Dissociable neural mechanisms underlying response-based and familiarity-based conflict in working memory

Cognitive control requires the resolution of interference among competing and potentially conflicting representations. Such conflict can emerge at different points between stimulus input and response generation, with the net effect being that of compromising performance. The goal of this article was to dissociate the neural mechanisms underlying different sources of conflict to elucidate the architecture of the neural systems that implement cognitive control. By using functional magnetic resonance imaging and a verbal working memory task (item recognition), we examined brain activity related to two kinds of conflict with comparable behavioral consequences. In a trial of our item-recognition task, participants saw four letters, followed by a retention interval, and a probe letter that did or did not match one of the letters held in working memory (positive probe and negative probe, respectively). On some trials, conflict arose solely because of the current negative probe having a high familiarity, due to its membership in the immediately preceding trial's target set. On other trials, additional conflict arose because of the current negative probe having also been a positive probe on the immediately preceding trial, producing response-level conflict. Consistent with previous work, conflict due to high familiarity was associated with left prefrontal activation, but not with anterior cingulate activation. The response-conflict condition, when compared with high-familiarity conflict trials, was associated with anterior cingulate cortex activation, but with no additional left prefrontal activation. This double dissociation points to differing contributions of specific cortical areas to cognitive control, which are based on the source of conflict.

[1]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[2]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Karl J. Friston,et al.  Distribution of cortical neural networks involved in word comprehension and word retrieval. , 1991, Brain : a journal of neurology.

[4]  Alan V. Oppenheim,et al.  Discrete-time Signal Processing. Vol.2 , 2001 .

[5]  Debra A. Fleischman,et al.  Double Dissociation Between Memory Systems Underlying Explicit and Implicit Memory in the Human Brain , 1995 .

[6]  C Andrew,et al.  Motor response suppression and the prepotent tendency to respond: a parametric fMRI study , 2000, Neuropsychologia.

[7]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[8]  S. Monsell Recency, immediate recognition memory, and reaction time , 1978, Cognitive Psychology.

[9]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[10]  D. McLachlan The frontal lobes. , 1951, The New Zealand medical journal.

[11]  Jonathan D. Cohen,et al.  A Developmental Functional MRI Study of Prefrontal Activation during Performance of a Go-No-Go Task , 1997, Journal of Cognitive Neuroscience.

[12]  K. Kiehl,et al.  Error processing and the rostral anterior cingulate: an event-related fMRI study. , 2000, Psychophysiology.

[13]  Robert A. Koeppe,et al.  Age Differences in Behavior and PET Activation Reveal Differences in Interference Resolution in Verbal Working Memory , 2000, Journal of Cognitive Neuroscience.

[14]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. Kawashima,et al.  Functional anatomy of GO/NO-GO discrimination and response selection : a PET study in man , 1996 .

[16]  Leslie G. Ungerleider,et al.  Discrete Cortical Regions Associated with Knowledge of Color and Knowledge of Action , 1995, Science.

[17]  J. Jonides,et al.  Inhibition in verbal working memory revealed by brain activation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Stuss,et al.  The Frontal Lobes , 1986 .

[19]  N. Cohen,et al.  The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. , 2001, Brain research. Cognitive brain research.

[20]  Y. Miyashita,et al.  No‐go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging , 1998, The European journal of neuroscience.

[21]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

[23]  Jin Fan,et al.  Cognitive and Brain Consequences of Conflict , 2003, NeuroImage.

[24]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[25]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[27]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[28]  M. Coles,et al.  "Where did I go wrong?" A psychophysiological analysis of error detection. , 1995, Journal of experimental psychology. Human perception and performance.