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Top-down modulation of visual processing and knowledge after 250 ms supports object constancy of category decisions.

Schendan HE, Ganis G - Front Psychol (2015)

Bottom Line: N3 impoverishment effects localized to both prefrontal and occipitotemporal cortex for real objects only.The N3 also showed knowledge effects by 230 ms that localized to occipitotemporal cortex.Finally, response activity in supplementary motor area during a posterior SW after 900 ms showed impoverishment effects that correlated with RTs.

View Article: PubMed Central - PubMed

Affiliation: School of Psychology, Cognition Institute, University of Plymouth Plymouth, UK.

ABSTRACT
People categorize objects more slowly when visual input is highly impoverished instead of optimal. While bottom-up models may explain a decision with optimal input, perceptual hypothesis testing (PHT) theories implicate top-down processes with impoverished input. Brain mechanisms and the time course of PHT are largely unknown. This event-related potential study used a neuroimaging paradigm that implicated prefrontal cortex in top-down modulation of occipitotemporal cortex. Subjects categorized more impoverished and less impoverished real and pseudo objects. PHT theories predict larger impoverishment effects for real than pseudo objects because top-down processes modulate knowledge only for real objects, but different PHT variants predict different timing. Consistent with parietal-prefrontal PHT variants, around 250 ms, the earliest impoverished real object interaction started on an N3 complex, which reflects interactive cortical activity for object cognition. N3 impoverishment effects localized to both prefrontal and occipitotemporal cortex for real objects only. The N3 also showed knowledge effects by 230 ms that localized to occipitotemporal cortex. Later effects reflected (a) word meaning in temporal cortex during the N400, (b) internal evaluation of prior decision and memory processes and secondary higher-order memory involving anterotemporal parts of a default mode network during posterior positivity (P600), and (c) response related activity in posterior cingulate during an anterior slow wave (SW) after 700 ms. Finally, response activity in supplementary motor area during a posterior SW after 900 ms showed impoverishment effects that correlated with RTs. Convergent evidence from studies of vision, memory, and mental imagery which reflects purely top-down inputs, indicates that the N3 reflects the critical top-down processes of PHT. A hybrid multiple-state interactive, PHT and decision theory best explains the visual constancy of object cognition.

No MeSH data available.


The sLORETA maps show estimated sources of the difference waves (Figure 7) between two conditions (impoverishment = MI minus LI; type = pseudo minus real) in the grand average ERPs. Maps shown superimposed on an inflated, canonical MNI152 (Colin) brain. Dark areas are sulci; light areas are gyri. L, left hemisphere; R, right hemisphere. Each brain shows standardized cortical current density distributions, and source activity reflects the location of differential source activity between conditions but not the direction of effects. Scale uses hot colors (red, yellow) for maximal current density value differences. (A–D)N3 Sources. sLORETA maps shown for the N3 from 300 to 400 ms on dorsal (top) and ventral (bottom) cortical surfaces. Estimated intracranial ERPs plotted on the left for prefrontal (MNI x y z coordinates −15 20 65) and occipitotemporal sources (55 −45 –25) between −100 and 500 ms. (A)N3 impoverishment sources for real objects. Occipitotemporal sources: inferior (BA 20, 60 −40 −20; BA 37, 55 −45 −25) and middle temporal (BA 21, 65 −35 −15; BA 20, 55 −40 −15), fusiform (BA 37, 50 −50 −25; BA 20, 55 −35 −25; BA 19, 45 −70 −20; BA 36, 45 −40 −25), middle occipital (BA 19, 50 −70 −15), lingual (BA 18, 15 −85 −20), and parahippocampal (BA 36, 40 −30 −25) gyri. Prefrontal sources: superior (BA 6, −15 20 65; BA 8, −25 30 55), middle (BA 6, −25 20 60; BA 9, −35 40 40), and inferior frontal (BA 47, 20 25 −20) gyri. (B)N3 impoverishment sources for pseudo objects. Same prefrontal sources as for real objects. (C)N3 object type sources for LI. Occipitotemporal sources: fusiform (BA 37, 55 −60 −20, −50 −60 −25; BA 36, 45 −40 −30; BA 19, −50 −70 −20), inferior temporal (BA 20, 50 −55 −20; −60 −55 −20), middle temporal (BA 37, 55 −55 −15, −55 −65 −15; BA 21, 65 −50 −10), middle occipital (BA 37, 50 −65 −15, −50 −65 −15; BA 19, 50 −75 −15), parahippocampal (BA 19, 35 −45 −10) gyri. (D)N3 object type sources for MI. Same occipitotemporal sources as for LI. (E–H)P600 and slow wave (SW) Sources. sLORETA maps shown for left medial (top) and ventral (bottom) cortical surfaces. OT, occipitotemporal cortex; AIT, anterior inferior temporal cortex; PCC, posterior cingulate cortex, including precuneus and cuneus. Estimated intracranial ERPs plotted for the voxel showing maximum impoverished-real-object effects from 300 to 400 ms (same as later) in OT (55, −45, −25), 500 to 700 ms in AIT (25, 0 −45), and 700 to 900 ms in PCC (0 −55, 65). (E)Late impoverishment sources for real objects. AIT sources (maximum BA 20, 25–30 −5 −45) occurred from 450 to 700 ms when the P600 peaks: middle (BA 21, 65 −30 −20) and inferior temporal (BA 20, 60 −35 −20), fusiform (BA 20, 55 −35 −25), parahippocampal (BA 36, 35 −25 −30; BA 35, 30 −25 −25), and other limbic structures (BA 20, 25 0 −45; BA 38, 25 5 −45; BA 36, 25 −5 −40; BA 28, 25 −10 −35). From 500 to 700 ms, limbic lobe dominated (BA 20/38, 25 0 −45), including parahippocampal gyrus (BA 35, 25 −15, −30). From 700 to 900 ms, impoverishment effects in anterotemporal cortex continued and appeared in medial posterior cortex around cingulate (BA 25, 0 5 −10; BA 31, −10 −45 40), cuneus (BA 17, 5 −100 −5), and precuneus (BA 7, 5 −60 65; −5 −50 50), and occipital extrastriate regions (BA 18, 0 −95 −15). The SW effect in PCC is active after 700 ms. (F)Late impoverishment sources for pseudo objects. P600-like wave in AIT and SW in PCC shown. (G)Late object type sources for LI, and (H)for MI: Occipitotemporal cortex only.
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Figure 8: The sLORETA maps show estimated sources of the difference waves (Figure 7) between two conditions (impoverishment = MI minus LI; type = pseudo minus real) in the grand average ERPs. Maps shown superimposed on an inflated, canonical MNI152 (Colin) brain. Dark areas are sulci; light areas are gyri. L, left hemisphere; R, right hemisphere. Each brain shows standardized cortical current density distributions, and source activity reflects the location of differential source activity between conditions but not the direction of effects. Scale uses hot colors (red, yellow) for maximal current density value differences. (A–D)N3 Sources. sLORETA maps shown for the N3 from 300 to 400 ms on dorsal (top) and ventral (bottom) cortical surfaces. Estimated intracranial ERPs plotted on the left for prefrontal (MNI x y z coordinates −15 20 65) and occipitotemporal sources (55 −45 –25) between −100 and 500 ms. (A)N3 impoverishment sources for real objects. Occipitotemporal sources: inferior (BA 20, 60 −40 −20; BA 37, 55 −45 −25) and middle temporal (BA 21, 65 −35 −15; BA 20, 55 −40 −15), fusiform (BA 37, 50 −50 −25; BA 20, 55 −35 −25; BA 19, 45 −70 −20; BA 36, 45 −40 −25), middle occipital (BA 19, 50 −70 −15), lingual (BA 18, 15 −85 −20), and parahippocampal (BA 36, 40 −30 −25) gyri. Prefrontal sources: superior (BA 6, −15 20 65; BA 8, −25 30 55), middle (BA 6, −25 20 60; BA 9, −35 40 40), and inferior frontal (BA 47, 20 25 −20) gyri. (B)N3 impoverishment sources for pseudo objects. Same prefrontal sources as for real objects. (C)N3 object type sources for LI. Occipitotemporal sources: fusiform (BA 37, 55 −60 −20, −50 −60 −25; BA 36, 45 −40 −30; BA 19, −50 −70 −20), inferior temporal (BA 20, 50 −55 −20; −60 −55 −20), middle temporal (BA 37, 55 −55 −15, −55 −65 −15; BA 21, 65 −50 −10), middle occipital (BA 37, 50 −65 −15, −50 −65 −15; BA 19, 50 −75 −15), parahippocampal (BA 19, 35 −45 −10) gyri. (D)N3 object type sources for MI. Same occipitotemporal sources as for LI. (E–H)P600 and slow wave (SW) Sources. sLORETA maps shown for left medial (top) and ventral (bottom) cortical surfaces. OT, occipitotemporal cortex; AIT, anterior inferior temporal cortex; PCC, posterior cingulate cortex, including precuneus and cuneus. Estimated intracranial ERPs plotted for the voxel showing maximum impoverished-real-object effects from 300 to 400 ms (same as later) in OT (55, −45, −25), 500 to 700 ms in AIT (25, 0 −45), and 700 to 900 ms in PCC (0 −55, 65). (E)Late impoverishment sources for real objects. AIT sources (maximum BA 20, 25–30 −5 −45) occurred from 450 to 700 ms when the P600 peaks: middle (BA 21, 65 −30 −20) and inferior temporal (BA 20, 60 −35 −20), fusiform (BA 20, 55 −35 −25), parahippocampal (BA 36, 35 −25 −30; BA 35, 30 −25 −25), and other limbic structures (BA 20, 25 0 −45; BA 38, 25 5 −45; BA 36, 25 −5 −40; BA 28, 25 −10 −35). From 500 to 700 ms, limbic lobe dominated (BA 20/38, 25 0 −45), including parahippocampal gyrus (BA 35, 25 −15, −30). From 700 to 900 ms, impoverishment effects in anterotemporal cortex continued and appeared in medial posterior cortex around cingulate (BA 25, 0 5 −10; BA 31, −10 −45 40), cuneus (BA 17, 5 −100 −5), and precuneus (BA 7, 5 −60 65; −5 −50 50), and occipital extrastriate regions (BA 18, 0 −95 −15). The SW effect in PCC is active after 700 ms. (F)Late impoverishment sources for pseudo objects. P600-like wave in AIT and SW in PCC shown. (G)Late object type sources for LI, and (H)for MI: Occipitotemporal cortex only.

Mentions: For the four difference waves (Figure 7), cortical sources were estimated. The main focus was the time of the N3 peak from 300 to 400 ms (Figures 8A–D). Sources of this impoverishment effect (MI vs. LI) for real objects localized to occipitotemporal and lateral prefrontal areas found with fMRI (Ganis et al., 2007), whereas, for pseudo objects, impoverishment differences localized only to prefrontal areas. Sources of the object type effects (real vs. pseudo) on both LI and MI trials were in occipitotemporal areas. Sources at other times were also estimated. At all times after 200 ms, type effects continued in the same occipitotemporal areas (Figures 8C,D,G,H). Impoverishment sources varied over time and with object type (Figures 8A,B,E,F). The 200 to 300 ms time during the P250/N250 component showed the same impoverished-real-object pattern of sources as the peak N3 time period. Later, from 400 to 500 ms when the N3 ends and the N400 peaks, impoverishment effects for real objects showed only the occipitotemporal source (see intracranial ERP in Figure 8A). Around 450 ms, the maximum source shifted to anterotemporal cortex for both real and pseudo objects, suggesting an additional contribution from this region to the N400. From 500 to 700 ms, the estimated intracranial ERP for the anterotemporal source resembled the scalp P600 impoverishment waveform, which is maximal at this time, and more mediotemporal sources also contributed (Figures 8E,F). From 700 to 900 ms when the late SW dominates, anterotemporal impoverishment activity continued only for real objects. In addition, for both object types, impoverishment effects now appeared in the posterior cingulate cortex (PCC; Figures 8E,F).


Top-down modulation of visual processing and knowledge after 250 ms supports object constancy of category decisions.

Schendan HE, Ganis G - Front Psychol (2015)

The sLORETA maps show estimated sources of the difference waves (Figure 7) between two conditions (impoverishment = MI minus LI; type = pseudo minus real) in the grand average ERPs. Maps shown superimposed on an inflated, canonical MNI152 (Colin) brain. Dark areas are sulci; light areas are gyri. L, left hemisphere; R, right hemisphere. Each brain shows standardized cortical current density distributions, and source activity reflects the location of differential source activity between conditions but not the direction of effects. Scale uses hot colors (red, yellow) for maximal current density value differences. (A–D)N3 Sources. sLORETA maps shown for the N3 from 300 to 400 ms on dorsal (top) and ventral (bottom) cortical surfaces. Estimated intracranial ERPs plotted on the left for prefrontal (MNI x y z coordinates −15 20 65) and occipitotemporal sources (55 −45 –25) between −100 and 500 ms. (A)N3 impoverishment sources for real objects. Occipitotemporal sources: inferior (BA 20, 60 −40 −20; BA 37, 55 −45 −25) and middle temporal (BA 21, 65 −35 −15; BA 20, 55 −40 −15), fusiform (BA 37, 50 −50 −25; BA 20, 55 −35 −25; BA 19, 45 −70 −20; BA 36, 45 −40 −25), middle occipital (BA 19, 50 −70 −15), lingual (BA 18, 15 −85 −20), and parahippocampal (BA 36, 40 −30 −25) gyri. Prefrontal sources: superior (BA 6, −15 20 65; BA 8, −25 30 55), middle (BA 6, −25 20 60; BA 9, −35 40 40), and inferior frontal (BA 47, 20 25 −20) gyri. (B)N3 impoverishment sources for pseudo objects. Same prefrontal sources as for real objects. (C)N3 object type sources for LI. Occipitotemporal sources: fusiform (BA 37, 55 −60 −20, −50 −60 −25; BA 36, 45 −40 −30; BA 19, −50 −70 −20), inferior temporal (BA 20, 50 −55 −20; −60 −55 −20), middle temporal (BA 37, 55 −55 −15, −55 −65 −15; BA 21, 65 −50 −10), middle occipital (BA 37, 50 −65 −15, −50 −65 −15; BA 19, 50 −75 −15), parahippocampal (BA 19, 35 −45 −10) gyri. (D)N3 object type sources for MI. Same occipitotemporal sources as for LI. (E–H)P600 and slow wave (SW) Sources. sLORETA maps shown for left medial (top) and ventral (bottom) cortical surfaces. OT, occipitotemporal cortex; AIT, anterior inferior temporal cortex; PCC, posterior cingulate cortex, including precuneus and cuneus. Estimated intracranial ERPs plotted for the voxel showing maximum impoverished-real-object effects from 300 to 400 ms (same as later) in OT (55, −45, −25), 500 to 700 ms in AIT (25, 0 −45), and 700 to 900 ms in PCC (0 −55, 65). (E)Late impoverishment sources for real objects. AIT sources (maximum BA 20, 25–30 −5 −45) occurred from 450 to 700 ms when the P600 peaks: middle (BA 21, 65 −30 −20) and inferior temporal (BA 20, 60 −35 −20), fusiform (BA 20, 55 −35 −25), parahippocampal (BA 36, 35 −25 −30; BA 35, 30 −25 −25), and other limbic structures (BA 20, 25 0 −45; BA 38, 25 5 −45; BA 36, 25 −5 −40; BA 28, 25 −10 −35). From 500 to 700 ms, limbic lobe dominated (BA 20/38, 25 0 −45), including parahippocampal gyrus (BA 35, 25 −15, −30). From 700 to 900 ms, impoverishment effects in anterotemporal cortex continued and appeared in medial posterior cortex around cingulate (BA 25, 0 5 −10; BA 31, −10 −45 40), cuneus (BA 17, 5 −100 −5), and precuneus (BA 7, 5 −60 65; −5 −50 50), and occipital extrastriate regions (BA 18, 0 −95 −15). The SW effect in PCC is active after 700 ms. (F)Late impoverishment sources for pseudo objects. P600-like wave in AIT and SW in PCC shown. (G)Late object type sources for LI, and (H)for MI: Occipitotemporal cortex only.
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Figure 8: The sLORETA maps show estimated sources of the difference waves (Figure 7) between two conditions (impoverishment = MI minus LI; type = pseudo minus real) in the grand average ERPs. Maps shown superimposed on an inflated, canonical MNI152 (Colin) brain. Dark areas are sulci; light areas are gyri. L, left hemisphere; R, right hemisphere. Each brain shows standardized cortical current density distributions, and source activity reflects the location of differential source activity between conditions but not the direction of effects. Scale uses hot colors (red, yellow) for maximal current density value differences. (A–D)N3 Sources. sLORETA maps shown for the N3 from 300 to 400 ms on dorsal (top) and ventral (bottom) cortical surfaces. Estimated intracranial ERPs plotted on the left for prefrontal (MNI x y z coordinates −15 20 65) and occipitotemporal sources (55 −45 –25) between −100 and 500 ms. (A)N3 impoverishment sources for real objects. Occipitotemporal sources: inferior (BA 20, 60 −40 −20; BA 37, 55 −45 −25) and middle temporal (BA 21, 65 −35 −15; BA 20, 55 −40 −15), fusiform (BA 37, 50 −50 −25; BA 20, 55 −35 −25; BA 19, 45 −70 −20; BA 36, 45 −40 −25), middle occipital (BA 19, 50 −70 −15), lingual (BA 18, 15 −85 −20), and parahippocampal (BA 36, 40 −30 −25) gyri. Prefrontal sources: superior (BA 6, −15 20 65; BA 8, −25 30 55), middle (BA 6, −25 20 60; BA 9, −35 40 40), and inferior frontal (BA 47, 20 25 −20) gyri. (B)N3 impoverishment sources for pseudo objects. Same prefrontal sources as for real objects. (C)N3 object type sources for LI. Occipitotemporal sources: fusiform (BA 37, 55 −60 −20, −50 −60 −25; BA 36, 45 −40 −30; BA 19, −50 −70 −20), inferior temporal (BA 20, 50 −55 −20; −60 −55 −20), middle temporal (BA 37, 55 −55 −15, −55 −65 −15; BA 21, 65 −50 −10), middle occipital (BA 37, 50 −65 −15, −50 −65 −15; BA 19, 50 −75 −15), parahippocampal (BA 19, 35 −45 −10) gyri. (D)N3 object type sources for MI. Same occipitotemporal sources as for LI. (E–H)P600 and slow wave (SW) Sources. sLORETA maps shown for left medial (top) and ventral (bottom) cortical surfaces. OT, occipitotemporal cortex; AIT, anterior inferior temporal cortex; PCC, posterior cingulate cortex, including precuneus and cuneus. Estimated intracranial ERPs plotted for the voxel showing maximum impoverished-real-object effects from 300 to 400 ms (same as later) in OT (55, −45, −25), 500 to 700 ms in AIT (25, 0 −45), and 700 to 900 ms in PCC (0 −55, 65). (E)Late impoverishment sources for real objects. AIT sources (maximum BA 20, 25–30 −5 −45) occurred from 450 to 700 ms when the P600 peaks: middle (BA 21, 65 −30 −20) and inferior temporal (BA 20, 60 −35 −20), fusiform (BA 20, 55 −35 −25), parahippocampal (BA 36, 35 −25 −30; BA 35, 30 −25 −25), and other limbic structures (BA 20, 25 0 −45; BA 38, 25 5 −45; BA 36, 25 −5 −40; BA 28, 25 −10 −35). From 500 to 700 ms, limbic lobe dominated (BA 20/38, 25 0 −45), including parahippocampal gyrus (BA 35, 25 −15, −30). From 700 to 900 ms, impoverishment effects in anterotemporal cortex continued and appeared in medial posterior cortex around cingulate (BA 25, 0 5 −10; BA 31, −10 −45 40), cuneus (BA 17, 5 −100 −5), and precuneus (BA 7, 5 −60 65; −5 −50 50), and occipital extrastriate regions (BA 18, 0 −95 −15). The SW effect in PCC is active after 700 ms. (F)Late impoverishment sources for pseudo objects. P600-like wave in AIT and SW in PCC shown. (G)Late object type sources for LI, and (H)for MI: Occipitotemporal cortex only.
Mentions: For the four difference waves (Figure 7), cortical sources were estimated. The main focus was the time of the N3 peak from 300 to 400 ms (Figures 8A–D). Sources of this impoverishment effect (MI vs. LI) for real objects localized to occipitotemporal and lateral prefrontal areas found with fMRI (Ganis et al., 2007), whereas, for pseudo objects, impoverishment differences localized only to prefrontal areas. Sources of the object type effects (real vs. pseudo) on both LI and MI trials were in occipitotemporal areas. Sources at other times were also estimated. At all times after 200 ms, type effects continued in the same occipitotemporal areas (Figures 8C,D,G,H). Impoverishment sources varied over time and with object type (Figures 8A,B,E,F). The 200 to 300 ms time during the P250/N250 component showed the same impoverished-real-object pattern of sources as the peak N3 time period. Later, from 400 to 500 ms when the N3 ends and the N400 peaks, impoverishment effects for real objects showed only the occipitotemporal source (see intracranial ERP in Figure 8A). Around 450 ms, the maximum source shifted to anterotemporal cortex for both real and pseudo objects, suggesting an additional contribution from this region to the N400. From 500 to 700 ms, the estimated intracranial ERP for the anterotemporal source resembled the scalp P600 impoverishment waveform, which is maximal at this time, and more mediotemporal sources also contributed (Figures 8E,F). From 700 to 900 ms when the late SW dominates, anterotemporal impoverishment activity continued only for real objects. In addition, for both object types, impoverishment effects now appeared in the posterior cingulate cortex (PCC; Figures 8E,F).

Bottom Line: N3 impoverishment effects localized to both prefrontal and occipitotemporal cortex for real objects only.The N3 also showed knowledge effects by 230 ms that localized to occipitotemporal cortex.Finally, response activity in supplementary motor area during a posterior SW after 900 ms showed impoverishment effects that correlated with RTs.

View Article: PubMed Central - PubMed

Affiliation: School of Psychology, Cognition Institute, University of Plymouth Plymouth, UK.

ABSTRACT
People categorize objects more slowly when visual input is highly impoverished instead of optimal. While bottom-up models may explain a decision with optimal input, perceptual hypothesis testing (PHT) theories implicate top-down processes with impoverished input. Brain mechanisms and the time course of PHT are largely unknown. This event-related potential study used a neuroimaging paradigm that implicated prefrontal cortex in top-down modulation of occipitotemporal cortex. Subjects categorized more impoverished and less impoverished real and pseudo objects. PHT theories predict larger impoverishment effects for real than pseudo objects because top-down processes modulate knowledge only for real objects, but different PHT variants predict different timing. Consistent with parietal-prefrontal PHT variants, around 250 ms, the earliest impoverished real object interaction started on an N3 complex, which reflects interactive cortical activity for object cognition. N3 impoverishment effects localized to both prefrontal and occipitotemporal cortex for real objects only. The N3 also showed knowledge effects by 230 ms that localized to occipitotemporal cortex. Later effects reflected (a) word meaning in temporal cortex during the N400, (b) internal evaluation of prior decision and memory processes and secondary higher-order memory involving anterotemporal parts of a default mode network during posterior positivity (P600), and (c) response related activity in posterior cingulate during an anterior slow wave (SW) after 700 ms. Finally, response activity in supplementary motor area during a posterior SW after 900 ms showed impoverishment effects that correlated with RTs. Convergent evidence from studies of vision, memory, and mental imagery which reflects purely top-down inputs, indicates that the N3 reflects the critical top-down processes of PHT. A hybrid multiple-state interactive, PHT and decision theory best explains the visual constancy of object cognition.

No MeSH data available.