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Behavioral/Systems/Cognitive

Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice

Giuseppe Iaria, Michael Petrides, Alain Dagher, Bruce Pike and Véronique D. Bohbot
Journal of Neuroscience 2 July 2003, 23 (13) 5945-5952; DOI: https://doi.org/10.1523/JNEUROSCI.23-13-05945.2003
Giuseppe Iaria
1Douglas Hospital Research Center, McGill University, Verdun, Quebec, Canada, H4H 1R3, 2Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada H3A 2B4, 3Dipartimento di Psicologia, Università di Roma “La Sapienza”, Roma, Italy, and Instituto di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia, Roma, Italy 00179
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Michael Petrides
1Douglas Hospital Research Center, McGill University, Verdun, Quebec, Canada, H4H 1R3, 2Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada H3A 2B4, 3Dipartimento di Psicologia, Università di Roma “La Sapienza”, Roma, Italy, and Instituto di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia, Roma, Italy 00179
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Alain Dagher
1Douglas Hospital Research Center, McGill University, Verdun, Quebec, Canada, H4H 1R3, 2Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada H3A 2B4, 3Dipartimento di Psicologia, Università di Roma “La Sapienza”, Roma, Italy, and Instituto di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia, Roma, Italy 00179
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Bruce Pike
1Douglas Hospital Research Center, McGill University, Verdun, Quebec, Canada, H4H 1R3, 2Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada H3A 2B4, 3Dipartimento di Psicologia, Università di Roma “La Sapienza”, Roma, Italy, and Instituto di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia, Roma, Italy 00179
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Véronique D. Bohbot
1Douglas Hospital Research Center, McGill University, Verdun, Quebec, Canada, H4H 1R3, 2Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada H3A 2B4, 3Dipartimento di Psicologia, Università di Roma “La Sapienza”, Roma, Italy, and Instituto di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia, Roma, Italy 00179
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  • Figure 1.
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    Figure 1.

    A view of the virtual environment. Note that the landscape and a tree can be viewed at a distance, whereas the objects down the stairs at the end of the arms are not visible from the center of the maze.

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    Figure 2.

    The behavioral results. A, The total number of errors made in the training phase (sections II and III) averaged across subjects in the spatial memory, shift, and nonspatial strategy groups. B, The number of errors made while performing the probe trial in sections I (probe 1) and IV (probe 2) averaged across subjects in the spatial memory, shift, and nonspatial strategy groups. C, The average time that the spatial memory, shift, and nonspatial strategy groups required to perform one trial in sections (S) I to IV of the experiment. SEM are shown. Asterisks indicate that the spatial memory group is different from the nonspatial strategy group; p < 0.05.

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    Figure 3.

    Brain activity common to both spatial memory and nonspatial strategy groups (experimental minus control task). The t maps are superimposed onto the anatomical average of all participants and displayed in the sagittal plane. A, Posterior parietal cortex. B, Middorsolateral prefrontal cortex. C, Motor–premotor cortical region. D, Supplementary motor cortex. E, Putamen. L, Left hemisphere; R, right hemisphere.

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    Figure 4.

    Activity in the hippocampus and caudate nucleus found in the spatial memory group and nonspatial strategy group, respectively. The t maps are superimposed onto the anatomical average of all participants and displayed in the sagittal and coronal planes. A, Activity in the right hippocampus when contrasting the experimental and control conditions of the spatial memory group, minus those of the nonspatial strategy group in the first scan (x = 32; y = -14; z = -20; t = 4.41). B, Activity in the right caudate nucleus found in the nonspatial strategy group (scan 5) (x = 14; y =-8; z = 22; t = 4.04).

Tables

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    Table 1.

    Brain activity common to both spatial memory and nonspatial strategy groups

    Talairach coordinates
    Anatomical region xyzt value
    Right
        Parietal cortex 18 -64 54 6.5
        Middle frontal gyrus 30 34 28 4.9
        Motor-premotor cortical region 24 -12 54 5.76
    4 4 48 4.51
        Supplementary motor cortex 8 -4 48 4.94
        Cingulate cortex 12 18 40 4.75
    12 4 40 4.77
        Putamen 28 4 4 4.05
        Caudate nucleus 16 -8 22 4.07
        Cerebellum 30 -34 -42 5.02
    Left
        Parietal cortex -28 -60 56 7.16
        Middle frontal gyrus -32 26 28 5.31
        Motor-premotor cortical region -28 -8 52 5.79
    -32 -24 62 5.76
        Supplementary motor cortex -6 -10 54 5.02
        Middle occipital gyrus -32 -82 16 4.6
        Putamen -30 4 0 4.99
    • View popup
    Table 2.

    Brain activity found in the hippocampus and caudate nucleus of the spatial memory and nonspatial strategy groups

    Talairach coordinates
    Anatomical region XYZt value
    Spatial memory group
    Right hippocampus
        scan 1 32 -14 -20 4.41
        scan 2 22 -16 -14 3.49
    Right caudate nucleus
        scan 2 14 -6 20 4.82
        scan 8 24 -22 24 4.65
    Left caudate nucleus
        scan 8 -20 -2 24 3.58
    Nonspatial strategy group
    Right caudate nucleus
        scan 4 20 8 18 3.81
        scan 5 14 -8 22 4.04
        scan 6 20 -24 22 4.41
        scan 8 8 -4 20 5.36
    Left caudate nucleus
        scan 6 -12 -10 18 4.3
    • View popup
    Table 3.

    Correlation between the BOLD signal increases and error rate in the spatial memory and nonspatial strategy groups

    Talairach coordinates
    Anatomical region XYZt value
    Spatial memory group (errors)
    Positive correlation
        Right hippocampus 32 -14 -20 2.38
        Left hippocampus -34 -36 -8 2.86
    Negative correlation
        Right caudate nucleus 14 -6 18 -3.75
    Nonspatial strategy group (errors)
    Positive correlation
        Right angular gyrus (area 39) 52 -70 24 4.48
    Negative correlation
        Right caudate nucleus 14 -16 22 -3.12
        Left caudate nucleus -18 -14 24 -3.91
        Left parietal cortex (area 7) -26 -60 56 -4.85
        Right cerebellum 0 -58 -26 -9.65
        Left cerebellum -6 -62 -22 -10.32
    • View popup
    Table 4.

    Correlation between the BOLD signal increases and latency in the spatial memory and nonspatial strategy groups

    Talairach coordinates
    Anatomical region XYZt value
    Spatial memory group (latency)
    Positive correlation
        Right hippocampus 32 -34 -8 2.53
        Left hippocampus -26 -34 -6 2.32
        Negative correlation
        Right superior temporal gyrus (area 39) 58 -60 36 -5.93
        Right cingulate gyrus (area 32) 10 20 30 -5.08
        Right caudate nucleus 10 10 -4 -3.43
    Nonspatial strategy group (latency)
    Negative correlation
        Right caudate nucleus 14 -18 24 -3.84
        Left caudate nucleus -18 -16 24 -4.03
        Right cerebellum 0 -58 -26 -9.71
        Left cerebellum -6 -62 -22 -10.36
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The Journal of Neuroscience: 23 (13)
Journal of Neuroscience
Vol. 23, Issue 13
2 Jul 2003
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Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice
Giuseppe Iaria, Michael Petrides, Alain Dagher, Bruce Pike, Véronique D. Bohbot
Journal of Neuroscience 2 July 2003, 23 (13) 5945-5952; DOI: 10.1523/JNEUROSCI.23-13-05945.2003

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Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice
Giuseppe Iaria, Michael Petrides, Alain Dagher, Bruce Pike, Véronique D. Bohbot
Journal of Neuroscience 2 July 2003, 23 (13) 5945-5952; DOI: 10.1523/JNEUROSCI.23-13-05945.2003
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Keywords

  • spatial memory
  • place learning
  • striatum
  • virtual environment
  • topographical amnesia
  • basal ganglia

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