Understanding Sex Differences in Developmental Stuttering

About the presenter: David M. Corey, PhD. As a graduate student, Dr. Corey studied perception with Steven Flynn and statistics with Bill Dunlap in Tulane's Department of Psychology. Having become fond of New Orleans, he remained after graduate school as a fellow in Anne Foundas' neuroimaging laboratory in Tulane University Health Sciences Center's Department of Psychiatry and Neurology. He subsequently returned to Tulane's main campus, where he continues to work as faculty in the Department of Psychology and the Neuroscience Program.

Understanding Sex Differences in Developmental Stuttering

by David M. Corey
from Louisiana, USA

Developmental stuttering (DS) is characterized by unintended repetitions and prolongations of speech sounds as well as temporary failures to produce any speech (blocks or hesitations). The word "developmental" indicates that fluency problems begin spontaneously during childhood. Although brain damage caused by injury or stroke can sometimes cause unintended dysfluencies, this condition is distinct from DS and is instead described as "acquired stuttering." DS occurs in about 4% of young children, about 75% of which recover by early adulthood. The remaining 25% (1% of the population) stutter throughout adulthood (Andrews, Morris-Yates, Howie, & Martin, 1991; Ardila, et al., 1994; DSM-IV, 1994). DS is strongly linked to sex, with males being more likely than females to stutter and less likely than females to recover. The result is that the M:F sex ratio increases from about 2:1 among children to about 4:1 to 5:1 among adults (Ambrose, Yairi, & Cox, 1993; Ambrose, Cox, & Yairi, 1997; Drayna, Kilshaw, & Kelly, 1999; Yairi, Ambrose, & Cox, 1996; Yairi, Ambrose, Paden, & Throneburg, 1996).

Although these and other characteristics of DS are well-known, we have yet to answer many of the most important questions about DS. Despite much study, we still do not know what causes DS or why some people recover and others do not. This paper was motivated by the notion that we might look to the large sex difference in DS prevalence for information that may move us closer to understanding the origins of DS. For example, might we consider characteristics that are linked to sex in the general population, as potential causes of the sex difference in DS? Are males at greater risk for DS because they are, on average, different from females in some characteristic that is related to production of fluent speech? A great many human sex differences are known, from hair growth to cognitive function. Most of these differences cannot in any reasonable way be linked to speech fluency. However, some sex differences in the normally-fluent population are intimately related to speech fluency. For example, consider speech feedback. Speech feedback, or auditory feedback, refers simply to the sound that leaves a talking person's mouth and then is heard by the talking person. We each hear our own voice while talking and, though we may not realize it, we use this feedback to adjust the way we speak. For example, you might occasionally have found yourself talking much more loudly than you intended because while you were talking you were listening to music through headphones. Because the amplified music makes hearing our own speech difficult, we unconsciously increase the volume of our speech until we can hear it above the music. What makes auditory feedback relevant in a discussion of DS is the effect of altering the auditory feedback itself. Certain manipulations of speech feedback can have strong effects on speech fluency. And, much like males are at higher risk than females for DS, males are more susceptible than females to these alterations of speech feedback. The remainder of this paper will be dedicated to the discussion of sex differences--primarily among normally-fluent people--in the effects of auditory feedback, and to the proposition that understanding why these sex differences exist may move us toward a better understanding of sex differences in the prevalence of DS, and in turn to the causes of DS.

Delayed Auditory Feedback

Auditory speech feedback is available whenever a talking person can hear his or her own voice. If a talker's voice is recorded with a microphone, the speech can be stored electronically for a short time (usually less than 300ms) and then replayed through speakers or headphones to the person who produced the speech. This stimulus is known as "delayed auditory feedback," or "DAF." DAF is interesting for several reasons. First and foremost, DAF can have strong effects on speech fluency. Many people who typically have no trouble producing fluent speech become dysfluent when exposed to DAF. Whereas DAF can cause dysfluencies in normally-fluent people, it can decrease or eliminate dysfluencies in people who stutter. In fact, a variety of alterations of speech feedback can improve the fluency of people who stutter; other examples are altering the pitch of auditory feedback (frequency altered feedback) and combining oral reading feedback with the sound of other people reading the same passage in time with the person who stutters (choral reading). However, DAF is the only type of feedback alteration that affects the fluency of normally-fluent individuals. As a group, the effects of these stimuli suggest that auditory processing plays a role in the production of fluent speech, both in people who stutter and in fluent controls.

Sex Differences in DAF Effects

As mentioned above, DAF's disruption of speech in normally-fluent people is stronger in males than in females (Bachrach, 1964; Corey & Cuddapah, 2008; Fukawa, Yoshioka, Ozawa, & Yoshida, 1988; Sutton, Roehrig, & Kramer, 1963). Very little is known of the corresponding sex difference in people who stutter; little has been reported in the scientific literature and the sparse data available do not clearly indicate whether a sex difference in DAF effects exists among people who stutter. Whereas some have found data suggestive of such a sex difference (Grosser, Natke, Langefeld, & Kalveram, 2000), others have not (Fukawa et al., 1988). In short, DAF disrupts speech more in fluent males than females; however, sex differences in DAF effects among PWS have very rarely been measured, and no conclusion can be drawn given the data presently available.

Developmental Changes in the Relationship between Sex and DAF Effects

Studies of developmental changes in the effects of DAF appear in the literature but are rare and have not been replicated in recent decades. These results suggest that the effects of DAF are greater for older children (7-9 yrs.) than younger children (4-6 yrs.; Chase, Sutton, First, & Zubin, 1961) and that the feedback delay interval maximizing dysfluency may decrease developmentally (MacKay, 1968). Only one report on developmental changes in sex differences in DAF effects was found in the literature. In this study, significant sex differences were observed in 7, 11, and 13 year old children, but not in 5 or 9 year olds (Timmons & Boudreau, 1976). This result may suggest that sex differences in DAF effects increase with increasing age. The older age range corresponds to the age range at which people who stuttered as children report having stopped stuttering (Martyn & Sheehan, 1968; Shearer & Williams, 1965; Wingate, 1964). This correspondence might suggest a developmental stage during which sex differences rise in both (a) DS prevalence and (b) DAF's dysfluency-inducing effects. The roughly-coincident changes in DS recovery (which is less likely for males than females) and in DAF effects (which are stronger for males than females) may suggest that developmental changes in some factor that is related to speech fluency is driving sex differences both in those who stutter and in those who do not. In other words, sex differences in various aspects of speech fluency may be mediated by some undiscovered factor impacting speech production (see Figure 1).

This is not to imply that dysfluencies produced by normally-fluent people during DAF presentation are the same as dysfluencies caused by DS. Although DAF effects have been discussed as a model for DS from the discovery of DAF (Lee, 1950) through relatively recent work (e.g., Saltuklaroglu, Kalinowski, & Guntupalli, 2004), DAF-disrupted speech and DS are clearly different, even to the untrained ear (Neelley, 1961). For example, DAF causes dysfluencies that are scattered throughout speech, whereas DS causes dysfluencies that tend to occur at the beginnings of utterances (Venkatagiri, 1982). Also, Corey and Cuddapah (2008) recently showed that DAF affects speech characteristics that are not affected by DS, including reading errors, interjections, articulation errors, and speech rate.

Corey and Cuddapah (2008) also observed the expected sex differences in DAF effects, with DAF affecting speech more in males than females. To test the correspondence between sex differences in DAF effects and in DS risk, Corey and Cuddapah tested DAF effects on stutter-like dysfluencies and on other speech characteristics separately. The prediction was that if the two sex differences are linked, then sex differences in DAF effects would be limited to DAF effects that are most similar to the dysfluencies associated with DS, but that sex differences would not be observed for DAF effects that are dissimilar to DS symptoms. As predicted, DAF effects on dysfluencies associated with DS--prolongations, repetitions, and blocks--showed sex differences; however, DAF effects on other speech characteristics--reading errors, interjections, articulation errors, and speech rate--did not vary with sex. In summary, although DAF-induced speech disruption in normally-fluent people is not a perfect model of DS, the selectivity of the sex differences in DAF's effects is consistent with a link between sex differences in DS and sex differences in DAF effects.

This discussion has revolved so far around the proposition that males are at risk for fluency problems as a result of a population-wide sex difference in some unknown factor. In other words, males tend to score higher (or lower) than females on a factor that increases risk for DS and also increases susceptibility to DAF in those without any history of DS. However, no specific factors have been suggested. In the next section selective attention is briefly considered as a candidate factor.

Attention

Attention determines the relative salience to an organism of myriad environmental features. "Selective" or "directed" attention is the intentional manipulation of attention to make some target aspect of the environment more salient than other aspects. During DAF presentation, individuals who can attend selectively to their natural, non-delayed speech might reasonably be expected to remain more fluent than individuals who are less able to focus attention selectively. And the converse may be true for people who stutter, with attention to the delayed speech maximizing the reduction of dysfluencies by DAF. In fact, when being fitted for SpeechEasy, a commercially-available device designed to treat DS, selective attention to DAF is explicitly instructed.

Attention and DS. Various researchers have described associations between DS and measures of attention (Angoosheev, 1975; Kalyagin, 1986; Knott & Johnson, 1936). A large literature also indicates that people who stutter are less fluent when attending to their speech, and are more fluent when distracted (see review by Bloodstein & Ratner, 2008, pp. 267-273). Further, a disproportionately high diagnosis of ADHD among people who stutter is consistent with a link between DS and attention. In short, a large amount of data from a variety of perspectives suggest a link between attention and DS.

Attention and Sex. Other investigators have reported gender differences in brain activation during auditory attentional tasks (recently, Goldstein et al., 2005; Simon-Dack, Friesen, & Teder-Sälejärvi, 2009). Various other studies suggest sex differences in attention (Anderson & Hugdahl, 1987; Bush, Korchin, Beall, & Kiritz, 1974; Dolu et al., 2004; Halley, 1975; Munro & Govier, 1993; Naglieri & Rojahn, 2001); however, neither sex has emerged as having superior global attention abilities, suggesting that sex differences in attention may depend on whether auditory, visual, or another type of attention is measured, or may depend on other non-sensory factors.

Although selective attention might reasonably explain sex differences in both DAF effects and DS prevalence, little is known about whether individual differences in the ability to attend selectively are associated with DAF effects in fluent or stuttering people. In the one study in which the goal was to assess a relationship between attention and DAF effects, Zelniker (1971) found that instruction to attend to non-delayed speech reduced disruption of speech during DAF presentation. No other studies were found. However, new data from the author's laboratory show that manipulating a talker's ability to hear his or her non-delayed speech significantly affected the frequency of dysfluency caused DAF effects, with reduced availability of non-delayed speech increasing DAF effects and vice versa. For example, in conditions in which participants whispered, virtually no non-delayed speech could be heard above the amplified delayed whisper. In these conditions, participants exhibited more dysfluencies than in conditions in which speech was voiced normally, allowing the talker to hear (and perhaps attend to) his or her non-delayed voice.

Conclusion

This paper has summarized the rationale for the proposition that the sex difference in susceptibility to DAF effects and the sex difference in DS prevalence are both caused by some factor(s) (1) linked to sex in the general population and (2) affecting fluency so as to make males more susceptible to DAF effects and at greater risk for DS. Reasons for considering selective attention ability as a candidate factor were presented. Data were summarized that support the existence of sex differences in attention, as were data suggesting an important role for attention in both DAF effects and DS.

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SUBMITTED: September 4, 2009