title: Not all declarative memories are created equal: Fast Mapping as a direct route to cortical declarative representations.
abstract: Memory formation for newly acquired associations typically depends on hippocampal-neocortical interactions. Through the process of system-consolidation, the mnemonic binding role of the hippocampus is subsequently replaced by cortical hubs, such as the ventromedial prefrontal cortex (vmPFC) or the anterior temporal lobe (ATL). Here, using BOLD-fMRI, we compared retrieval of semantic associations acquired through Fast Mapping (FM), an incidental, exclusion-based learning procedure, to retrieval of similar associations that were intentionally acquired through Explicit Encoding (EE). Despite an identical retrieval task, the encoding histories of the retrieved semantic associations (FM vs. EE) induced distinct neural substrates and disparate related neural dynamics in time. Retrieval of associations acquired through EE engaged the expected hippocampal and vmPFC related networks. Furthermore, retrieval intentionally encoded associations gave rise to a typical overnight increase in engagement of the vmPFC and increased vmPFC-hippocampal-neocortical functional connectivity. On the other hand, retrieval of associations acquired through FM immediately engaged an ATL related network that typically supports well-established semantic knowledge, a network that did not engage the hippocampus and the vmPFC. Moreover, FM learning was associated with minimal overnight changes in the BOLD responses and in the functional connectivity. Our findings indicate that FM may induce a direct, ATL-mediated acquisition and retention of novel arbitrary associations, bypassing the initial hippocampal-cortical representation phase. A direct, ATL-mediated vocabulary acquisition through FM could support the learning and retention of new associations in young children with presumably an immature hippocampal system, and possibly even in amnesic adults with hippocampal lesions.
authors.affiliation: Sagol Department of Neurobiology, University of Haifa, Mount Carmel, Haifa 39105, Israel.
authors.forename: Maayan
authors.initials: M
authors.lastname: Merhav
authors.affiliation: Sagol Department of Neurobiology, University of Haifa, Mount Carmel, Haifa 39105, Israel; Department of Human Biology, University of Haifa, Mount Carmel, Haifa 39105, Israel.
authors.forename: Avi
authors.initials: A
authors.lastname: Karni
authors.affiliation: Rotman Research Institute, Baycrest and Canadian Partnership for Stroke Recovery, Toronto, ON M6A 2E1, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3G3, Canada. Electronic address: agilboa@research.baycrest.org.
authors.forename: Asaf
authors.initials: A
authors.lastname: Gilboa
mesh_terms: D000328:Adult; D001921:Brain / Q000502:physiology*; D001931:Brain Mapping; D005260:Female; D006624:Hippocampus / Q000502:physiology; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D011939:Mental Recall / Q000502:physiology*; D017397:Prefrontal Cortex / Q000502:physiology; D021641:Recognition, Psychology / Q000502:physiology; D012660:Semantics; D013702:Temporal Lobe / Q000502:physiology; D055815:Young Adult
keywords: Anterior temporal lobe (ATL); Fast Mapping; Hippocampus; Semantic memory; System level consolidation; Ventromedial prefrontal cortex (vmPFC)