Elsevier

Neuropsychologia

Volume 42, Issue 8, 2004, Pages 1017-1028
Neuropsychologia

Object–location memory impairment in patients with thermal lesions to the right or left hippocampus

https://doi.org/10.1016/j.neuropsychologia.2004.01.002Get rights and content

Abstract

Memory for object–location was investigated by testing subjects with small unilateral thermolesions to the medial temporal lobe using small-scale 2D (Abstract) or large-scale 3D (Real) recall conditions. Four patients with lesions of the left hippocampus (LH), 10 patients with damage to the right hippocampus (RH) and 9 matched normal controls (NC) were tested. Six task levels were presented in a pseudorandom order. During each level, subjects viewed one to six different objects on the floor of a circular curtained arena 2.90 m in diameter for 10 s. Recall was tested by marking the locations of objects on a map of the arena (Abstract recall) and then by replacing the objects in the arena (Real recall). Two component errors were studied by calculating the Location Error (LE), independent of the object identity and the configuration error by finding the best match to the presented configuration. The RH group was impaired relative to the NC for nearly all combinations of recall and error types. An impairment was observed in this group even for one object and it deepened sharply with an increasing object number. Damage to the right perirhinal or parahippocampal cortices did not add to the impairment. Deficits in the LH group were also observed, but less consistently. The data indicate that spatial memory is strongly but not exclusively lateralised to the right medial temporal lobe.

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.

References (54)

  • E.A. Maguire et al.

    Topographical disorientation following unilateral temporal lobe lesions in humans

    Neuropsychologia

    (1996)
  • L. Nadel et al.

    The hippocampal complex and long-term memory revisited

    Trends in Cognitive Science

    (2001)
  • M.L. Smith et al.

    The role of the right hippocampus in the recall of spatial location

    Neuropsychologia

    (1981)
  • M.L. Smith et al.

    Right hippocampal impairment in the recall of spatial location: Encoding deficit or rapid forgetting?

    Neuropsychologia

    (1989)
  • J.P. Aggleton et al.

    Episodic memory, amnesia, and the hippocampal-anterior thalamic axis

    Behavioral and Brain Sciences

    (1999)
  • G.K. Aguirre et al.

    The parahippocampus subserves topographical learning in man

    Cerebral Cortex

    (1996)
  • G.K. Aguirre et al.

    Neural components of topographical representation

    Proceedings of the National Academy of Sciences

    (1998)
  • Bachevalier, J., Nemanic, S., Alvarado, M. C. (2002). The medial temporal lobe structures and object recognition memory...
  • V.D. Bohbot et al.

    Memory deficits characterized by patterns of lesions to the hippocampus and parahippocampal cortex

    Annals of the New York Academy of Sciences

    (2000)
  • V.D. Bohbot et al.

    Experience dependent modulation of medial temporal lobe fMRI activity

    Neuroimage

    (2000)
  • J.B. Brewer et al.

    Making memories: Brain activity that predicts how well visual experience will be remembered

    Science

    (1998)
  • Conover, W. J. (1980). Practical non-parametric statistics. New York:...
  • Crane, J. (2000). Right medial temporal-lobe contribution to object–location memory. Unpublished doctoral thesis,...
  • J. Crane et al.

    Spatial array learning by patients with focal temporal lobe excisions

    Society for Neuroscience Abstracts

    (1995)
  • H. Eichenbaum

    A cortical-hippocampal system for declarative memory

    Nature Reviews Neuroscience

    (2000)
  • R. Epstein et al.

    A cortical representation of the local visual environment

    Nature

    (1998)
  • D. Gaffan

    Idiothetic input into object–place configuration as the contribution to memory of the monkey and human hippocampus: A review

    Experimental Brain Research

    (1998)
  • Cited by (73)

    • Material-specific interference control is dissociable and lateralized in human prefrontal cortex

      2014, Neuropsychologia
      Citation Excerpt :

      To test whether RVLPFC or LVLPFC is critical in resolving conflict in the Stroop and flanker tasks, non-parametric, between-subject comparisons were performed on the interference effects in each task, here defined as the difference between mean incongruent and congruent RT. For three-group comparisons (Experiment 1), the Kruskal–Wallis test was used, followed by post-hoc Dunn׳s tests where appropriate (for similar analytic approach in other small sample human lesion studies, see Hilz et al., 2006; Petrides, 1985; Stepankova et al., 2004). The Mann–Whitney test was used for two-group comparisons (Experiment 2).

    View all citing articles on Scopus
    View full text