emory formation and long-term retention in humans and animals : onvergence towards a transformation account of ippocampal – neocortical interactions

Historically, the hippocampus has been viewed as a temporary memory structure. Consistent with the central premise of standard consolidation theory (SCT), a memory is initially hippocampus-dependent but, over time, it undergoes a consolidation process and eventually becoming represented in a distributed cortical network independent of the hippocampus. In this paper, we review evidence that is incompatible with each of the following essential features of SCT that are derived from its central premise: (1) Hippocampal damage reliably produces temporally graded retrograde amnesia, (2) all declarative explicit memories are equivalent with respect to consolidation, (3) consolidation entails a process of duplication in which a particular cortically based memory is identical to the hippocampus-dependent memory from which it derived, (4) consolidated memories are permanent and immutable. We propose an alternative hypothesis that assumes a transformation process and changes in the memory over time. Building on multiple trace theory (Nadel & Moscovitch, 1997), the transformation hypothesis contains three key elements that differentiate it from SCT: (1) An initially formed memory, which is assumed to be episodic and context-bound, remains dependent on the hippocampus for as long as it is available, (2) with time and experience, a hippocampal memory supports the development, in neocortex, of a less integrated, schematic version, which retains the gist of the original memory, but few of its contextual details, (3) there is a dynamic interplay between the two types of memory such that one or another may be dominant, depending on the circumstances at retrieval. Evidence is provided in support of the transformation hypothesis, which is advanced as a framework for unifying the seemingly disparate results of studies of de m anterograde and retrogra Since the classic work of Brenda Milner and her colleagues Penfield & Milner, 1958; Scoville & Milner, 1957), we have known hat bilateral lesions to the medial temporal lobes (MTL), that nclude the hippocampus, produce a profound anterograde amneia that is characterized by impaired long-term memory in the ace of preserved intelligence, perception and short-term memory. n addition, such patients exhibit a temporally graded retrograde mnesia (RA) in which information acquired shortly before surgery ∗ Corresponding author at: Rotman Research Institute, Baycrest Centre, 3560 athurst Street, Toronto, Ontario M6A 2E1, Canada. el. : +1 416 785 2500x3592; fax: +1 416 785 2474. E-mail address: gwinocur@rotman-baycrest.on. ca (G. Winocur). 028-3932/$ – see front matter © 2010 Elsevier Ltd. All rights reserved. oi:10.1016/j.neuropsychologia. 2010.04. 016 emory in the animal and human literatures. © 2010 Elsevier Ltd. All rights reserved. is lost whereas older memories are retained. Historically, this pattern of lost and spared memory has been interpreted in terms of standard consolidation theory (SCT) originally formulated in the 19th century (Burnham, 1904; Muller & Pilzecker, 1900; Ribot, 1882). The central feature of SCT is the idea that the formation of durable long-term memories, from transient short-term memories, is a time-dependent process (Hebb, 1949). Initially, retention and retrieval of long-term memories rely on the hippocampus, but eventually become independent of it as the memories become consolidated in extra-hippocampal (presumably neocortical) structures. Evidence consistent with SCT has also been reported in studies of animals subjected to hippocampal ablation and other amnestic treatments (Agranoff & Davis, 1967; Duncan, 1949; Winocur, 1985). Although not always explicitly stated, it is impor-