Human Hippocampal Dynamics during Response Conflict

Besides its relevance for declarative memory functions, hippocampal activation has been observed during disambiguation of uncertainty and conflict. Uncertainty and conflict may arise on various levels. On the perceptual level, the hippocampus has been associated with signaling of contextual deviance and disambiguation of similar items (i.e., pattern separation). Furthermore, conflicts can occur on the response level. Animal experiments showed a role of the hippocampus for inhibition of prevailing response tendencies and suppression of automatic stimulus-response mappings, potentially related to increased theta oscillations (3-8 Hz). In humans, a recent fMRI study demonstrated hippocampal involvement in approach-avoidance conflicts. However, the more general significance of hippocampal activity for dealing with response conflicts also on a cognitive level is still unknown. Here, we investigated the role of the hippocampus for response conflict in the Stroop task by combining intracranial electroencephalography (iEEG) recordings from the hippocampus of epilepsy patients with region of interest-based fMRI in healthy participants. Both methods revealed converging evidence that the hippocampus is recruited in a regionally specific manner during response conflict. Moreover, our iEEG data show that this activation depends on theta oscillations and is relevant for successful response conflict resolution.

[1]  Memory, amnesia, and the hippocampal system , 1994 .

[2]  Current Biology , 2012, Current Biology.

[3]  L. Jarrard,et al.  The hippocampus and inhibitory learning: a ‘Gray’ area? , 2004, Neuroscience & Biobehavioral Reviews.

[4]  C Brock Kirwan,et al.  Overcoming interference: an fMRI investigation of pattern separation in the medial temporal lobe. , 2007, Learning & memory.

[5]  R. Passingham.  The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[6]  Simon Hanslmayr,et al.  Neural Communication Patterns Underlying Conflict Detection, Resolution, and Adaptation , 2014, The Journal of Neuroscience.

[7]  P. Dudchenko.  The hippocampus as a cognitive map , 2010 .

[8]  M. Wilson,et al.  Dentate Gyrus NMDA Receptors Mediate Rapid Pattern Separation in the Hippocampal Network , 2007, Science.

[9]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[10]  K. Okada,et al.  Neural activity in the hippocampus during conflict resolution , 2013, Behavioural Brain Research.

[11]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[12]  J. Gray.  The neuropsychology of anxiety. , 1985, Issues in mental health nursing.

[13]  J. Rawlins,et al.  Hippocampal synaptic plasticity, spatial memory and anxiety , 2014, Nature Reviews Neuroscience.

[14]  D. Kumaran,et al.  Which computational mechanisms operate in the hippocampus during novelty detection? , 2007, Hippocampus.

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

[16]  Laura A. Ewell,et al.  Frequency-Tuned Distribution of Inhibition in the Dentate Gyrus , 2010, The Journal of Neuroscience.

[17]  T. Egner,et al.  Neural conflict-control mechanisms improve memory for target stimuli. , 2015, Cerebral cortex.

[18]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[19]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[20]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[21]  J. Rawlins,et al.  Hippocampal NMDA receptors are important for behavioural inhibition but not for encoding associative spatial memories , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  Frank Schneider,et al.  Dependence of amygdala activation on echo time: Results from olfactory fMRI experiments , 2006, NeuroImage.

[23]  J. Rawlins,et al.  Dissecting Spatial Knowledge from Spatial Choice by Hippocampal NMDA Receptor Deletion , 2012, Nature Neuroscience.

[24]  Nikolai Axmacher,et al.  Activation of the caudal anterior cingulate cortex due to task‐related interference in an auditory Stroop paradigm , 2009, Human brain mapping.

[25]  Michael A. Yassa,et al.  Perceptual versus conceptual interference and pattern separation of verbal stimuli in young and older adults , 2013, Hippocampus.

[26]  E. Rolls.  A theory of hippocampal function in memory , 1996, Hippocampus.

[27]  D. Kimble,et al.  Hippocampectomy and response perseveration in the rat. , 1965, Journal of comparative and physiological psychology.

[28]  M. Kutas,et al.  Limbic P300s in temporal lobe epilepsy with and without Ammon's horn sclerosis , 1999, The European journal of neuroscience.

[29]  Dominik R. Bach,et al.  Human Hippocampus Arbitrates Approach-Avoidance Conflict , 2014, Current Biology.

[30]  C. Stark,et al.  Pattern Separation in the Human Hippocampal CA3 and Dentate Gyrus , 2008, Science.

[31]  D. Kumaran,et al.  An Unexpected Sequence of Events: Mismatch Detection in the Human Hippocampus , 2006, PLoS biology.

[32]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .