When the extended hippocampal system is of no need for context-free memory: a case of developmental amnesia

International audienceIntroductionWe describe the case of a patient with severely impaired episodic memory who has acquired normal to supra-normal context-free (semantic) memory.A large body of data converges to consider that medial temporal lobe structures (MTL) critically contribute to declarative memory. However, it remains unclear whether and how declarative memory can be subdivided in different functional systems. Selective hippocampal injury has led to deficits of both recollection- and familiarity-based recognition memory in some cases but, alternatively, recent evidence for a double anatomo-functional dissociation between subhippocampal structures and hippocampus has challenged unitary accounts of MTL contributions to declarative memory. Further, lesion studies mainly focus on subhippocampal structures and hippocampus rather than considering possible damage to other components of the extended hippocampal system (EHS). Here we bring evidence that acquisition of a supra-normal amount of context-free memories can occur despite massive damage to the whole EHS sparing rhinal cortices.Case description and resultsKA, a 27 year-old man, suffered from severe hypoxia at birth. At age 7-8, his parents worried about spatial disorientation and memory loss. Medical consultations remained helpless until KA consulted our memory clinic. Neuropsychological examination revealed a typical pattern of anterograde amnesia, with a 44 point discrepancy between Intelligence and Memory Quotients. Impairment across recall tasks was severe, but recognition memory was normal for 9/11 standardized tests, even after a delay. Experiments using the Speed and Accuracy Boosting procedure highlighted normal familiarity-based recognition memory for meaningful items. Strikingly, KA demonstrated supra normal context-free verbal and visual memories (mean percentile score was 69 across 6 tasks), and he performed better than and as fast as controls under temporal constraints. Neuroimaging findings revealed selective abnormalities of the hippocampus (bilateral atrophy >50%), mammillary bodies, fornix and mammillothalamic tract, as well as bilateral thalamus, anterior cingulate and right retrosplenial cortices. In contrast, anterior subhippocampal cortices were either preserved or thicker than controls.ConclusionPreserved anterior subhippocampal cortices within a severely impaired extended hippocampal system can subserve familiarity-dependent recognition memory. To our knowledge, this is the first report of supra-normal context-free memory in such a severely amnesic patient. These findings raise important questions about how such knowledge has been acquired in KA. Overall, that case strongly speaks for at least two dissociable declarative memory systems, either supporting context-rich or context-free memories