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Stimulus set meaningfulness and neurophysiological differentiation: a functional magnetic resonance imaging study.

Boly M, Sasai S, Gosseries O, Oizumi M, Casali A, Massimini M, Tononi G - PLoS ONE (2015)

Bottom Line: We tested this hypothesis by quantifying the differentiation of brain activity patterns in response to a movie sequence, to the same movie scrambled in time, and to 'TV noise', where the pixels from each movie frame were scrambled in space.Stimulus set meaningfulness was also associated with higher information integration among cortical regions.These results suggest that the differentiation of neural responses can be used to assess the meaningfulness of a given set of stimuli for a given subject, without the need to identify the features and categories that are relevant to the subject, nor the precise location of selective neural responses.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of Wisconsin, Madison, Wisconsin, United States of America; Department of Psychiatry, University of Wisconsin, Madison, Wisconsin, United States of America.

ABSTRACT
A meaningful set of stimuli, such as a sequence of frames from a movie, triggers a set of different experiences. By contrast, a meaningless set of stimuli, such as a sequence of 'TV noise' frames, triggers always the same experience--of seeing 'TV noise'--even though the stimuli themselves are as different from each other as the movie frames. We reasoned that the differentiation of cortical responses underlying the subject's experiences, as measured by Lempel-Ziv complexity (incompressibility) of functional MRI images, should reflect the overall meaningfulness of a set of stimuli for the subject, rather than differences among the stimuli. We tested this hypothesis by quantifying the differentiation of brain activity patterns in response to a movie sequence, to the same movie scrambled in time, and to 'TV noise', where the pixels from each movie frame were scrambled in space. While overall cortical activation was strong and widespread in all conditions, the differentiation (Lempel-Ziv complexity) of brain activation patterns was correlated with the meaningfulness of the stimulus set, being highest in the movie condition, intermediate in the scrambled movie condition, and minimal for 'TV noise'. Stimulus set meaningfulness was also associated with higher information integration among cortical regions. These results suggest that the differentiation of neural responses can be used to assess the meaningfulness of a given set of stimuli for a given subject, without the need to identify the features and categories that are relevant to the subject, nor the precise location of selective neural responses.

No MeSH data available.


Related in: MedlinePlus

Experimental paradigm.Left panel: Schematic representation of a human brain with 3 representative voxels whose fMRI BOLD activity will be measured in a block design analysis and in a differentiation analysis. The red voxel is known to respond to faces, the orange voxel to places, and the green voxel has unknown selectivity. The colored traces in the right side panels represent the expected BOLD signal of these representative voxels during the fMRI experiments. Right, Top Panel: in the block design paradigm, 20 seconds sequences of movie, scrambled movie, or ‘TV noise’ are presented in alternation with a black screen baseline. The block design analysis is expected to reveal significant increases in the mean activity of the three pictured voxels for each of the three stimulus sequences compared to the black screen baseline. Bottom Panel: in the differentiation analysis paradigm, a 4 min sequence of movie, scrambled movie or ‘TV noise’ is presented to the subjects, each sequence repeated 30 times across different scanning sessions (only 3 of these repetitions are depicted, corresponding to 3 BOLD activity traces per voxel). In all three conditions, we expect an overall activation with respect to the black screen baseline similar to that in the block design paradigm. However, unlike the block design analysis, the differentiation analysis focuses on systematic time-locked increases or decreases in activity with respect to: i) each voxel’s the black screen baseline (dashed black line); ii) each voxel’s mean activity during the 4 min sequence. Movie sequence: for each voxel, we expect systematic time-locked increases and decreases of activity across the session (neurophysiological differentiation over time); moreover, we expect different voxels to show different patterns of systematic activations/deactivations in response to different movie frames (neurophysiological differentiation over space). Altogether, high neurophysiological differentiation in space and time (many different spatio-temporal patterns) is expected to go along high phenomenological differentiation (many different experiences). Scrambled movie sequence: we expect intermediate levels of neurophysiological differentiation, corresponding to intermediate levels of phenomenological differentiation. TV noise sequence: we expect no or minimal systematic time-locked incease or decreases in activity. Low neurophysiological differentiation (a single, unchanging pattern of activation/deactivation) corresponds to low phenomenological differentiation (a single, unchanging experience of ‘TV noise’). Spontaneous fluctuations in BOLD activity from scan to scan are also expected in the ‘TV noise’ session, but they will not be time locked to specific ‘TV noise’ frames, which cortical regions treat as equivalent. For copyright reasons, all movie pictures were replaced in Figures by numbered blank frames representing their order of appearance in the movie.
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pone.0125337.g001: Experimental paradigm.Left panel: Schematic representation of a human brain with 3 representative voxels whose fMRI BOLD activity will be measured in a block design analysis and in a differentiation analysis. The red voxel is known to respond to faces, the orange voxel to places, and the green voxel has unknown selectivity. The colored traces in the right side panels represent the expected BOLD signal of these representative voxels during the fMRI experiments. Right, Top Panel: in the block design paradigm, 20 seconds sequences of movie, scrambled movie, or ‘TV noise’ are presented in alternation with a black screen baseline. The block design analysis is expected to reveal significant increases in the mean activity of the three pictured voxels for each of the three stimulus sequences compared to the black screen baseline. Bottom Panel: in the differentiation analysis paradigm, a 4 min sequence of movie, scrambled movie or ‘TV noise’ is presented to the subjects, each sequence repeated 30 times across different scanning sessions (only 3 of these repetitions are depicted, corresponding to 3 BOLD activity traces per voxel). In all three conditions, we expect an overall activation with respect to the black screen baseline similar to that in the block design paradigm. However, unlike the block design analysis, the differentiation analysis focuses on systematic time-locked increases or decreases in activity with respect to: i) each voxel’s the black screen baseline (dashed black line); ii) each voxel’s mean activity during the 4 min sequence. Movie sequence: for each voxel, we expect systematic time-locked increases and decreases of activity across the session (neurophysiological differentiation over time); moreover, we expect different voxels to show different patterns of systematic activations/deactivations in response to different movie frames (neurophysiological differentiation over space). Altogether, high neurophysiological differentiation in space and time (many different spatio-temporal patterns) is expected to go along high phenomenological differentiation (many different experiences). Scrambled movie sequence: we expect intermediate levels of neurophysiological differentiation, corresponding to intermediate levels of phenomenological differentiation. TV noise sequence: we expect no or minimal systematic time-locked incease or decreases in activity. Low neurophysiological differentiation (a single, unchanging pattern of activation/deactivation) corresponds to low phenomenological differentiation (a single, unchanging experience of ‘TV noise’). Spontaneous fluctuations in BOLD activity from scan to scan are also expected in the ‘TV noise’ session, but they will not be time locked to specific ‘TV noise’ frames, which cortical regions treat as equivalent. For copyright reasons, all movie pictures were replaced in Figures by numbered blank frames representing their order of appearance in the movie.

Mentions: Fig 1, Top Panel, displays the experimental paradigm used for block design analysis. In this paradigm, 20 sec sequences of movie, scrambled movie, or ‘TV noise’ were presented in alternation with a black screen baseline. The block design analysis was expected to show significant increases in the mean activity of many voxels for each of the three stimulus sequences compared to the black screen baseline.


Stimulus set meaningfulness and neurophysiological differentiation: a functional magnetic resonance imaging study.

Boly M, Sasai S, Gosseries O, Oizumi M, Casali A, Massimini M, Tononi G - PLoS ONE (2015)

Experimental paradigm.Left panel: Schematic representation of a human brain with 3 representative voxels whose fMRI BOLD activity will be measured in a block design analysis and in a differentiation analysis. The red voxel is known to respond to faces, the orange voxel to places, and the green voxel has unknown selectivity. The colored traces in the right side panels represent the expected BOLD signal of these representative voxels during the fMRI experiments. Right, Top Panel: in the block design paradigm, 20 seconds sequences of movie, scrambled movie, or ‘TV noise’ are presented in alternation with a black screen baseline. The block design analysis is expected to reveal significant increases in the mean activity of the three pictured voxels for each of the three stimulus sequences compared to the black screen baseline. Bottom Panel: in the differentiation analysis paradigm, a 4 min sequence of movie, scrambled movie or ‘TV noise’ is presented to the subjects, each sequence repeated 30 times across different scanning sessions (only 3 of these repetitions are depicted, corresponding to 3 BOLD activity traces per voxel). In all three conditions, we expect an overall activation with respect to the black screen baseline similar to that in the block design paradigm. However, unlike the block design analysis, the differentiation analysis focuses on systematic time-locked increases or decreases in activity with respect to: i) each voxel’s the black screen baseline (dashed black line); ii) each voxel’s mean activity during the 4 min sequence. Movie sequence: for each voxel, we expect systematic time-locked increases and decreases of activity across the session (neurophysiological differentiation over time); moreover, we expect different voxels to show different patterns of systematic activations/deactivations in response to different movie frames (neurophysiological differentiation over space). Altogether, high neurophysiological differentiation in space and time (many different spatio-temporal patterns) is expected to go along high phenomenological differentiation (many different experiences). Scrambled movie sequence: we expect intermediate levels of neurophysiological differentiation, corresponding to intermediate levels of phenomenological differentiation. TV noise sequence: we expect no or minimal systematic time-locked incease or decreases in activity. Low neurophysiological differentiation (a single, unchanging pattern of activation/deactivation) corresponds to low phenomenological differentiation (a single, unchanging experience of ‘TV noise’). Spontaneous fluctuations in BOLD activity from scan to scan are also expected in the ‘TV noise’ session, but they will not be time locked to specific ‘TV noise’ frames, which cortical regions treat as equivalent. For copyright reasons, all movie pictures were replaced in Figures by numbered blank frames representing their order of appearance in the movie.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4430458&req=5

pone.0125337.g001: Experimental paradigm.Left panel: Schematic representation of a human brain with 3 representative voxels whose fMRI BOLD activity will be measured in a block design analysis and in a differentiation analysis. The red voxel is known to respond to faces, the orange voxel to places, and the green voxel has unknown selectivity. The colored traces in the right side panels represent the expected BOLD signal of these representative voxels during the fMRI experiments. Right, Top Panel: in the block design paradigm, 20 seconds sequences of movie, scrambled movie, or ‘TV noise’ are presented in alternation with a black screen baseline. The block design analysis is expected to reveal significant increases in the mean activity of the three pictured voxels for each of the three stimulus sequences compared to the black screen baseline. Bottom Panel: in the differentiation analysis paradigm, a 4 min sequence of movie, scrambled movie or ‘TV noise’ is presented to the subjects, each sequence repeated 30 times across different scanning sessions (only 3 of these repetitions are depicted, corresponding to 3 BOLD activity traces per voxel). In all three conditions, we expect an overall activation with respect to the black screen baseline similar to that in the block design paradigm. However, unlike the block design analysis, the differentiation analysis focuses on systematic time-locked increases or decreases in activity with respect to: i) each voxel’s the black screen baseline (dashed black line); ii) each voxel’s mean activity during the 4 min sequence. Movie sequence: for each voxel, we expect systematic time-locked increases and decreases of activity across the session (neurophysiological differentiation over time); moreover, we expect different voxels to show different patterns of systematic activations/deactivations in response to different movie frames (neurophysiological differentiation over space). Altogether, high neurophysiological differentiation in space and time (many different spatio-temporal patterns) is expected to go along high phenomenological differentiation (many different experiences). Scrambled movie sequence: we expect intermediate levels of neurophysiological differentiation, corresponding to intermediate levels of phenomenological differentiation. TV noise sequence: we expect no or minimal systematic time-locked incease or decreases in activity. Low neurophysiological differentiation (a single, unchanging pattern of activation/deactivation) corresponds to low phenomenological differentiation (a single, unchanging experience of ‘TV noise’). Spontaneous fluctuations in BOLD activity from scan to scan are also expected in the ‘TV noise’ session, but they will not be time locked to specific ‘TV noise’ frames, which cortical regions treat as equivalent. For copyright reasons, all movie pictures were replaced in Figures by numbered blank frames representing their order of appearance in the movie.
Mentions: Fig 1, Top Panel, displays the experimental paradigm used for block design analysis. In this paradigm, 20 sec sequences of movie, scrambled movie, or ‘TV noise’ were presented in alternation with a black screen baseline. The block design analysis was expected to show significant increases in the mean activity of many voxels for each of the three stimulus sequences compared to the black screen baseline.

Bottom Line: We tested this hypothesis by quantifying the differentiation of brain activity patterns in response to a movie sequence, to the same movie scrambled in time, and to 'TV noise', where the pixels from each movie frame were scrambled in space.Stimulus set meaningfulness was also associated with higher information integration among cortical regions.These results suggest that the differentiation of neural responses can be used to assess the meaningfulness of a given set of stimuli for a given subject, without the need to identify the features and categories that are relevant to the subject, nor the precise location of selective neural responses.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of Wisconsin, Madison, Wisconsin, United States of America; Department of Psychiatry, University of Wisconsin, Madison, Wisconsin, United States of America.

ABSTRACT
A meaningful set of stimuli, such as a sequence of frames from a movie, triggers a set of different experiences. By contrast, a meaningless set of stimuli, such as a sequence of 'TV noise' frames, triggers always the same experience--of seeing 'TV noise'--even though the stimuli themselves are as different from each other as the movie frames. We reasoned that the differentiation of cortical responses underlying the subject's experiences, as measured by Lempel-Ziv complexity (incompressibility) of functional MRI images, should reflect the overall meaningfulness of a set of stimuli for the subject, rather than differences among the stimuli. We tested this hypothesis by quantifying the differentiation of brain activity patterns in response to a movie sequence, to the same movie scrambled in time, and to 'TV noise', where the pixels from each movie frame were scrambled in space. While overall cortical activation was strong and widespread in all conditions, the differentiation (Lempel-Ziv complexity) of brain activation patterns was correlated with the meaningfulness of the stimulus set, being highest in the movie condition, intermediate in the scrambled movie condition, and minimal for 'TV noise'. Stimulus set meaningfulness was also associated with higher information integration among cortical regions. These results suggest that the differentiation of neural responses can be used to assess the meaningfulness of a given set of stimuli for a given subject, without the need to identify the features and categories that are relevant to the subject, nor the precise location of selective neural responses.

No MeSH data available.


Related in: MedlinePlus