This study is the first to identify neural correlates of top-down letter processing in the absence of any systematic bottom-up information. By examining illusory letter detection to pure noise images, the reported activation differences can be attributed primarily to endogenous top-down processing. Compared to trials where letters were not detected, illusory letter detection was associated with greater activation in several cortical areas ranging from the occipital cortex to the frontal cortex.
Together with the existing evidence regarding these areas, the present findings shed important lights on the specific functions of these areas in top-down processing. The present study revealed that the SPL was activated by the letter response relative to the no-letter response. Different sub-regions in the SPL have been demonstrated to be involved in various processes such as spatial attention processing, episodic memory retrieval, and word processing. Recent studies reported that some sub-regions of the SPL were specifically activated by letter naming, but not by naming objects or scramble letters, with the activation peak (-38, -50, 48) highly consistent with what was found here (-34, -50, 50), suggesting such region may be specifically involved in letter processing rather than words processing or other object processing (Joseph, Cerullo, Farley, Steinmetz & Mier, 2006
; Joseph, Gathers & Piper, 2003
). In line with this suggestion, Price, Wise, and Frackowiak (1996)
found activation of this region of the SPL elicited by pseudowords relative to words, and attributed this activation to the phonological coding during the translation of individual letters into their sounds. The patients with damage to the left SPL and posterior temporal cortex presented the absence of the ability to retrieve sounds from letters (Friedman, Ween & Albert, 1993
). Given these evidence, the activation of the SPL elicited by letter response relative to the no-response in the present study may be related to the phonological translation from letter into sound when a letter was ‘detected’.
It should be noted that some sub-regions within the left SPL was also reported to be involved in a number of non-letter related top-down processes, such as imagery of objects (-13, -74, 52, Mechelli, Price, Friston & Ishai, 2004
), imagery of famous faces (-38, 37, 40, Ishai, Haxby & Ungerleider, 2002
) and detection of faces from noise (-45, -44, 44, Zhang, et al., 2008
). However, the exact loci of the peak activation reported in these studies are not consistent with that found in the present study (-34, -50, 50), especially for the study of Zhang, et al., (2008)
who used the same experimental paradigm as the presents study except that their participants were required to detect faces instead of letters from noisy images. The differences between these previous studies and the present study suggest that the sub-region of the SPL identified by the present results might indeed play a unique role in the top-down processing of letters.
With regard to the left IFG, there is evidence to suggest that the left IFG may have a broad top-down function. The above mentioned recent study (Zhang et al., 2008
) used exactly the same experimental paradigm as the presents study except that participants were required to detect faces instead of letters from pure noise images. They found that the left IFG (-48, 13, 24) also was activated when faces were purportedly detected from noise pictures relative to when faces were not detected. Further, as revealed by our correlation analyses, the proportion of letter detections made by each participant was negatively correlated with the BOLD signal differences between letter and no-letter responses in the left IFG. In other words, the larger a participant's activation difference the less likely the participant would report to have seen letters. One explanation for this finding can be provided by Huettel, Song & McCarthy (2005)
who suggested that the posterior left IFG was related to making decision under uncertainty and the activation of this region increased with the increasing uncertainty of a decision. On this account, the participants who were more liberal in responding may make decision about whether the letter was detected in a less uncertainty situation, and therefore, a small amount of top-down activation was sufficient to prompt letter detection. In contrast, for conservative individuals, the uncertainty of the detection task may increase though the same noise pictures were used for all the participants. As a result, more top-down activation was required to produce illusory letter detection in this more uncertainty situation.
However, recent studies have reported that the IFG is specifically activated by the bottom-up processing of letters (Joseph, Cerullo, Farley, Steinmetz & Mier, 2006
; Joseph, Gathers & Piper, 2003
; Pernet, Franceries, Basan, Cassol, Démonet & Celsis, 2004
). For example, some studies have reported that the left IFG responded more to the naming of letters and objects than to the matching of letters or objects, suggesting that this region may be involved in phonological processing (Joseph, Cerullo, Farley, Steinmetz & Mier, 2006
; Joseph, Gathers & Piper, 2003
). The locus of the activation of the left IFG in these studies (-47, 5, 27) is highly consistent with that (-48, 5, 26) of our study. Further, in our study, although the participants were instructed to only respond to whether a letter was detected in the noise picture using a response key during the scanning sessions, they reported silently reading the letter when they ‘detected’ it from the noise picture. Unlike the words, letters have little semantic content but simple phonological information. Therefore, in line with Joseph et al., (Joseph, Cerullo, Farley, Steinmetz & Mier, 2006
; Joseph, Gathers & Piper, 2003
), the activation of the left IFG in our study may be due to the phonological processing of the ‘detected’ letters. This interpretation is also supported by the evidence form recent studies about word processing (Xu et al., 2001
), wherein the same region (-44, 4, 28) in the left IFG was activated by pseudoword rhyming relative to color matching with letters. More interestingly, this region (-42, 4, 26) responded more to alphabetic word than to Chinese characters (for a review, see Tan, Laird, Li & Fox 2005
). Thus, the evidence from the top-down and bottom-up studies taken together suggests that the sub-region in the left IFG identified in the present study might be involved in the integration of bottom-up letter specific processes and general top-down processes.
With regard to the function of precuneus, previous studies has demonstrated that bilateral precuneus was involved in different processes, such as mental imagery, working memory, and episodic memory (Cabeza & Nyberg, 2000
). For example, studies have shown that the bilateral precuneus produced greater activation during visual imagery (e.g., famous faces) compared to passively viewing letter strings (e.g., Ishai, Haxby, & Ungerleider, 2002
). Additionally, it is reported that precunues was activated by visual imagery such as faces, house, and chair (Mechelli, Price, Friston, & Ishai 2004
). Also, Zhang et al. (2008)
who use the same experimental paradigm to the present study have found that the left precuneus (-30, -62, 36) also shown more activation when detecting a face from noise picture than when not detecting a face. In the present study, to find the letter from the noise picture, individuals have to perform a match between the pattern seen in the noisy pictures and the letters stored in their memory. Once that match is successful, one could then report a detection of a letter. Therefore, the potential interpretation of the activation of precuneus in the present study may be due to the retrieval of letter information, based on which a letter has been ‘detected’. Our finding that the precuneus is active during top-down letter detection is consistent with the existing findings, and suggests that the precuneus may be more generally involved in top-down object identification for a variety of object classes, including letters.
The right MOG and right MTG also responded to letter response than to no-letter response. This finding is not readily related to the previous literature. The activation of these regions within visual cortex may be due to the top-down modulation of the SPL (Silvanto, Muggleton Lavie & Walsh, 2009
); however, their exact roles in the top-down processing of letters need to be further investigated.
The present study using the pure noise paradigm represents the first attempt to reveal the neural regions involved the top-down processing of letters. Further research is however needed. For example, one needs to use the pure noise paradigm along with the existing bottom-up paradigms to compare the neural regions involved in top-down and bottom-up processing of letter. Further, one can use the same pure noise paradigm to contrast the top-down processing of letters with that of digits, shapes, and other objects as well as that of words using a within-subjects design. Such design should provide firmer evidence as to the extent to which some of the regions activated during top-down letter detection are indeed specific to letter or word processing and the others are associated with the top-down processing of objects generally. Furthermore, functional connectivity analyses are needed to identify the neural networks specifically involved in the top-down processing of letters as opposed to that of words, digits, shapes, and other objects. Such additional research should help greatly the elucidation of the neural organizations involved in the top-down processing of various ecological salient objects in our environment.