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Articles, Behavioral/Systems/Cognitive

Relationship between Functional Magnetic Resonance Imaging-Identified Regions and Neuronal Category Selectivity

Andrew H. Bell, Nicholas J. Malecek, Elyse L. Morin, Fadila Hadj-Bouziane, Roger B. H. Tootell and Leslie G. Ungerleider
Journal of Neuroscience 24 August 2011, 31 (34) 12229-12240; DOI: https://doi.org/10.1523/JNEUROSCI.5865-10.2011
Andrew H. Bell
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Nicholas J. Malecek
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Elyse L. Morin
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Fadila Hadj-Bouziane
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Roger B. H. Tootell
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Leslie G. Ungerleider
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  • Figure 1.
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    Figure 1.

    Identifying category-selective cortex in inferior temporal cortex. A, Examples of stimuli used for neuroimaging and neuronal recording studies. In the case of neuroimaging experiments, stimuli were presented on a random-dot background (right). In the case of neuronal recording experiments, all stimuli were presented on a black background and face stimuli were cropped (oval). B, Inflated views of the fMRI-identified category-selective regions in the left and right IT cortex of monkeys S and W, respectively. Insets show flattened views of the STS. Dashed ovals indicate the approximate areas accessible by the recording chambers. Arrows indicate the anterior and posterior face-selective regions. A, Anterior; S, superior.

  • Figure 2.
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    Figure 2.

    Methods for targeted recordings of fMRI-identified category-selective cortex. A, Coronal slice showing the recording chamber and a single electrode penetration (indicated by arrow) targeting category-selective cortex (left). High-resolution coronal (middle) and axial (right) slices showing a representation of the electrode tip, terminating in the inferior bank of the STS (marked by red and indicated by arrows). B, Top-down view of the recording chamber with the fMRI-identified category-selectivity in the inferior bank of the STS indicated as a function of grid hole, for monkeys S (left) and W (right). Thick white outlines indicate sampled grid locations. A, Anterior; M, medial.

  • Figure 3.
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    Figure 3.

    Response profiles of neurons in IT cortex. Individual examples of neurons exhibiting either excitatory (A), suppressed (B), or both excitatory and suppressed (C) responses to visual stimuli. Spike–density functions (top) show the mean response for all stimuli from a given category. Each row of the color plots represents the mean response to each of the 80 stimuli presented (minimum of 3 repetitions/stimulus). sp/s, Spikes per second.

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    Figure 4.

    Excitatory and suppressed responses to visual stimuli. Normalized excitatory (left) and suppressed (right) responses to each of the 80 visual stimuli for monkey S (A) and W (B). Each row represents an individual neuron, ordered according to the category of stimuli that evoked the strongest (or weakest, in the case of the suppressed responses) response. Note that neurons that exhibited both excitatory and suppressed responses appear in both panels. Response magnitudes were calculated by first subtracting out the baseline activity (average activity, −200 to 50 ms surrounding stimulus onset) and normalizing the activity to the maximum firing rate of the neuron.

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    Figure 5.

    Properties of neurons in IT cortex. A, Excitatory responses to each of the four categories tested for each subpopulation of visually responsive neurons (i.e., face neurons, body-part neurons, etc.). Responses are normalized to the maximum firing rate of each neuron to illustrate the consistency in the pattern of responses to the nonpreferred categories. B, Average CSIs (see Materials and Methods) for each subpopulation of neurons. This analysis compares the degree of selectivity for each subpopulation of neurons with the associated preferred stimulus category. CSI values reflect the degree to which a given group of neurons is selective for their preferred category (e.g., faces for face neurons, body parts for body-part neurons, etc.). Greater CSI values indicate larger differences between the response to the preferred category of a given neuron versus the average of the other three categories. Thus, the red bar indicates to what degree face neurons are selective for faces, the yellow bar indicates to what degree body-part neurons are selective for body parts, etc. Note that CSI values were calculated for each neuron using the raw (i.e., not normalized) response magnitudes. C, Normalized suppressed responses to each of the four categories tested for each subpopulation of neurons (i.e., face neurons, body-part neurons, etc.). By definition, suppressed responses must have some baseline activity. Therefore, to show how the different responses relate to one another, in this case, responses are normalized to the average baseline activity for each neuron. Note that neurons that exhibited both excitatory and suppressed responses appear in both analyses. D, Average absolute category selectivity indices for each subpopulation of neurons (values presented unsigned to ease comparison to excitatory responses). As above, CSI values were calculated using the raw response magnitudes. E, Average response latencies for each subpopulation of neurons to their preferred category (i.e., the average response latency to face stimuli for face neurons, the average response latency to body-part stimuli for body-part neurons, etc.). Error bars indicate SEM. *p < 0.05, ***p < 0.005.

  • Figure 6.
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    Figure 6.

    Distribution of category-selectivity across IT cortex. A, B, Top-down view of the recording chambers for monkeys S (A) and W (B), showing the different fMRI-identified category-selective regions (reproduced from Fig. 1B). We identified four subdivisions in monkey S and 5 in monkey W, each corresponding to a single fMRI-identified category-selective region accessible from our recording chambers (indicated by the shaded regions). Below each map are the corresponding distributions of excitatory (left column) and suppressed (right column) responses among individual neurons recorded from within each of these subdivisions (note that neurons that exhibited both excitatory and suppressed responses appear in both columns). Next to each are the results of individual χ2 tests comparing the actual distributions with a hypothetical, evenly distributed, allotment, based on the total number of neurons sampled from each subdivision. A, Anterior; M, medial. *p < 0.05, ***p < 0.005.

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    Figure 7.

    Comparing neuronal distributions within versus outside fMRI-identified category-selective regions. A comparison of the relative proportions of neurons that prefer a given category (e.g., face neurons, body-part neurons, etc.) found within, near, or outside the corresponding fMRI-identified category-selective region (e.g., face-selective region). The accompanying top-down views of the recording chambers indicate which recording site (marked by the circles) fall within each area: colored sites correspond to those defined as “In” the given fMRI region; shaded sites correspond to those defined as “Near” the given fMRI region (fall within 1–4 mm from the edge of the fMRI region); all remaining sites correspond to those defined as “Out” of the given fMRI region. ant, Anterior; post, posterior. Note that the sites defined as Out for the anterior face region do not include those found in the posterior face region and vice versa. The color within each recording site corresponds to the fMRI-based category selectivity predicted for that location (Fig. 1D). Only excitatory responses are considered for this analysis. A, Anterior; M, medial.

  • Figure 8.
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    Figure 8.

    Contrasting fMRI and neuronal responses. A, B, fMRI time series and corresponding neuronal distribution and population neuronal responses for the anterior face-selective region in monkey W (A) and the object-selective region in monkey S (B). Time series data are averaged across all runs, shown interleaved with the scrambled condition (see Materials and Methods). Population neuronal responses are shown as the average spike–density functions (±SEM). Inset shows the neuronal distributions (reproduced from Fig. 6), including the total number of neurons contributing to the population spike–density functions. C, Correlation between the category selectivity based on the fMRI data and that for the neuronal responses within each fMRI-identified category-selective region. Each region contributed four points, one for each category. Thus, the selectivity for faces (based on fMRI) is contrasted with the selectivity for faces (based on the average face selectivity across all neurons found within that region). Both Pearson's and Spearman's (SC) correlation coefficients (and corresponding p values) are shown to contrast linear versus rank analysis methods. D, Correlation between the magnitude of the fMRI response to each category (defined as the peak signal change across the block) within a given fMRI-identified category-selective region and the average category response among all neurons found within that region.

  • Figure 9.
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    Figure 9.

    Properties of neurons found within versus outside fMRI-identified category-selective regions. A, B, Average CSI (see Materials and Methods) for neurons that prefer a given category (e.g., face neurons, body-part neurons, etc.) found within versus outside the corresponding fMRI-identified category-selective region (e.g., face-selective region, body-part-selective region). In the case of face neurons, data are grouped across the two fMRI face-selective regions (anterior and posterior). Only excitatory responses are considered for these analyses. *p < 0.05.

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    Table 1.

    Response distribution in IT cortex

    Category-selective* (n)Not category-selective (n)Total (n)
    Visually responsive
        Excitatory response only379 (72%)150 (28%)529 (42%)
            Faces15849
            Body parts7926
            Objects9042
            Places5233
        Suppressed response only148 (59%)102 (41%)250 (20%)
            Faces8441
            Body parts2318
            Objects1618
            Places2525
        Both (excite)196 (100%)0 (0%)196 (15%)
            Faces66
            Body parts69
            Objects37
            Places24
        Both (suppress)196 (100%)0 (0%)
            Faces104
            Body parts35
            Objects19
            Places38
    Not visually responsive297 (23%)
        Total1272
    • *p < 0.05, main effect of stimulus category (ANOVA).

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    Table 2.

    Summary of stimulus selectivity among IT neurons

    Visually responsiveStimulus-selectivea (n)Not stimulus-selective (n)Total (n)
    Excitatory responses*
        Faces42 (15%)231273
        Body parts78 (45%)96174
        Objects70 (41%)99169
        Places25 (23%)84109
        Total725
    Suppressed responses*
        Faces27 (12%)202229
        Body parts11 (14%)6576
        Objects11 (21%)4253
        Places7 (8%)8188
        Total446
    • aIncludes neurons that exhibit both excitatory and suppressed responses (see Fig. 3C).

    • *p < 0.05, main effect of stimulus identity (ANOVA).

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The Journal of Neuroscience: 31 (34)
Journal of Neuroscience
Vol. 31, Issue 34
24 Aug 2011
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Relationship between Functional Magnetic Resonance Imaging-Identified Regions and Neuronal Category Selectivity
Andrew H. Bell, Nicholas J. Malecek, Elyse L. Morin, Fadila Hadj-Bouziane, Roger B. H. Tootell, Leslie G. Ungerleider
Journal of Neuroscience 24 August 2011, 31 (34) 12229-12240; DOI: 10.1523/JNEUROSCI.5865-10.2011

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Relationship between Functional Magnetic Resonance Imaging-Identified Regions and Neuronal Category Selectivity
Andrew H. Bell, Nicholas J. Malecek, Elyse L. Morin, Fadila Hadj-Bouziane, Roger B. H. Tootell, Leslie G. Ungerleider
Journal of Neuroscience 24 August 2011, 31 (34) 12229-12240; DOI: 10.1523/JNEUROSCI.5865-10.2011
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