The Neural Mechanisms of Associative Memory Revisited: fMRI Evidence from Implicit Contingency Learning

Marco P Caviezel; Carolin F Reichert; Dena Sadeghi Bahmani; Christoph Linnemann; Caroline Liechti; Oliver Bieri; Stefan Borgwardt; Thomas Leyhe; Tobias Melcher

doi:10.3389/fpsyt.2019.01002

The Neural Mechanisms of Associative Memory Revisited: fMRI Evidence from Implicit Contingency Learning

Front Psychiatry. 2020 Feb 3:10:1002. doi: 10.3389/fpsyt.2019.01002. eCollection 2019.

Authors

Marco P Caviezel¹, Carolin F Reichert^{2

3}, Dena Sadeghi Bahmani^{1

4

5}, Christoph Linnemann¹, Caroline Liechti^{1

6}, Oliver Bieri⁷, Stefan Borgwardt^{8

9}, Thomas Leyhe^{1

6}, Tobias Melcher¹

Affiliations

¹ Center of Old Age Psychiatry, Psychiatric University Hospital (UPK), University of Basel, Basel, Switzerland.
² Transfaculty Research Platform Molecular and Cognitive Neuroscience, University of Basel, Basel, Switzerland.
³ Centre for Chronobiology, Psychiatric University Hospital (UPK), University of Basel, Basel, Switzerland.
⁴ Center of Affective, Stress and Sleep Disorders (ZASS), Psychiatric Clinics (UPK), University of Basel, Basel, Switzerland.
⁵ Kermanshah University of Medical Sciences (KUMS), Substance Abuse Prevention Research Center, Health Institute, and Sleep Disorders Research Center, Kermanshah, Iran.
⁶ Geriatric Psychiatry, Department of Geriatric Medicine FELIX PLATTER, University of Basel, Basel, Switzerland.
⁷ Division of Radiological Physics, Department of Radiology, University Hospital of Basel, University of Basel, Basel, Switzerland.
⁸ Translational Psychiatry Unit (TPU), Department of Psychiatry and Psychotherapy, University of Lübeck, Lübeck, Germany.
⁹ Psychiatric University Hospital (UPK), University of Basel, Basel, Switzerland.

Abstract

The literature describes a basic neurofunctional antagonism between episodic memory encoding and retrieval with opposed patterns of neural activation and deactivation, particularly in posterior midline regions. This has been coined the encoding/retrieval (E/R) flip. The present fMRI study uses an innovative task paradigm to further elucidate neurofunctional relations of encoding and retrieval in associative memory. Thereby, memory encoding is implemented as implicit (non-deliberate) cognitive process, whereas the prior literature focused mainly on explicit encoding. Moreover, instead of defining brain activations related to successful (vs. unsuccessful) memory performance, the task paradigm provides proper no-memory baseline conditions. More specifically, the encoding task includes trials with non-contingent (not learnable) stimulus combinations, while the retrieval task uses trials with a simple matching exercise with no mnemonic requirements. The analyses revealed circumscribed activation in the posterior middle cingulate cortex (pMCC) together with prominent deactivation in the anterior insula cortex (aIC) as core neural substrate of implicit memory encoding. Thereby, the pMCC exhibited positive functional connectivity to the hippocampus. Memory retrieval was related to an activation pattern exactly opposed to memory encoding with deactivation in the pMCC and activation in the aIC, while the aIC additionally exhibited a negative (i.e., arguably inhibitive) functional connectivity to the pMCC. Important to note, the observed pattern of activations/de-activations in the pMCC appears to conflict with prevalent E/R flip findings. The outlined results and their (alleged) discrepancies with prior study reports are discussed primarily in the context of the default mode network's functioning and its context-sensitive regulation. Finally, we point out the relevance of the present work for the understanding and further investigation of the neurofunctional aberrations occurring during normal and pathological aging.

Keywords: Alzheimer’s disease; association memory; cingulate cortex; contingency learning; default mode network; fMRI; functional connectivity; implicit memory.