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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.


Theories of visual category decisions. Timing estimates based on human brain electromagnetic potential data. Black arrows are bottom-up. Green arrows are top-down. Dotted arrows are implied but not specified. Times in black are earliest time of bottom-up input to that region. Times in green are earliest time of feedback input from nearest higher order area to that region. Times in magenta are when prefrontal top-down inputs interact with bottom-up and/or feedback interactions along the visual pathways. Times in gray are associated with implied activity. Theories posit an early time course before 200 ms (A–F) or a later time course (G). (A) Bottom-up theories posit that the initial feedforward pass through the ventral visual pathway supports object cognition. According to decision theory, this supports a category decision in lateral prefrontal cortex (LPFC). In contrast, perceptual hypothesis testing (PHT) theories (B–G) emphasize top-down contributions: (B) Temporal lobe variants assume bottom-up inputs along the ventral visual hierarchy trigger feedback along the pathway, which consequently modifies bottom-up processing. (C) Parietal variants emphasize that the dorsal stream is necessary for complete object constancy. (D) One prefrontal variant posits a role for top-down input from ventral LPFC (VLPFC) and orbitofrontal cortex (OFC). (E) Temporal-prefrontal variants emphasize bottom-up and feedback processes from visual areas along the ventral pathway through prefrontal cortex. (F) Parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention to locations and features associated with an object category that have been cued by a search template prior to stimulus onset; this modulates visual processing early in time from 80 to 200 ms. (G) Late parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention that contribute model prediction and testing processes when the category is not cued before stimulus onset; note, fMRI tests of parietal-prefrontal PHT variants implicate VLPFC in model prediction and testing (Ganis et al., 2007; Schendan and Stern, 2008).
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Figure 1: Theories of visual category decisions. Timing estimates based on human brain electromagnetic potential data. Black arrows are bottom-up. Green arrows are top-down. Dotted arrows are implied but not specified. Times in black are earliest time of bottom-up input to that region. Times in green are earliest time of feedback input from nearest higher order area to that region. Times in magenta are when prefrontal top-down inputs interact with bottom-up and/or feedback interactions along the visual pathways. Times in gray are associated with implied activity. Theories posit an early time course before 200 ms (A–F) or a later time course (G). (A) Bottom-up theories posit that the initial feedforward pass through the ventral visual pathway supports object cognition. According to decision theory, this supports a category decision in lateral prefrontal cortex (LPFC). In contrast, perceptual hypothesis testing (PHT) theories (B–G) emphasize top-down contributions: (B) Temporal lobe variants assume bottom-up inputs along the ventral visual hierarchy trigger feedback along the pathway, which consequently modifies bottom-up processing. (C) Parietal variants emphasize that the dorsal stream is necessary for complete object constancy. (D) One prefrontal variant posits a role for top-down input from ventral LPFC (VLPFC) and orbitofrontal cortex (OFC). (E) Temporal-prefrontal variants emphasize bottom-up and feedback processes from visual areas along the ventral pathway through prefrontal cortex. (F) Parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention to locations and features associated with an object category that have been cued by a search template prior to stimulus onset; this modulates visual processing early in time from 80 to 200 ms. (G) Late parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention that contribute model prediction and testing processes when the category is not cued before stimulus onset; note, fMRI tests of parietal-prefrontal PHT variants implicate VLPFC in model prediction and testing (Ganis et al., 2007; Schendan and Stern, 2008).

Mentions: Timing is important because theories can be grouped into two major classes based on time course, early or late: Early theories propose an early time course within 130–215 ms via bottom-up (Thorpe et al., 1996) and/or top-down processes (Bar, 2003), and late theories propose a later time course and a key role for decision-making (Philiastides and Sajda, 2007) or top-down processes for attention (Stuss et al., 1992; Ganis et al., 2007; Schendan and Lucia, 2010; Clarke et al., 2011). Most vision theories, accounts, or models posit an early time course. Bottom-up models are based on the initial bottom-up pass through the ventral visual hierarchical pathway (Riesenhuber and Poggio, 1999) and posit early time courses (Figure 1A). However, a bottom-up model cannot fully explain the visual constancy of human object cognition (Serre et al., 2007a). For example, on ultra rapid category detection tasks, a name cues the target category before a masked image appears briefly (~20 ms) (Delorme et al., 2000). When masking reduces feedback processing (Di Lollo et al., 2000), the initial fast feedforward sweep along the ventral stream dominates performance, consistent with computational models (Serre et al., 2007a). Critically, however, such bottom-up models cannot match human performance (a) when the mask is removed and so feedback inputs are involved, or (b) when people see the image longer before the mask appears (e.g., 80 vs. 50 ms) because then feedback inputs come into play long enough to boost performance. Bottom-up models also perform poorly when objects are impoverished (as by distance, i.e., farther away). Such limitations led to the suggestion that the bottom-up pathway could provide the initial input and object hypothesis to test using top-down processes (Serre et al., 2007b).


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

Schendan HE, Ganis G - Front Psychol (2015)

Theories of visual category decisions. Timing estimates based on human brain electromagnetic potential data. Black arrows are bottom-up. Green arrows are top-down. Dotted arrows are implied but not specified. Times in black are earliest time of bottom-up input to that region. Times in green are earliest time of feedback input from nearest higher order area to that region. Times in magenta are when prefrontal top-down inputs interact with bottom-up and/or feedback interactions along the visual pathways. Times in gray are associated with implied activity. Theories posit an early time course before 200 ms (A–F) or a later time course (G). (A) Bottom-up theories posit that the initial feedforward pass through the ventral visual pathway supports object cognition. According to decision theory, this supports a category decision in lateral prefrontal cortex (LPFC). In contrast, perceptual hypothesis testing (PHT) theories (B–G) emphasize top-down contributions: (B) Temporal lobe variants assume bottom-up inputs along the ventral visual hierarchy trigger feedback along the pathway, which consequently modifies bottom-up processing. (C) Parietal variants emphasize that the dorsal stream is necessary for complete object constancy. (D) One prefrontal variant posits a role for top-down input from ventral LPFC (VLPFC) and orbitofrontal cortex (OFC). (E) Temporal-prefrontal variants emphasize bottom-up and feedback processes from visual areas along the ventral pathway through prefrontal cortex. (F) Parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention to locations and features associated with an object category that have been cued by a search template prior to stimulus onset; this modulates visual processing early in time from 80 to 200 ms. (G) Late parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention that contribute model prediction and testing processes when the category is not cued before stimulus onset; note, fMRI tests of parietal-prefrontal PHT variants implicate VLPFC in model prediction and testing (Ganis et al., 2007; Schendan and Stern, 2008).
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Figure 1: Theories of visual category decisions. Timing estimates based on human brain electromagnetic potential data. Black arrows are bottom-up. Green arrows are top-down. Dotted arrows are implied but not specified. Times in black are earliest time of bottom-up input to that region. Times in green are earliest time of feedback input from nearest higher order area to that region. Times in magenta are when prefrontal top-down inputs interact with bottom-up and/or feedback interactions along the visual pathways. Times in gray are associated with implied activity. Theories posit an early time course before 200 ms (A–F) or a later time course (G). (A) Bottom-up theories posit that the initial feedforward pass through the ventral visual pathway supports object cognition. According to decision theory, this supports a category decision in lateral prefrontal cortex (LPFC). In contrast, perceptual hypothesis testing (PHT) theories (B–G) emphasize top-down contributions: (B) Temporal lobe variants assume bottom-up inputs along the ventral visual hierarchy trigger feedback along the pathway, which consequently modifies bottom-up processing. (C) Parietal variants emphasize that the dorsal stream is necessary for complete object constancy. (D) One prefrontal variant posits a role for top-down input from ventral LPFC (VLPFC) and orbitofrontal cortex (OFC). (E) Temporal-prefrontal variants emphasize bottom-up and feedback processes from visual areas along the ventral pathway through prefrontal cortex. (F) Parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention to locations and features associated with an object category that have been cued by a search template prior to stimulus onset; this modulates visual processing early in time from 80 to 200 ms. (G) Late parietal-prefrontal variants emphasize parietal-prefrontal processes of selective attention that contribute model prediction and testing processes when the category is not cued before stimulus onset; note, fMRI tests of parietal-prefrontal PHT variants implicate VLPFC in model prediction and testing (Ganis et al., 2007; Schendan and Stern, 2008).
Mentions: Timing is important because theories can be grouped into two major classes based on time course, early or late: Early theories propose an early time course within 130–215 ms via bottom-up (Thorpe et al., 1996) and/or top-down processes (Bar, 2003), and late theories propose a later time course and a key role for decision-making (Philiastides and Sajda, 2007) or top-down processes for attention (Stuss et al., 1992; Ganis et al., 2007; Schendan and Lucia, 2010; Clarke et al., 2011). Most vision theories, accounts, or models posit an early time course. Bottom-up models are based on the initial bottom-up pass through the ventral visual hierarchical pathway (Riesenhuber and Poggio, 1999) and posit early time courses (Figure 1A). However, a bottom-up model cannot fully explain the visual constancy of human object cognition (Serre et al., 2007a). For example, on ultra rapid category detection tasks, a name cues the target category before a masked image appears briefly (~20 ms) (Delorme et al., 2000). When masking reduces feedback processing (Di Lollo et al., 2000), the initial fast feedforward sweep along the ventral stream dominates performance, consistent with computational models (Serre et al., 2007a). Critically, however, such bottom-up models cannot match human performance (a) when the mask is removed and so feedback inputs are involved, or (b) when people see the image longer before the mask appears (e.g., 80 vs. 50 ms) because then feedback inputs come into play long enough to boost performance. Bottom-up models also perform poorly when objects are impoverished (as by distance, i.e., farther away). Such limitations led to the suggestion that the bottom-up pathway could provide the initial input and object hypothesis to test using top-down processes (Serre et al., 2007b).

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.