A Puzzling Paradigm 1
Running head: A PUZZLING PARADIGM
Syllables and Nonpronounceable Clusters Do Not Appear to Activate Distinct Regions in the Brain: A Functional Magnetic Resonance Imaging Study
Brian G. Skotko, Bora Lee, Jason Katzen, Dirk Stanley, Hua Guo,
Allen Song, and Gregory McCarthy
Brain Imaging and AnalysisCenter, DukeUniversity
Correspondence to:
Brian G. Skotko
16987 Stag Thicket Ln.
Strongsville, OH44136
Email:
Phone: (440) 238-2964
A Puzzling Paradigm 1
Abstract
The simultaneous presentation of an orthographic cue (letter string cue) with a semantic cue (cue for meaning) for a target word results in synergistic memory retrieval. When solving crossword puzzles, individuals integrate both orthographic and semantic information present in the puzzle. Several studies have found that a subject's success in solving a crossword puzzle is more dependent on the orthographic and semantic cues provided for a target word than on the subject's verbal abilities. Goldblum and Frost found that phonologic units, particularly syllables, were highly facilitative for puzzle solving. Functional Magnetic Resonance Imaging (fMRI) was used in conjunction with a crossword puzzle paradigm to study brain regions involved in language processing. First, the activation generated from the presentation of an alphabetizing task was compared to the activation from the presentation of an orthographic cue. Activation from the presentation of an orthographic cue was then compared to the activation generated by the simultaneous presentation of an orthographic and a semantic cue. The third part of the experiment was used to determine if the presentation of a syllable resulted in any differential activation from that of nonpronounceable cluster presentation. The results can be explained using the Wernicke-Geschwind model of language processing. As the provided cues became increasingly more complex (alphabetize; orthographic ; orthographic and semantic), activation was detected in higher processing areas of the Wernicke-Geschwind model. Differential activation between syllables and nonpronounceable clusters could not be detected. The implications for these findings in the study of language processing are discussed.
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Introduction
Orthographic (letters) and semantic (words) cues provide the basis for complex tasks such as reading and comprehension. In many languages like English, letters are combined into phonological components like syllables to form sounds, phonological components are combined to form meaning in the form of words, and words are combined to form complex thought in the form of sentence fragments. Here in this paper, we (1) investigate the dual contributions of orthographic and semantic cuing and (2) investigate the notion that lexical units—like the syllable—do exist somewhere between the letter and the word.
Massaro et al. (1991) have shown that orthographic and semantic cues can jointly provide better memory retrieval than either cue alone (in a process called multiplicative cuing). Most commonly, this result is experienced by individuals who solve crossword puzzle on a regular basis. According to Nickerson (1977), crosswords can be viewed as cued retrieval tasks containing both orthographic cues (i.e., the letters already printed in the grid) and semantic cues (i.e., the Across and Down clues). Other crossword studies have further suggested that proficiency of puzzles depends more on the manipulation of letters and word fragments rather than a knowledge of a large number of words (Underwood, Diehim, and Batt, 1994). According to Hambrick, Salthouse, and Meinz (1999), “there is no indication . . . that either inductive or analytical reasoning processes contribute to the success in crossword puzzle solving.” Instead, word retrieval remains central to the task, and the question remains: do certain arrangements of letters—like those frequently encountered in a crossword puzzle—constitute a distinct unit in the mental lexicon?
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Since the early nineteenth century, many linguistic and cognitive neuroscientists have argued that some such units may include the phoneme, the morpheme, the diphthong, and the syllable. While all these classifications have been hard to define, the delineation of the syllabic function has been particularly so. According to the third edition of the American Heritage Dictionary of English Language, a syllable is “a unit of spoken language consisting of a single uninterrupted sound formed by a vowel, diphthong, or syllabic consonant alone, or by any of these sounds preceded, surrounded, or followed by one or more consonants.”
Syllables are widely accepted as important for both auditory word perception (Kahn, 1976; Mehler, et al., 1981; Segui, 1984) and written word recognition (Goldblum and Frost, 1988). In this last study, participants were asked to generate words from a series of word fragments, accompanied by semantic clues. Ultimately, the participants retrieved words more accurately and quickly from word-initial syllabic fragments (e.g., M E R_ _ _ _ for MERCURY) than from non-initial pronounceable clusters (e.g., _ E R C _ _ _ ), non-initial unpronounceable clusters (e.g., _ _ R C U _ _ ), or randomly dispersed letters (e.g., M _ R _ U _ _ ). This suggests that organization of letter strings, alone, is not enough to facilitate word retrieval. Lexical units seem to be organized according to phonological principles—in this case, the syllable.
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Only a few positron emission tomography (PET) studies and functional magnetic resonance imaging (fMRI) studies have examined lexical units. Passive listening or silent reading of words have been shown to activate Brodmann’s areas 22/42 in the left temporal cortex (Peterson et al., 1990; Frith et al., 1991; Howard et al., 1992; Price et al., 1997). Discriminating between concrete and abstract words activates the posterior part of the left superior and middle temporal gyrus (Friederici et al., 2000) and discriminating between spoken pragmatic, semantic, and syntactic sentence errors activates distinct brain regions to varying degrees (Kuperberg et al., 2000). In another recent fMRI study, German participants were flashed twenty unpronounceable letter strings and twenty highly imaginable German nouns (Jessen et al., 1999). Classical language-related brain areas such as the left inferior frontal gyrus, the left superior temporal gyrus, and the left parietal-occipital regions were activated with the random letter strings, alone. The whole German words, however, activated additional areas: the left angular gyrus, the bilateral percuneus and the left posterior cingulate gyrus. In short, the study suggests that letter strings alone can activate language areas, but other regions may be reserved for higher semantic associations such as the word. Does the syllable, however, activate an amount of brain region somewhere between that of the letter strings and the whole word? Or does it activate the same minimal region as the letter strings or the same maximal area as the whole word? Perhaps the syllable can even activate a unique region.
The goal of this paper is to answer these hypothesis questions using a series of syllabic cues, typical to those encountered in a crossword puzzle. Semantic cues are also added at varying stages to test the neural basis of multiplicative cuing.
Methods
Participants.
Four healthy Duke undergraduates—three males and one female—were recruited through word of mouth. None of the participants, ages 18- to 22-years-old, had a history of neurological injury or disease such as trauma, seizures, strokes, or prior neurosurgery. Three of the four participants were right-handed, and all were monolingual English speakers. Each participant was compensated for his time. This study was approved by the Duke University Medical Center Institutional Review Board, and each participant provided informed consent.
Stimulus Display.
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Each participant was tested for 40 words and 5 practice words, each presented across four consecutive stages (see Table 1). All words were eight letters in length, began with a three-letter syllable (consonant-vowel-consonant), and fell within a low frequency range (0 – 45) according to Kucera and Francis (1967). Whenever possible, the fourth letter of each word was also a consonant to ensure a clear division between the first and second syllable. All letters were white and appeared on a black background. The participants viewed the displays through an angled mirror mounted on eyeglasses.
Each word set was divided into four stages. In the first stage, participants were asked to determine whether a random 3-letter string of letters was in alphabetical order. The three-letter strings were placed either in the first three positions of the mock clue (e.g., t a s _ _ _ _ _ ) or in the third, fourth, and fifth positions (e.g., _ _ w e r _ _ _ ). Care was taken not to pick three letters that were actually part of the 40 test words, thereby minimizing the influence of priming. Underneath each clue fragment, the word “alphabetize” appeared to remind participants of the task. This stage served as a control to Stage 2.
In the second stage, participants were asked to think of a word from a three-letter string. When placed at the beginning of the clue, the three-letter string was a syllable
(e.g., c o n _ _ _ _ _ for concerto). When placed in the third, fourth, and fifth positions, the three-letter string was a nonpronounceable cluster (e.g., _ _ n c e _ _ _ for concerto). From the list of 40 test words, participants were presented with an equal number of alternating syllables and nonprounceable clusters (see Table 2). Underneath each clue fragment, the word “fill-in-the-blank” appeared to remind participants of the task.
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In the third stage, participants were asked to think of a word from the same three-letter string encountered in stage 2; this time a semantic clue was printed underneath the word fragment. Letter position was conserved. So, if a participant was presented with c o n _ _ _ _ _ in Stage 2, they would be presented with c o n _ _ _ _ _ and the clue “masterpiece.” If they were instead presented with _ _ n c e _ _ _ in Stage 2, they would be presented with _ _ n c e _ _ _ with the clue “masterpiece.” As such, participants were presented with an equal number of semantic clues with syllabic prompts (n = 20) and semantic clues with cluster prompts (n = 20).
In the final stage, the words “say answer” were flashed on the screen, giving the participant an opportunity to communicate his answer for the word fragment.
Procedure.
Before the experiment began, each participant were given directions and asked to complete five practice sets, generated on the computer using Showtime software (The MathWorks Company).
All scanning was performed on a General Electric 1.5T scanner equipped with an Advanced Development Workstation for realtime echoplanar imaging. The experimenter identified the location of the anterior and posterior commisure, and 16 slices on this plane, 7.5mm thick, were chosen for the study. Sagittal T1-weighted localizer images were first collected for approximately 30 minutes. The functional images measured changes in BOLD contrast and were collected using a T2*-weighted gradient-echo, echoplanar imaging sequence [echo time (TE) = 40 msec; repetition time (TR) = 1.5 s; matrix = 64 x 64; field of view = 24 x 24 cm].
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The 40 test words were divided into 4 runs of 10 word sets each, allowing participants to have short mental breaks in between. During the runs, the alphabetizing stage was first presented for 3.0 s, and participants were asked to indicate with a two-button system whether or not the letter-strings were in alphabetical order. The responses were recorded in a computerized output file. After this stimulus, 6.0 s of blank screen was presented to ensure recovery of the hemodynamic response (Huettel and McCarthy, 2000). Afterwards, the fill-in-the-blank task was presented for 10.5 s followed immediately with the fill-in-the-blank task with a semantic clue for another 10.5 s. Immediately afterwards, the screen “say answer” was presented for 3.0 s, and participants were given an opportunity to verbalize their response. The correct answer was then flashed for 1.5 s. Finally, 6.0 s of blank screen was flashed to ensure recovery of the hemodynamic response before the next word was tested (see Table 5 for schematic illustration). One word set then lasted 40.5 s. With a 12 s delay at the beginning of each run, each run lasted 417 s (6 min, 57 s).
In order to ensure that words were tested for both syllables and nonpronounceable clusters, two versions of the test were alternated between subjects. For example, participant 1 and 2 were tested for “concerto” in the syllable format (i.e., c o n _ _ _ _ _ ) while participants 3 and 4 were tested in the nonprounceable format (i.e., _ _ n c e _ _ _ ). For the next word, the formats would be switched—participants 1 and 2 would receive the nonpronounceable format and participants 3 and 4 would receive the syllable formats (see Table 2). This variation eliminates the small possibility that “easier” words were picked for the syllable format and “harder” words were picked for the nonpronounceable format. In short, if there is a difference between formats, the reason does not lie in the word selection.
Data Analysis.
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The statistical analysis of the fMRI data was performed at the individual level (within-subject analysis). The data was analyzed by using a subtractive t-test to compare activation from one condition with the activation from another condition. First, the activation from the alphabetizing task was compared to activation invoked by the fill-in-the-blank task. Therefore, the t-test eliminated the similar areas of activation that these two tasks shared. Then, the activation from the fill-in-the-blank task was compared to the activation from the fill-in-the-blank task plus semantic clue. Finally, the activation from syllable processing was compared to differential activation from the nonpronounceable cluster tasks. The Matlab Overlay2 function (The MathWorks Company) was utilized to project the acquired activation as a Z-score map superimposed over anatomical brain images. The significant Z value was thresholded at a value of 3.6 which correlated to a p value of .001. Activated brain regions were identified using the Talairach and Tournoux brain atlas (1988). The Region of Interest (ROI) Matlab function was used to analyze activation common to all subjects. Due to time constraints, only one subject was analyzed with ROI. These calculations were performed using the bin analysis of epochs acquired during the scan.
Results
The fill-in-the-blank task activates additional brain regions when compared to the alphabetize task.
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The alphabetize task significantly activated (p < 0.001) a distinct region of the visual cortices in 3 out of 4 participants (Table 3; Figure 1a), and the hemodynamic response of Participant 2 (Figure 4a) is consistent with the 6 s expected delay. Here we see activation beginning 6 s after the onset of a stimulus and peaking around 7 s. The fill-in-the-blank task significantly activated (p < 0.001) distinct regions of the visual cortices in 4 out of 4 participants. These regions were located posteriorly and laterally to the visual regions uniquely activated by the alphabetize task (Figure 1b). The fill-in-the-blank task also significantly activated (p < 0.001) a region of Broca’s area in 4 out of 4 participants (Figure 1c). The hemodynamic responses of Participant 2 to these fill-in-the-blank regions, however, (Figure 4b & 4c) are suspect and need to be further examined (see Discussion). Nevertheless, our results are largely consistent with Jessen et al. (1999): the fill-in-the-blank task required higher semantic associations compared to the random letter strings.
The fill-in-the blank task with semantic clues activated distinct brain regions compared to the fill-in-the-blank task, alone.
The fill-in-the-blank task without a clue significantly activated (p < 0.001) a distinct region of Broca’s area in 2 out of the 4 participants (Table 4; Figure 2a). However, the fill-in-the-blank task with clues significantly activated (p < 0.001) a distinct region of Broca’s area in 4 out of 4 participants (Figure 2b). The hemodynamic response of Participant 2 (Figure 4d) to the fill-in-the-blank with clue task is suspect and needs to be further examined (see Discussion). Nonetheless, our results are consistent with Massaro et al. (1991) and Jessen et al. (1999): semantic clues will assist in word retrieval and activate higher semantic associations.
Syllables do not activate additional brain regions compared to nonprounceable clusters.
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Since the fill-in-the-blank task resulted in different regions of activation for the clue and non-clue conditions (see above), we separated these conditions in our analyses of the syllables and nonprounceable clusters. However, contrary to our initial hypotheses, syllables did not activate distinct brain regions compared to nonpronounceable clusters in either the fill-in-the-blank task without clues (Figure 3a) or the fill-in-the-blank task with clues (Figure 3b). These results raise into question the importance of distinct neural substrates for seemingly different cognitive cues.
Discussion
Our distinct differences between the alphabetize task and the fill-in-the-blank task nicely fit into the Wernicke-Geschwind model of language comprehension (Kandel, Swartz, and Jessel, 1995). According to this model, visual information from reading a word is passed from the retina to the lateral geniculate nucleus and on to the primary visual cortex (Brodmann’s area 17). The information subsequently is transferred to higher-order regions of the visual cortices (Brodmann’s area 18). Afterwards, it travels to Wernicke’s area (Brodmann’s area 22) to be comprehended and to Broca’s area (Brodmann’s area 45), by means of the arcuate fasciculus, to be verbalized. Information can also bypass Wernicke’s area and be directly transmitted to Broca’s area.