Functional Integration across Brain Regions Improves Speech Perception under Adverse Listening Conditions

Discussion

We have demonstrated how changes in functional integration across very distributed brain regions improve speech perception under acoustically suboptimal conditions. Using a design that varied orthogonally intelligibility (Shannon et al., 1995) and semantic predictability (Stickney and Assmann, 2001) revealed functional connections between areas in the temporal, inferior parietal, and prefrontal cortices that strengthened and supported comprehension of sentences with high semantic predictability but intermediate signal quality. Because the signal quality was constant (eight-band noise-vocoded speech) across sentences of both low and high predictability, this effect could be attributed to the modulating effect of semantic context (Kalikow et al., 1977; Stickney and Assmann, 2001) (Obleser, Alba-Ferrara, and Scott, unpublished observation). This was further confirmed by the observation that the strengthening of functional connections was between areas that were not responding simply to increased sentence comprehension, because activity was not maintained in response to the easily understood 32-band noise-vocoded sentences.

Activation in the contrast of high- and low-predictable eight-band noise-vocoded sentences was most evident in the left angular gyrus. Activity in this area, and at the other extreme of the left temporal lobe, in the anterior temporal cortex extending into the ventral inferior frontal gyrus, showed this effect of high predictability more than low predictability at intermediate signal quality. Additional areas demonstrating the same effect were the left dorsolateral and medial prefrontal cortices and the left posterior cingulate cortex. In contrast, the lateral temporal necortex within the superior temporal gyrus and sulcus was sensitive to the increasing spectral detail across all stimuli.

The enhanced activity was seen only in the high-predictability eight-band condition; when speech comprehension was effortless in response to 32-band speech, activity in the angular gyrus, posterior cingulate cortex, and dorsolateral prefrontal cortex returned to baseline level (Fig. 3). In other words, only if speech comprehension succeeds despite adverse acoustic conditions are these regions involved. Changes in predictability in the absence of signal degradation (i.e., for 32-band signals) were not accompanied by substantial increases in brain activation, nor did they lead to differences in speech recognition in the behavioral pretests. The conclusion is that the influence of semantic context when listening to short sentences only becomes crucial once the signal is compromised.

Functional connectivity analysis among the activated clusters yielded positive correlations between their time courses of activity. This evidence for functional integration was most evident when the subjects listened to eight-band noise-vocoded speech that could be decoded because of semantic context compared with the corresponding signal when semantic context was absent. As summarized in Table 2, the connectivity between the angular gyrus and the other four activation clusters showed the greatest increase (Fig. 4). Interestingly, this strength of connectivity between the angular gyrus and the frontal lobe is reduced in developmental dyslexia (Horwitz et al., 1998), and a recent study demonstrated parietal-frontal “underconnectivity” during sentence comprehension in autistic subjects (Kana et al., 2006). The strengthened connectivity along the temporal lobe (between the angular gyrus and temporal pole) fits well with recent evidence on anatomical links between these areas (middle longitudinal fasciculus), as does the link between the angular gyrus and lateral prefrontal cortex (Schmahmann and Pandya, 2006). A recent study on written text comprehension also identified an increase in activity in the angular gyrus [Brodmann's area (BA) 39] in a contrast of real-word sentences with sentences comprising pseudowords (Ferstl and von Cramon, 2002). This is additional evidence that the angular gyrus is a resource for semantic processing, activated in our study when semantics had a decisive influence on speech perception.

Because all of the regions are distributed across the frontal and parietal cortices, their contribution to speech comprehension is likely to be of higher order than basic acoustic processing. These widespread activations are likely to represent a number of cognitive-supporting mechanisms, among them aspects of working memory and attention. One hypothesis is that the contribution of the angular gyrus is through its role in verbal working memory, and it is a region that has frequently been implicated in explicit semantic decision tasks (Binder et al., 2003; Scott et al., 2003; Sharp et al., 2004). Other processes such as phonological memory and auditory–motor transformation processes (Jacquemot et al., 2003; Hickok and Poeppel, 2004; Warren et al., 2005; Jacquemot and Scott, 2006) that might contribute to recovering meaning from degraded speech signals are located in adjacent but separate temporo-parietal areas. Working memory operations in the left dorsolateral prefrontal cortex [Petrides, 1994; Owen, 1997; for a review on working memory, see Owen et al. (2005)] might support comprehension under adverse conditions by permitting the manipulation of the degraded stimuli within short-term memory. Thus, components of the degraded sentence that do not map automatically onto meaning can be reconstructed by reprocessing them within the context of semantic predictability.

The fronto-parietal network seen here might also reflect monitoring and selection processes more commonly associated with attention than only maintaining information in short-term memory (Lebedev et al., 2004). This interpretation postulates that the prefrontal cortex has a role in directing attention to relevant auditory features, to guide both short-term memory and access to long-term memory representations (for review, see Miller and Cohen, 2001). Most relevant to comprehending distorted speech in a sentence context is the concept of competition among lexical and phonological candidates, because signal degradation introduces considerable ambiguity. A recently suggested framework for the prefrontal cortex and conceptual selection problems (Kan and Thompson-Schill, 2004) would imply that the system for speech perception has to solve problems associated with lexical selection. Because of the acoustic ambiguity, each key word might activate multiple possible word candidates. With high semantic coherence, top-down influences guide correct lexical selection, but with low semantic coherence, lexical selection will be much less successful. For such selection and competition processes, the left prefrontal cortex is engaged (Tippett et al., 2004). Also, top-down control of selective attention in our study might encompass the on-line formation of increasingly specific hypotheses about which sentence-final word to expect in a degraded yet predictable sentence. This in turn would enable more thorough and, ultimately, more successful (re-)analysis of the noise-vocoded signal as more elements of the sentence become available.

Finally, the facilitation through context in the current stimulus set is likely to entail a range of possible subordinate lexical mechanisms by which predictability supports comprehension. Both verb semantics (by narrowing down the context) and semantic associations in general (by allowing to “prime” for other word candidates) are possible influences here (Kalikow et al., 1977; Friederici and Kotz, 2003), a matter to disentangle in additional studies.

To summarize, successful speech perception under less than ideal listening conditions depends on greater functional integration across a very distributed left-hemispheric network of cortical areas. Therefore, speech perception is facilitated when high-order cognitive subsystems become engaged, and it cannot be considered as the product of processing within the unimodal auditory cortex alone (Jacquemot and Scott, 2006).

A clear lateralization to the left was observed. Left-hemisphere predominance is often absent from studies of speech perception and comprehension, and it was by and large absent in the main effect of intelligibility results in the present study (Fig. 2). Thus, it appears that only once higher-order processes interact with downstream perceptual systems is the left lateralization established. Notably, left- and right-hemispheric temporal cortices also varied in their degree of responsiveness to the entirely unintelligible sounds of rotated speech: as can be seen in Figure 2, right STS areas show near-baseline activation in response to rotated speech, whereas the left STS area clearly exhibits a relative deactivation [compare previous findings on rotated speech (Scott et al., 2000; Narain et al., 2003)].

Interestingly, Broca's area (BA 44/45) was not activated differentially by high and low predictability despite its known role in rule-based processing also in speech. Its response pattern was statistically indistinguishable from the anterolateral STS (Fig. 2). Thus, structural processing of the language content in our set of stimuli may only have become possible once a certain level of signal quality was attained, and that it increased further as perceptual ambiguity was overcome.

By using a factorial design, parametric degradation of the speech signal and an acoustically matched unintelligible baseline, we have not only been able to confirm the network of cortical areas that respond to speech intelligibility (Binder et al., 2000; Scott et al., 2000, 2004; Davis and Johnsrude, 2003; Obleser et al., 2006; Zekveld et al., 2006) but have demonstrated the dynamic changes within the network that occur when intelligibility and semantic context interact. This captures the nature of speech perception under real-life conditions.

In conclusion, the combination of two established manipulations of speech, one acoustic (spectral degradation through noise vocoding) and the other linguistic (semantic predictability), allowed us to demonstrate a widely distributed left-hemisphere array of cortical areas that can establish speech perception under adverse listening conditions. These areas are remote from the unimodal auditory cortex in high-order heteromodal and amodal cortices. Their functional connectivity is strengthened when semantic context has a beneficial influence on speech perception.