Elsevier

Neuropsychologia

Volume 44, Issue 9, 2006, Pages 1560-1568
Neuropsychologia

Prefrontal cortex hemispheric specialization for categorical and coordinate visual spatial memory

https://doi.org/10.1016/j.neuropsychologia.2006.01.018Get rights and content

Abstract

During visual spatial perception of multiple items, the left hemisphere has been shown to preferentially process categorical spatial relationships while the right hemisphere has been shown to preferentially process coordinate spatial relationships. We hypothesized that this hemispheric processing distinction would be reflected in the prefrontal cortex during categorical and coordinate visual spatial memory, and tested this hypothesis using functional magnetic resonance imaging (fMRI). During encoding, abstract shapes were presented in the left or right hemifield in addition to a dot at a variable distance from the shape (with some dots on the shape); participants were instructed to remember the position of each dot relative to the shape. During categorical memory retrieval, each shape was presented centrally and participants responded whether the previously corresponding dot was ‘on’ or ‘off’ of the shape. During coordinate memory retrieval, each shape was presented centrally and participants responded whether the previously corresponding dot was ‘near’ or ‘far’ from the shape (relative to a reference distance). Consistent with our hypothesis, a region in the left prefrontal cortex (BA10) was preferentially associated with categorical visual spatial memory and a region in the right prefrontal cortex (BA9/10) was preferentially associated with coordinate visual spatial memory. These results have direct implications for interpreting previous findings that the left prefrontal cortex is associated with source memory, as this cognitive process is categorical in nature, and the right prefrontal cortex is associated with item memory, as this process depends on the precise spatial relations among item features or components.

Introduction

Visual spatial perception of an item (e.g., a face, an object, or an abstract shape) produces activity in both the ventral cortical processing stream – occipital and ventral temporal cortex – for item identification and the dorsal cortical processing stream – occipital and parietal cortex – for item spatial localization in nonhuman primates (Ungerleider & Mishkin, 1982; although there are between stream connections, see Felleman & Van Essen, 1991). In humans, neuroimaging evidence indicates that the ventral (‘what’) processing stream extends from occipital cortex to ventral temporal cortex and into ventral prefrontal cortex, while the dorsal (‘where’) processing stream extends from occipital cortex to parietal cortex (Haxby et al., 1991; Haxby et al., 1994; Köhler, Kapur, Moscovitch, Winocur, & Houle, 1995).

There has been a long-standing debate as to whether this dorsal–ventral visual spatial perceptual processing distinction also exists in the prefrontal cortex during working memory (given that this cognitive function has been associated with the prefrontal cortex; see Baddeley & Della Sala, 1996). There is now compelling evidence that the ventral prefrontal cortex is preferentially associated with item working memory and the dorsal prefrontal cortex is preferentially associated with spatial working memory (Belger et al., 1998; Courtney, Petit, Maisog, Ungerleider, & Haxby, 1998; Courtney, Ungerleider, Keil, & Haxby, 1996; Haxby, Petit, Ungerleider, & Courtney, 2000; Rowe, Toni, Josephs, Frackowiak, & Passingham, 2000; Sala, Rämä, & Courtney, 2003). Although some researchers have failed to find differential item and spatial working memory effects in prefrontal cortex (D’Esposito et al., 1998; Owen et al., 1998; Postle, Berger, Taich, & D’Esposito, 2000; Postle & D’Esposito, 1999), such null results can occur due to a number of reasons (e.g., a lack of sensitivity or insufficient task demands). In illustration of this point, a reanalysis of Postle et al.'s (2000) functional magnetic resonance imaging (fMRI) data was conducted using event-related timecourse analysis, rather than the more typically used beta-weight analysis, and revealed spatial working memory specific activity in dorsal prefrontal cortex, supporting the dorsal–ventral prefrontal cortex working memory distinction (Slotnick, 2005). Thus, the significant findings affirm that the ventral and dorsal visual spatial perceptual processing streams extend into ventral and dorsal prefrontal cortex during item and spatial working memory.

In everyday life, visual spatial perception not only involves processing items in isolation, but is also engaged in processing the positions of items relative to one another. Kosslyn (1987) proposed that the left hemisphere is preferentially associated with between-item categorical processing (e.g., one item is ‘above’ or ‘below’ the other, a discrete judgment) and the right hemisphere is preferentially associated with between-item coordinate processing (e.g., one item is ‘near’ to or ‘far’ from the other, an analog judgment). These distinct types of processing can also refer to the relative positions of parts or features of a single item (for further elaboration, see Section 4). This left–right hemisphere categorical–coordinate visual spatial perceptual processing distinction has been convincingly supported in a number of subsequent behavioral studies (Banich & Federmeier, 1999; Bruyer, Scailquin, & Coibion, 1997; French & Painter, 1991; Hellige & Michimata, 1989; Koenig, Reiss, & Kosslyn, 1990; Kosslyn et al., 1989; Laeng & Peters, 1995; Laeng, Shah, & Kosslyn, 1999; Michimata, 1997; Niebauer & Christman, 1998; Okubo & Michimata, 2002; Sergent, 1991; Servos & Peters, 1990). Some investigators have taken failures to find such categorical and coordinate hemispheric laterality effects as contradictory evidence (Bruyer et al., 1997; Cowin & Hellige, 1994; Rybash & Hoyer, 1992; Sergent, 1991). However, direct support for Kosslyn's hemispheric processing distinction has been confirmed with patients that had one hemisphere (usually followed by the other) temporarily deactivated by injection with sodium amobarbital – the left hemisphere was preferentially associated with categorical visual spatial processing and the right hemisphere was preferentially associated with coordinate visual spatial processing, but only under sufficiently demanding task conditions (which may provide some explanation of previous null findings; Slotnick, Moo, Tesoro, & Hart, 2001). Furthermore, evidence from patients with focal lesions (Laeng, 1994; Laeng, Carlesimo, Caltagirone, Capasso, & Miceli, 2002) and neuroimaging (Baciu et al., 1999) suggests that categorical and coordinate perceptual processing may be particularly reliant on the left and right parietal lobes, respectively, although there is neuroimaging evidence that this hemispheric distinction also occurs in the prefrontal cortex during perceptual processing (Kosslyn, Thompson, Gitelman, & Alpert, 1998) and spatial imagery (Trojano et al., 2002). The overall pattern of results can be taken as strong evidence that the left hemisphere is preferentially associated with categorical visual spatial perceptual processing and the right hemisphere is preferentially associated with coordinate visual spatial perceptual processing (see meta-analysis by Laeng, Chabris, & Kosslyn, 2003).

Similar to the ventral–dorsal prefrontal cortex distinction that has been associated with item and spatial working memory, we hypothesized that the left–right hemisphere prefrontal cortex distinction would be manifested during categorical and coordinate visual spatial memory. In particular, we focused on the dorsolateral and anterior prefrontal cortex, as these regions have been associated with source memory and item memory (Cansino, Maquet, Dolan, & Rugg, 2002; Nyberg, McIntosh, Cabeza, Habib, & Houle, 1996; Rugg, Fletcher, Chua, & Dolan, 1999; Slotnick, Moo, Segal, & Hart, 2003). To anticipate the results, a region in left prefrontal cortex was associated with categorical visual spatial memory while a region in right prefrontal cortex was associated with coordinate visual spatial memory.

Section snippets

Participants

After providing informed consent, 11 right-handed participants took part in the imaging study, which had been approved by the Johns Hopkins University institutional review board. Due to excessive head movement in three participants (i.e. greater than 1 mm), eight participants were included in the analysis (age range 23–35 years, five females), which was sufficient to conduct the imaging analysis (Friston, Holmes, & Worsley, 1999). A follow-up behavioral study, approved by the Harvard University

Results

The power analysis revealed activity in regions associated with visual spatial perceptual processing, including striate and extrastriate occipital cortex (right BA17, bilateral BA18 and BA19) extending into temporal cortex (bilateral BA37, left BA20 and BA21) and parietal cortex (left BA7 and bilateral BA40). Activity was also observed in regions associated with motor response (BA6 including the supplementary motor area and bilateral premotor cortex, BA24, and the right caudate; see Picard &

Discussion

In direct support of our hypothesis, we observed a double dissociation with regard to visual spatial memory related activity in prefrontal cortex – a region in left prefrontal cortex (BA10) was associated with categorical visual spatial memory and a region in right prefrontal cortex (BA9/10) was associated with coordinate visual spatial memory. Furthermore, a right parahippocampal gyrus region (BA36) was identified that was associated with both types of visual spatial memory. The latter finding

Conclusion

In the present study, the left prefrontal cortex has been associated with categorical visual spatial memory and the right prefrontal cortex has been associated with coordinate visual spatial memory. The left prefrontal cortex categorical memory finding provides a direct explanation for source memory related activity in this region given the categorical nature of the associated decisions, and the right prefrontal cortex coordinate memory finding suggest item memory related activity in this

Acknowledgement

Lauren Moo is supported by NIDCD grant DC05068.

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