The neural correlates of implicit and explicit sequence learning: Interacting networks revealed by the process dissociation procedure.

In two H2(15)O PET scan experiments, we investigated the cerebral correlates of explicit and implicit knowledge in a serial reaction time (SRT) task. To do so, we used a novel application of the Process Dissociation Procedure, a behavioral paradigm that makes it possible to separately assess conscious and unconscious contributions to performance during a subsequent sequence generation task. To manipulate the extent to which the repeating sequential pattern was learned explicitly, we varied the pace of the choice reaction time task-a variable that is known to have differential effects on the extent to which sensitivity to sequence structure involves implicit or explicit knowledge. Results showed that activity in the striatum subtends the implicit component of performance during recollection of a learned sequence, whereas the anterior cingulate/mesial prefrontal cortex (ACC/MPFC) supports the explicit component. Most importantly, we found that the ACC/MPFC exerts control on the activity of the striatum during retrieval of the sequence after explicit learning, whereas the activity of these regions is uncoupled when learning had been essentially implicit. These data suggest that implicit learning processes can be successfully controlled by conscious knowledge when learning is essentially explicit. They also supply further evidence for a partial dissociation between the neural substrates supporting conscious and nonconscious components of performance during recollection of a learned sequence.

[1]  David G. Lavond,et al.  Trace conditioning: Abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations , 1985, Brain Research.

[2]  M. Erdelyi,et al.  Experimental indeterminacies in the dissociation paradigm of subliminal perception , 1986, Behavioral and Brain Sciences.

[3]  E. Reingold,et al.  Using direct and indirect measures to study perception without awareness , 1988, Perception & psychophysics.

[4]  Daniel B. Willingham,et al.  On the development of procedural knowledge. , 1989, Journal of experimental psychology. Learning, memory, and cognition.

[5]  L. Jacoby A process dissociation framework: Separating automatic from intentional uses of memory , 1991 .

[6]  Eyal M. Reingold,et al.  Comparing Direct (Explicit) and Indirect (Implicit) Measures to Study Unconscious Memory , 1991 .

[7]  M. Amorim,et al.  Conscious knowledge and changes in performance in sequence learning: evidence against dissociation. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[8]  David R. Shanks,et al.  A critical examination of the evidence for unconscious (implicit) learning , 1994 .

[9]  Peder J. Johnson,et al.  Assessing implicit learning with indirect tests: Determining what is learned about sequence structure. , 1994 .

[10]  R. F. Thompson,et al.  Organization of memory traces in the mammalian brain. , 1994, Annual review of neuroscience.

[11]  S. Kosslyn,et al.  A PET investigation of implicit and explicit sequence learning , 1995 .

[12]  Scott T. Grafton,et al.  Functional Mapping of Sequence Learning in Normal Humans , 1995, Journal of Cognitive Neuroscience.

[13]  Axel Cleeremans,et al.  Comparing direct and indirect measures of sequence learning , 1996 .

[14]  John M. Gardiner,et al.  Memory: Task dissociations, process dissociations and dissociations of consciousness , 1996 .

[15]  M. Stadler Distinguishing implicit and explicit learning , 1997 .

[16]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[17]  Thomas Goschke,et al.  Implicit learning and unconscious knowledge: Mental representation, computational mechanisms, and brain structures. , 1997 .

[18]  Daniel B. Willingham,et al.  Response-to-stimulus interval does not affect implicit motor sequence learning, but does affect performance , 1997, Memory & cognition.

[19]  S. Rauch,et al.  Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging , 1997, Human brain mapping.

[20]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[21]  Scott T. Grafton,et al.  Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. , 1997, Brain : a journal of neurology.

[22]  A. Graybiel The Basal Ganglia and Chunking of Action Repertoires , 1998, Neurobiology of Learning and Memory.

[23]  Benjamin A Clegg,et al.  Sequence learning , 1998, Trends in Cognitive Sciences.

[24]  M. Hallett,et al.  Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study. , 1998, Brain : a journal of neurology.

[25]  R. Clark,et al.  Classical conditioning and brain systems: the role of awareness. , 1998, Science.

[26]  Axel Cleeremans,et al.  Implicit learning: news from the front , 1998, Trends in Cognitive Sciences.

[27]  Christian Lebiere,et al.  Implicit and explicit learning in a hybrid architecture of cognition , 1999, Behavioral and Brain Sciences.

[28]  D R Shanks,et al.  Evaluating the relationship between explicit and implicit knowledge in a sequential reaction time task. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[29]  Daniel B. Willingham,et al.  The Relation Between Implicit and Explicit Learning: Evidence for Parallel Development , 1999 .

[30]  Axel Cleeremans,et al.  Striatum forever, despite sequence learning variability: A random effect analysis of PET data , 2000, Human brain mapping.

[31]  Axel Cleeremans,et al.  Can sequence learning be implicit? New evidence with the process dissociation procedure , 2001, Psychonomic bulletin & review.

[32]  Patrick Rabbitt,et al.  Consciousness is slower than you think , 2002, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[33]  J. Gabrieli,et al.  Direct comparison of neural systems mediating conscious and unconscious skill learning. , 2002, Journal of neurophysiology.

[34]  J. Churchwell,et al.  Medial prefrontal cortex and pavlovian conditioning: trace versus delay conditioning. , 2002, Behavioral neuroscience.

[35]  J. Steinmetz,et al.  Eyeblink Classical Conditioning: Volume 2 , 2002 .

[36]  Steven Laureys,et al.  Cerebral correlates of explicit sequence learning. , 2003, Brain research. Cognitive brain research.

[37]  Katsunori Kitano,et al.  Time representing cortical activities: two models inspired by prefrontal persistent activity , 2003, Biological Cybernetics.

[38]  S. Keele,et al.  The cognitive and neural architecture of sequence representation. , 2003, Psychological review.

[39]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[40]  L. Jiménez Attention and implicit learning , 2003 .

[41]  P. Dash,et al.  A Role for Prefrontal Cortex in Memory Storage for Trace Fear Conditioning , 2004, The Journal of Neuroscience.

[42]  Leonora Wilkinson,et al.  Intentional control and implicit sequence learning. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

[43]  C. Carter,et al.  Regional brain activation during concurrent implicit and explicit sequence learning. , 2004, Cerebral cortex.