Contributions of the hippocampus and the striatum to simple association and frequency-based learning

Using fMRI and a learning paradigm, this study examined the independent contributions of the hippocampus and striatum to simple association and frequency-based learning. We scanned 10 right-handed young adult subjects using a spiral in/out sequence on a GE 3.0 T scanner during performance of the learning paradigm. The paradigm consisted of 2 cues that predicted each of 3 targets with varying probabilities. Simultaneously, we varied the frequency with which each target was presented throughout the task, independent of cue associations. Subjects had shorter response latencies to frequently occurring and highly associated target stimuli and longer response latencies to infrequent target stimuli, indicating learning. Imaging results showed increased caudate activity to infrequent relative to frequent targets and increased hippocampal activity to infrequent relative to frequent cue-target associations. This work provides evidence of different neural mechanisms underlying learning based on simple frequencies versus associations within a single paradigm.

[1]  E. Crone,et al.  Dissociation of response conflict, attentional selection, and expectancy with functional magnetic resonance imaging. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[2]  R. Benson,et al.  Responses to rare visual target and distractor stimuli using event-related fMRI. , 2000, Journal of neurophysiology.

[3]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[4]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[5]  J. Rohrbaugh,et al.  Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events. , 1980, Science.

[6]  Norman A. Krasnegor,et al.  Measurement of Audition and Vision in the First Year of Postnatal Life: A Methodological Overview , 1985 .

[7]  Mark D'Esposito,et al.  Rapid Prefrontal-Hippocampal Habituation to Novel Events , 2004, The Journal of Neuroscience.

[8]  R N Aslin,et al.  Statistical Learning by 8-Month-Old Infants , 1996, Science.

[9]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[10]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[11]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  H Eichenbaum,et al.  Memory for items and memory for relations in the procedural/declarative memory framework. , 1997, Memory.

[13]  Gary H Glover,et al.  Improved combination of spiral‐in/out images for BOLD fMRI , 2004, Magnetic resonance in medicine.

[14]  Aziz M. Ulug,et al.  Parametric manipulation of conflict and response competition using rapid mixed-trial event-related fMRI , 2003, NeuroImage.

[15]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[16]  M. Bornstein Habituation of attention as a measure of visual information processing in human infants: Summary , 1985 .

[17]  B. J. Casey,et al.  The Effect of Preceding Context on Inhibition: An Event-Related fMRI Study , 2002, NeuroImage.

[18]  Suzanne Corkin,et al.  Dissociations Among Structural-Perceptual, Lexical-Semantic, and Event-Fact Memory Systems in Alzheimer, Amnesic, and Normal Subjects , 1994, Cortex.

[19]  M. Gluck,et al.  Dissociating medial temporal and basal ganglia memory systems with a latent learning task , 2003, Neuropsychologia.

[20]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[21]  Aziz M. Ulug,et al.  Differential cingulate and caudate activation following unexpected nonrewarding stimuli , 2004, NeuroImage.

[22]  R. O’Reilly,et al.  Conjunctive representations in learning and memory: principles of cortical and hippocampal function. , 2001, Psychological review.

[23]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[24]  M. Gluck,et al.  Dissociating Hippocampal versus Basal Ganglia Contributions to Learning and Transfer , 2003, Journal of Cognitive Neuroscience.

[25]  J. Horvitz Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

[26]  Elizabeth K. Johnson,et al.  Statistical learning of tone sequences by human infants and adults , 1999, Cognition.

[27]  B. Strange,et al.  Adaptive anterior hippocampal responses to oddball stimuli , 2001, Hippocampus.

[28]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[29]  J. W. Rudy,et al.  The Role of the Dorsal Hippocampus in the Acquisition and Retrieval of Context Memory Representations , 2004, The Journal of Neuroscience.

[30]  Michael J. Frank,et al.  Hippocampus, cortex, and basal ganglia: Insights from computational models of complementary learning systems , 2004, Neurobiology of Learning and Memory.

[31]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[32]  Anthony R. McIntosh,et al.  Memory encoding and hippocampally-based novelty/familiarity discrimination networks , 2003, Neuropsychologia.

[33]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[34]  Scott P. Johnson,et al.  Visual statistical learning in infancy: evidence for a domain general learning mechanism , 2002, Cognition.

[35]  K. Kunz,et al.  Dissociating Striatal and Hippocampal Function Developmentally with a Stimulus–Response Compatibility Task , 2002, The Journal of Neuroscience.

[36]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  R. Knight Contribution of human hippocampal region to novelty detection , 1996, Nature.

[38]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[39]  R. Poldrack,et al.  Competition among multiple memory systems: converging evidence from animal and human brain studies , 2003, Neuropsychologia.

[40]  E. N. Solokov Perception and the conditioned reflex , 1963 .

[41]  G. Berns,et al.  Brain regions responsive to novelty in the absence of awareness. , 1997, Science.