Object–location memory impairment in patients with thermal lesions to the right or left hippocampus
Introduction
Bilateral lesions of the medial temporal lobes result in profound global amnesia (Scoville & Milner, 1957). Neuropsychological effects of unilateral medial temporal lobe lesions involve milder memory deficits that were often found to be material-specific. Left-sided lesions were associated with verbal memory impairment (Bohbot et al., 1998, Frisk & Milner, 1990, Helmstaedter & Elger, 1996) and episodic memory recall deficits (Spiers et al., 2001) while right-sided damage was accompanied by poor performance on non-verbal and spatial memory tasks (Bohbot et al., 1998, Jones-Gotman, 1986, Smith & Milner, 1981, Smith & Milner, 1989). Brain imaging protocols supported evidence of lateralisation of information since verbal tasks in fMRI studies activated the left hemisphere more (Kirchhoff, Wagner, Maril, & Stern, 2000), and spatial tasks in PET or fMRI studies preferentially activated the right (Bohbot et al., 2000b; Iaria, Petrides, Dagher, Pike, & Bohbot, 2003; Maguire et al., 1998). However, there is evidence that subjects with unilateral damage to the hippocampus are deficient at certain memory tasks regardless of the side of the lesion (Dobbins, Kroll, Tulving, Knight, & Gazzaniga, 1998; Kroll, Knight, Metcalfe, Wolf, & Tulving, 1996; Maguire, Burke, Phillips, & Staunton, 1996). Memory impairment for object–location is thought to be part of a broader class of spatial memory deficit observed in patients with lesions of the right medial temporal lobe (O’Keefe & Nadel, 1978). Just how broad the class of hippocampus-dependent behaviours may be, is still a matter of intense speculation (Aggleton & Brown, 1999, Eichenbaum, 2000, Nadel & Moscovitch, 2001, Squire, 1992, Tulving & Markowitsch, 1998, Vargha-Khadem et al., 1997).
Among non-verbal memory tasks, those assessing memory for object–location are unique in the sense that they require a synthesis of two forms of knowledge, object identity and its placement. Smith & Milner, 1981, Smith & Milner, 1989 were the first to suggest that object–location memory was mediated by the right hippocampus (RH) in humans. The convergence in the hippocampus of pathways involved in object recognition such as the perirhinal cortex (Murray & Mishkin, 1998) and memory for places such as the parahippocampal cortex (Bohbot et al., 1998) supports this view (Ungerleider & Mishkin, 1982). Smith & Milner, 1981, Smith & Milner, 1989 and Crane, Milner, and Leonard (1995) used small-scale object–location tests in patients with unilateral temporal lobe damage of varying size. Subjects with large hippocampal excisions from the right temporal lobe were found to perform worse than normal controls (NC) when recall of object–locations was tested after a delay of 2–4 min. On the other hand, subjects with left temporal lesions involving small or large portions of the hippocampus and those with small right-sided hippocampal removals performed normally. Smith and Milner (1989) also reported that the recall deficit in their patients was not related to the size of the neocortical excision. Bohbot et al. (1998) showed that a lesion involving the RH leaving the right parahippocampal cortex intact was sufficient to produce an object–location memory impairment. The dissociation between the hippocampus and parahippocampal cortex could not be shown explicitly until then since the patients that were previously tested typically had medial temporal lobe resections that included the parahippocampal cortex in addition to the lesion of the hippocampus, amygdala and other cortical structures (Smith & Milner, 1989). Crane (2000) and Nunn, Graydon, Polkey, and Morris (1999) started to address this issue by finding a positive correlation between memory for object–location and the amount of RH present in patients with right medial temporal resections.
In comparison to the studies with humans, the results of experiments addressing the role of the non-human hippocampus in location and object–location memories are rather controversial. Parkinson, Murray, and Mishkin (1988) and Angeli, Murray, and Mishkin (1993) found that monkeys who underwent bilateral hippocampectomy could not remember two places out of three in a delayed matched to sample location task. Gaffan (1998) also noted that monkeys with lesions to the Delay–Brion system (formed by the fornix, mamillary bodies and anterior thalamic nuclei) showed similar deficits when required to remember one out of two places that were either occupied by identical dots or different objects. Murray and Mishkin (1998), however, demonstrated intact memory for two locations in monkeys with bilateral excitotoxic lesions of the amygdala and hippocampus. When discussing the neural substrates of location memory, the authors pointed out that medial temporal lobe removals in the studies of Parkinson et al. (1988) and Angeli et al. (1993) extended beyond the hippocampus proper, involving also the subicular complex and the parahippocampal cortex. The fact that the cortical structures surrounding the hippocampus could have a specific role in memory for object–locations is supported by the results of Bussey, Duck, Muir, and Aggleton (2000). They used a task requiring rats to discriminate between objects that remained in fixed locations from those that exchanged locations with other objects. The deficit found in rats with bilateral lesions to the perirhinal and postrhinal cortices (rat equivalent of the primate parahippocampal cortex) was more robust than that detected in animals with bilateral fornix lesions.
The aim of the present study was to clarify the involvement of the human hippocampus and related temporal lobe structures in the memory for object–location in an extended extra-personal space. Unlike the patients described in most of the literature concerned with object–location memory, our subjects had received small stereotaxic thermocoagulation lesions involving different combinations of medial temporal lobe structures. An example of the precise lesion resulting from this type of surgery is shown in Fig. 1. The initial assessment of this population showed that a lesion of the RH led to a deficit in memory for four object–location associations (Bohbot et al., 1998). In that study, the subjects were tested in an open rectangular room with various other objects and features that were presumed to be used only as orienting cues. The present experiment was designed to answer four questions that arise from the initial study. (1) Is the object–location memory impairment primarily caused by inaccurate encoding and recall, i.e. a memory deficit, or could the deficit observed in Bohbot et al. (1998) have originated from a deficient 3D to 2D translation of object–location associations, i.e. a procedural deficit? (2) Do other medial temporal lobe structures contribute to this impairment seen in the patients with right hippocampal damage? (3) Is it possible to define and quantify any components of the object–location memory impairment, such as a deficient memory for the locations alone or an inability to orient the correctly recalled arrangement of objects on the map? (4) Does a higher memory load increase the magnitude of a deficit associated with lesions to the RH and does it reveal an impairment in cases of damage to the left hippocampus (LH)?.
Section snippets
Normal controls
Nine right-handed NC were chosen to match the brain-operated patients with respect to sex, age and education. Their basic characteristics are shown in Table 1.
Brain-operated patients
This group consisted of 14 subjects who underwent stereotaxic thermolesions involving the medial temporal lobes at the Department of Neurosurgery, Central Military Hospital, Prague, Czech Republic as a treatment for their pharmacoresistant epilepsy. The lesions were unilateral in all but three cases (these three people had sustained
Relationship between performance and various medial temporal lobe structures
The patients were assigned to two groups according to which of their hippocampi was damaged. Patients with lesions to the right hippocampus (RH: N=10) could be subdivided in two ways. One option was to define two subgroups consisting of people with and without additional damage to the right parahippocampal cortex (RH+PH+: N=3; RH+PH−: N=7). The second possibility was to separate patients with and without additional lesions of the right perirhinal cortex (RH+PR+: N=6; RH+PR−: N=4). Two patients
Object–locations: a deficit in 3D to 2D translation or encoding and recall?
The patients with lesions of the hippocampus had no consistent deficits in Translation phase, suggesting that they can accurately perceive the object–location associations and translate them to a map. Yet, they were impaired at immediate recall of the object–location associations. When amnesic patients had a greater memory impairment after a delay compared to immediate recall, it was interpreted as a retrieval deficit (Smith & Milner, 1989, Warrington & Weiskrantz, 1970). Most imaging studies
Acknowledgements
We are grateful to Dr. J. Bures for his help with the realisation of the experiments and data evaluation and for his comments on the manuscript. We would also like to thank to Ing. Yu. Kaminsky for his participation in the development of hardware and software. This work was supported by grants 97-34EE, 98-38 CNS-QUA.05 from the McDonnell Foundation, as well as NSERC, and by GA 309/02/1218/A from the Grant Agency of the Czech Republic.
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