Impaired Auditory Recognition Memory in Amnesic Patients with Medial Temporal Lobe Lesions

Abstract

Two tests of auditory recognition memory were given to four patients with bilateral hippocampal damage (H+) and three patients with large medial temporal lobe lesions and additional variable damage to lateral temporal cortex (MTL+). When single stimuli were presented, performance was normal across delays as long as 30 sec, presumably because information could be maintained in working memory through rehearsal. When lists of 10 stimuli were presented, performance was impaired after a 5-min delay. Patients with MTL+ lesions performed marginally worse than patients with H+ lesions, consistent with findings for recognition memory in other modalities. The findings show that auditory recognition, like recognition memory in other sensory modalities, is dependent on the medial temporal lobe.Bilateral medial temporal lobe lesions in humans produce severe, multimodal memory impairment (Scoville and Milner 1957;Stefanacci et al. 2000). In one study, the noted patient H.M. failed tests of recognition memory when either visual stimuli (shades of red, lights flashes, or nonsense patterns) or auditory stimuli (tones or clicks) were presented, and delays of 60 sec were interposed between study and test (Milner 1972). After the development of one-trial tests of recognition memory for the monkey (Gaffan 1974;Mishkin and Delacour 1975), impaired recognition memory after medial temporal lobe lesions has been observed in the visual (Mishkin 1978;Zola-Morgan et al. 1982) and tactile (Murray and Mishkin 1984;Suzuki et al. 1993) modalities. Impaired recognition memory also has been observed in rats in the visual and olfactory modalities, when tests were given that were similar to those used with the monkey (Clark et al. 2000(Clark et al. , 2001Otto and Eichenbaum 1992).Aside from early studies of patient H.M., the effects of medial temporal lobe lesions on auditory recognition memory have not been well studied. Patients with left or right unilateral temporal lobe excisions, which included the amygdala, temporal pole, anterior neocortex, and variable extents of hippocampus and parahippocampal gyrus, were impaired at recognizing novel melodies (Samson and Zatorre 1992). However, it is unclear to what extent this impairment depended on damage specifically to the medial temporal lobe.Preliminary studies in the monkey suggested that large medial temporal lobe lesions do impair auditory recognition memory (Fritz et al. 1999). However, smaller lesions limited to perirhinal and entorhinal cortex had little effect (Saunders et al. 1998), in sharp contrast with the deficit in both visual and tactile recognition memory that is found in monkeys after perirhinal and entorhinal lesions (Meunier et al. 1993;Buffalo et al. 1999) . In addition, studies of auditory recognition memory have been conducted in dogs, with delays of up to 90 sec (Kowalskaet al. 2001). Neither lesions of the hippocampus (H), lesions of perirhinal and entorhinal cortex (Rh), nor combined lesions (H + Rh) had a detectable effect on performance. These findings raise questions abou...

When recognition memory is independent of hippocampal function

“…For example, recognition memory was impaired after hippocampal lesions for unfamiliar pseudowords and nonword letter strings (26,27). Recognition memory was also impaired for junk objects (5) and novel sounds after hippocampal lesions (28). In summary, for face recognition memory to be spared after hippocampal lesions, it is necessary that the faces be unfamiliar, but their familiar-unfamiliar status does not fully account for spared face memory after hippocampal lesions.…”

Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregions

“…The important result from our study remains, nonetheless, that same-range disruptions of hippocampal CA1 and CA3 subregions result in a deficit in the encoding and consolidation of memory, whereas they spare the retrieval mechanism, leading to the observation that hippocampal networks are not evenly requested during all stages of contextual memory processing. A more compelling explanation can nevertheless be put forward; retrieval tests in animal experiments generally make use of recognition rather than recall procedures, as is the case in our study, so that the subject can recognize the environment, which does not need a functional hippocampus, since it has been widely demonstrated in humans and animals that recognition memory remains relatively performing when the hippocampus has been damaged either by ischemia (Mayes et al 2004), or lesions of various origins (Squire et al 2001), experimental lesions (Forwood et al 2005), aging (McIntosh et al 1999;Sekuler et al 2005), or even degenerative processes as in Alzheimer's disease (Karlsson et al 2003).…”

Impaired odor recognition memory in patients with hippocampal lesions

“…In humans, monkeys, and rats, recognition memory depends on the integrity of the hippocampal region (the hippocampus proper, the dentate gyrus, and the subicular complex) (for review, see Squire et al 2004). In humans, impaired recognition memory following lesions thought to be limited to the hippocampal region has been demonstrated for verbal and nonverbal material (Reed and Squire 1997) as well as for nonsense sounds (Squire et al 2001) (For the view that some aspects of recognition performance are spared following hippocampal lesions, see Brown and Aggleton, 2001;Yonelinas et al 2002; but see Manns et al 2003, Wixted and.…”