

Neural dynamics of error processing in medial frontal cortex

https://doi.org/10.1016/j.neuroimage.2005.06.041Get rights and content

Abstract

Adaptive behavior requires an organism to evaluate the outcome of its actions, such that future behavior can be adjusted accordingly and the appropriate response selected. During associative learning, the time at which such evaluative information is available changes as learning progresses, from the delivery of performance feedback early in learning to the execution of the response itself during learned performance. Here, we report a learning-dependent shift in the timing of activation in the rostral cingulate zone of the anterior cingulate cortex from external error feedback to internal error detection. This pattern of activity is seen only in the anterior cingulate, not in the pre-supplementary motor area. The dynamics of these reciprocal changes are consistent with the claim that the rostral cingulate zone is involved in response selection on the basis of the expected outcome of an action. Specifically, these data illustrate how the anterior cingulate receives evaluative information, indicating that an action has not produced the desired result.

Introduction

To survive in changing environments, an organism must be able to adapt its behavior to the situation at hand. This flexibility can be achieved by evaluating response outcomes and adjusting behavior accordingly (Dickinson, 1985). In this regard, error signals provide important evaluative information, since they indicate that a behavior was inadequate given the current context and that, in future, a different response needs to be selected (Holroyd and Coles, 2002).

Existing data on the neural substrates of action selection indicate that the medial frontal cortex plays a crucial role in selecting actions on the basis of their outcomes (Matsumoto and Tanaka, 2004) and subsequent monitoring of response outcomes (Holroyd et al., 2004a, Ridderinkhof et al., 2004). Rather than attributing a single role to this vast cortical expanse, recent studies have started to associate different functions to the different anatomical structures that lay within the medial frontal cortex (Picard and Strick, 2001, Rushworth et al., 2004). In this context, an anterior portion of the cingulate cortex, the rostral cingulate zone anterior (RCZa), has been specifically associated with processing of error information and selecting appropriate behavioral adjustments (Holroyd and Coles, 2002, Rushworth et al., 2004, Fiehler et al., 2004).

These inferences on the neural bases of error processing have been obtained in the context of a “static” experimental environment, in which the organism knows the behavior that is appropriate for the current situation. Thus, a given response can be evaluated immediately against an internal representation of the correct stimulus–response relationship. Should the response be incorrect, error information is available from an internal error-detection process at the time of the response (Gehring et al., 1993, Holroyd et al., 2005). However, in a novel environment, with as yet unknown stimulus–response associations, error information is not available until the delivery of external performance feedback. This implies that, during the learning of stimulus–response associations by trial and error, the time at which error information is available will change. Prior to learning, error information will not be available until external performance feedback is delivered, but after learning, error information will be available earlier from internal sources at the time of the response itself. Thus, a neural structure that adjusts behavior as a function of the evaluation of response outcomes should dynamically shift its responsivity as a function of learning, from external sources provided by error feedback to internal sources associated with the error response itself. We predicted that, following error feedback, activity in the anterior cingulate cortex would decrease as learning proceeds; conversely, following an erroneous response, activity in the anterior cingulate would increase as learning proceeds. These predictions can be derived from a neuro-computational model (Holroyd and Coles, 2002) that formally describes the relationship between neural systems involved in outcome evaluation with those involved in action selection.

To test these predictions, we asked human subjects to learn arbitrary visuomotor mappings (Wise and Murray, 2000, Toni et al., 2001), using performance feedback, while measuring their cerebral activity using functional magnetic resonance imaging (fMRI). Participants were presented with line drawings, each of which was associated with pressing one of four response buttons (Fig. 1). We manipulated the degree of learning achieved during the scanning session by varying the number of times a given visuomotor mapping was presented. For one condition (High Learning, HL), four distinct visuomotor mappings were presented 36 times each over the course of the scanning session, enabling the subject to fully learn the visuomotor associations. For a control condition (Low Learning, LL), 24 different mappings were presented 6 times each. A reaction time (RT) deadline ensured that participants made errors, even during learned performance. Crucially, by varying the delay between response and feedback, and by introducing neutral feedback on some of the trials, we were able to dissociate the hemodynamic responses elicited by response and feedback (see Experimental timing).

Section snippets

Subjects

We studied eight right-handed male volunteers (mean age = 30.4 years, SD = 13.4) with normal or corrected-to-normal vision after obtaining informed consent according to institutional guidelines of the local ethics committee (CMO region Arnhem-Nijmegen, Netherlands). They were paid €10 per hour for their participation. Imaging data from 5 additional subjects were discarded, since these subjects either failed to learn the appropriate stimulus–response mappings adequately (2 subjects, less than

Behavioral data

Behavioral data indicated that our design was successful in manipulating the degree of learning achieved by the participants during the scanning session. Participants learned the stimulus–response mappings at a faster rate in the High Learning condition than in the Low Learning condition (Condition × Time interaction on Error Rate: F(7,49) = 3.2, P = 0.035, Fig. 3a). Although participants never reached error-free performance during the scanning session in either condition (because of the RT

Discussion

The present data indicate that, over the course of learning a set of arbitrary visuomotor mappings, a region along the cingulate sulcus (RCZa) shifts its responsiveness to different sources of error information as a function of learning. Error feedback-related activation decreases as learning proceeds, while error response-related activation increases, and these effects are reciprocal (Fig. 4). These results show not only that the anterior cingulate cortex responds to both internal (Carter et

Acknowledgments

The authors would like to thank Paul Gaalman for excellent technical assistance and Peter Hagoort, Karl Magnus Petersson, and Guillen Fernandez for helpful comments on an earlier draft of the manuscript. C.B.H. was supported by National Institute of Mental Health (NIMH) postdoctoral fellowship MH63550. S.N. was supported by the Netherlands Organization for Scientific Research (NWO).

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