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Broad and narrow conceptual tuning in the human frontal lobes.

Gotts SJ, Milleville SC, Bellgowan PS, Martin A - Cereb. Cortex (2010)

Bottom Line: Broad superordinate conceptual information was represented as early as extrastriate and posterior ventral temporal cortex.Separate sites within prefrontal cortex represented broad and narrow conceptual tuning, with more anterior sites tuned narrowly to close conceptual associates in a manner that was invariant to stimulus form/position and that matched independent similarity ratings of the stimuli.The combination of broad and narrow conceptual tuning within prefrontal cortex may support flexible selection, retrieval, and classification of objects at different levels of categorical abstraction.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA. gottss@mail.nih.gov

ABSTRACT
Previous work has implicated prefrontal cortices in selecting among and retrieving conceptual information stored elsewhere. However, recent neurophysiological work in monkeys suggests that prefrontal cortex may play a more direct role in representing conceptual information in a flexible context-specific manner. Here, we investigate the nature of visual object representations from perceptual to conceptual levels in an unbiased data-driven manner using a functional magnetic resonance imaging adaptation paradigm with pictures of animals. Throughout much of occipital cortex, activity was highly sensitive to changes in 2D stimulus form, consistent with tuning to form and position within retinotopic coordinates and matching an automated measure of shape similarity. Broad superordinate conceptual information was represented as early as extrastriate and posterior ventral temporal cortex. These regions were not completely invariant to form, suggesting that form similarity remains an important organizational constraint into the temporal cortex. Separate sites within prefrontal cortex represented broad and narrow conceptual tuning, with more anterior sites tuned narrowly to close conceptual associates in a manner that was invariant to stimulus form/position and that matched independent similarity ratings of the stimuli. The combination of broad and narrow conceptual tuning within prefrontal cortex may support flexible selection, retrieval, and classification of objects at different levels of categorical abstraction.

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Conceptual distance manipulation, similarity ratings, and stimulus form similarity. (A) Repeated anchor pictures in the fMRI experiment were followed by a single deviant picture sharing 1 of 5 levels of conceptual distance from the anchor. Pictures could be 1) identical (e.g., identical “cow” picture), 2) same concept (e.g., different exemplar picture of a cow), 3) highly related conceptually to the anchor (e.g., another farm animal such as a “donkey”), 4) medium related (e.g., another land animal such as an “elephant”), or 5) low related (e.g., both anchor and deviant are living things, such as cow and “lobster”). Four unique anchor pictures were used throughout the experiment (cow, lion, bass fish, and shark, as shown in the left-most column), and each of the deviant levels, with the exception of Level 1 (identical), employed multiple distinct examples (4 or more) of the relation for each anchor (see Supplementary Material for complete list). (B) A ratings study (n = 7 subjects) confirmed that the 5 levels of conceptual distance used in the fMRI experiment were significantly different from one another. Subjects were shown anchor–deviant stimuli in pairs presented simultaneously on the screen (one left, one right) and asked to rate how similar the objects were on a scale from 1 to 5 (5 = very similar). Rated similarity of the anchor–deviant pairs decreased as a function of increasing conceptual distance (Levels 1–5). (C) Differences in visual stimulus form between anchor–deviant pairs in the 5 deviant conditions. Pairwise distance values (D) were calculated from an automated shape similarity algorithm (Belongie et al. 2002). Distances were small to Deviant Level 1 (identical to anchor) and large to the other deviant conditions, with little variation among them. Distance values have an inverted scale relative to the similarity values shown in (B).
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fig2: Conceptual distance manipulation, similarity ratings, and stimulus form similarity. (A) Repeated anchor pictures in the fMRI experiment were followed by a single deviant picture sharing 1 of 5 levels of conceptual distance from the anchor. Pictures could be 1) identical (e.g., identical “cow” picture), 2) same concept (e.g., different exemplar picture of a cow), 3) highly related conceptually to the anchor (e.g., another farm animal such as a “donkey”), 4) medium related (e.g., another land animal such as an “elephant”), or 5) low related (e.g., both anchor and deviant are living things, such as cow and “lobster”). Four unique anchor pictures were used throughout the experiment (cow, lion, bass fish, and shark, as shown in the left-most column), and each of the deviant levels, with the exception of Level 1 (identical), employed multiple distinct examples (4 or more) of the relation for each anchor (see Supplementary Material for complete list). (B) A ratings study (n = 7 subjects) confirmed that the 5 levels of conceptual distance used in the fMRI experiment were significantly different from one another. Subjects were shown anchor–deviant stimuli in pairs presented simultaneously on the screen (one left, one right) and asked to rate how similar the objects were on a scale from 1 to 5 (5 = very similar). Rated similarity of the anchor–deviant pairs decreased as a function of increasing conceptual distance (Levels 1–5). (C) Differences in visual stimulus form between anchor–deviant pairs in the 5 deviant conditions. Pairwise distance values (D) were calculated from an automated shape similarity algorithm (Belongie et al. 2002). Distances were small to Deviant Level 1 (identical to anchor) and large to the other deviant conditions, with little variation among them. Distance values have an inverted scale relative to the similarity values shown in (B).

Mentions: We manipulated the conceptual relationship between anchor and deviant pictures in a graded manner at 5 levels, ranging from identical in stimulus form and concept (Level 1: identical picture to anchor) to same concept (Level 2: different exemplar picture of the same type of animal with a reversed left/right orientation) to different concepts with varying degrees of similarity (Levels 3–5: high-, medium-, and low-related concepts, see Fig. 2A for examples). This allowed us to measure recovery from adaptation and conceptual tuning along 5 data points in each fMRI voxel, spanning Rosch’s taxonomy of basic- and superordinate-level conceptual categories (Rosch et al. 1976; Rosch 1978). We anticipated that recovery curves could cover the full range of tuning from 2D stimulus form up to conceptual categories. At the perceptual extreme of tuning to stimulus form, recovery might show an “image-selective” pattern, with continued adaptation only to an identical picture and full recovery to any picture with different stimulus form in 2D retinotopic coordinates, including different exemplars of the same type of animal that have been reversed in their left/right orientation. At the conceptual extreme, recovery might show a “category-selective” pattern with continued adaptation to any object within the same superordinate-level category (either “land animals” or “sea creatures”) and full recovery to any object from a different superordinate category. Within the scope of these perceptual (image selective) and conceptual (category selective) extremes, we can make the following predictions about tuning to visual objects within visually responsive cortical regions:


Broad and narrow conceptual tuning in the human frontal lobes.

Gotts SJ, Milleville SC, Bellgowan PS, Martin A - Cereb. Cortex (2010)

Conceptual distance manipulation, similarity ratings, and stimulus form similarity. (A) Repeated anchor pictures in the fMRI experiment were followed by a single deviant picture sharing 1 of 5 levels of conceptual distance from the anchor. Pictures could be 1) identical (e.g., identical “cow” picture), 2) same concept (e.g., different exemplar picture of a cow), 3) highly related conceptually to the anchor (e.g., another farm animal such as a “donkey”), 4) medium related (e.g., another land animal such as an “elephant”), or 5) low related (e.g., both anchor and deviant are living things, such as cow and “lobster”). Four unique anchor pictures were used throughout the experiment (cow, lion, bass fish, and shark, as shown in the left-most column), and each of the deviant levels, with the exception of Level 1 (identical), employed multiple distinct examples (4 or more) of the relation for each anchor (see Supplementary Material for complete list). (B) A ratings study (n = 7 subjects) confirmed that the 5 levels of conceptual distance used in the fMRI experiment were significantly different from one another. Subjects were shown anchor–deviant stimuli in pairs presented simultaneously on the screen (one left, one right) and asked to rate how similar the objects were on a scale from 1 to 5 (5 = very similar). Rated similarity of the anchor–deviant pairs decreased as a function of increasing conceptual distance (Levels 1–5). (C) Differences in visual stimulus form between anchor–deviant pairs in the 5 deviant conditions. Pairwise distance values (D) were calculated from an automated shape similarity algorithm (Belongie et al. 2002). Distances were small to Deviant Level 1 (identical to anchor) and large to the other deviant conditions, with little variation among them. Distance values have an inverted scale relative to the similarity values shown in (B).
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fig2: Conceptual distance manipulation, similarity ratings, and stimulus form similarity. (A) Repeated anchor pictures in the fMRI experiment were followed by a single deviant picture sharing 1 of 5 levels of conceptual distance from the anchor. Pictures could be 1) identical (e.g., identical “cow” picture), 2) same concept (e.g., different exemplar picture of a cow), 3) highly related conceptually to the anchor (e.g., another farm animal such as a “donkey”), 4) medium related (e.g., another land animal such as an “elephant”), or 5) low related (e.g., both anchor and deviant are living things, such as cow and “lobster”). Four unique anchor pictures were used throughout the experiment (cow, lion, bass fish, and shark, as shown in the left-most column), and each of the deviant levels, with the exception of Level 1 (identical), employed multiple distinct examples (4 or more) of the relation for each anchor (see Supplementary Material for complete list). (B) A ratings study (n = 7 subjects) confirmed that the 5 levels of conceptual distance used in the fMRI experiment were significantly different from one another. Subjects were shown anchor–deviant stimuli in pairs presented simultaneously on the screen (one left, one right) and asked to rate how similar the objects were on a scale from 1 to 5 (5 = very similar). Rated similarity of the anchor–deviant pairs decreased as a function of increasing conceptual distance (Levels 1–5). (C) Differences in visual stimulus form between anchor–deviant pairs in the 5 deviant conditions. Pairwise distance values (D) were calculated from an automated shape similarity algorithm (Belongie et al. 2002). Distances were small to Deviant Level 1 (identical to anchor) and large to the other deviant conditions, with little variation among them. Distance values have an inverted scale relative to the similarity values shown in (B).
Mentions: We manipulated the conceptual relationship between anchor and deviant pictures in a graded manner at 5 levels, ranging from identical in stimulus form and concept (Level 1: identical picture to anchor) to same concept (Level 2: different exemplar picture of the same type of animal with a reversed left/right orientation) to different concepts with varying degrees of similarity (Levels 3–5: high-, medium-, and low-related concepts, see Fig. 2A for examples). This allowed us to measure recovery from adaptation and conceptual tuning along 5 data points in each fMRI voxel, spanning Rosch’s taxonomy of basic- and superordinate-level conceptual categories (Rosch et al. 1976; Rosch 1978). We anticipated that recovery curves could cover the full range of tuning from 2D stimulus form up to conceptual categories. At the perceptual extreme of tuning to stimulus form, recovery might show an “image-selective” pattern, with continued adaptation only to an identical picture and full recovery to any picture with different stimulus form in 2D retinotopic coordinates, including different exemplars of the same type of animal that have been reversed in their left/right orientation. At the conceptual extreme, recovery might show a “category-selective” pattern with continued adaptation to any object within the same superordinate-level category (either “land animals” or “sea creatures”) and full recovery to any object from a different superordinate category. Within the scope of these perceptual (image selective) and conceptual (category selective) extremes, we can make the following predictions about tuning to visual objects within visually responsive cortical regions:

Bottom Line: Broad superordinate conceptual information was represented as early as extrastriate and posterior ventral temporal cortex.Separate sites within prefrontal cortex represented broad and narrow conceptual tuning, with more anterior sites tuned narrowly to close conceptual associates in a manner that was invariant to stimulus form/position and that matched independent similarity ratings of the stimuli.The combination of broad and narrow conceptual tuning within prefrontal cortex may support flexible selection, retrieval, and classification of objects at different levels of categorical abstraction.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA. gottss@mail.nih.gov

ABSTRACT
Previous work has implicated prefrontal cortices in selecting among and retrieving conceptual information stored elsewhere. However, recent neurophysiological work in monkeys suggests that prefrontal cortex may play a more direct role in representing conceptual information in a flexible context-specific manner. Here, we investigate the nature of visual object representations from perceptual to conceptual levels in an unbiased data-driven manner using a functional magnetic resonance imaging adaptation paradigm with pictures of animals. Throughout much of occipital cortex, activity was highly sensitive to changes in 2D stimulus form, consistent with tuning to form and position within retinotopic coordinates and matching an automated measure of shape similarity. Broad superordinate conceptual information was represented as early as extrastriate and posterior ventral temporal cortex. These regions were not completely invariant to form, suggesting that form similarity remains an important organizational constraint into the temporal cortex. Separate sites within prefrontal cortex represented broad and narrow conceptual tuning, with more anterior sites tuned narrowly to close conceptual associates in a manner that was invariant to stimulus form/position and that matched independent similarity ratings of the stimuli. The combination of broad and narrow conceptual tuning within prefrontal cortex may support flexible selection, retrieval, and classification of objects at different levels of categorical abstraction.

Show MeSH