Elsevier

Journal of Communication Disorders

Volume 40, Issue 1, January–February 2007, Pages 1-41
Journal of Communication Disorders

Stuttering in adults: The acoustic startle response, temperamental traits, and biological factors

https://doi.org/10.1016/j.jcomdis.2006.04.001Get rights and content

Abstract

The purpose of this study was to investigate the relation between stuttering and a range of variables of possible relevance, with the main focus on neuromuscular reactivity, and anxiety. The explorative analysis also included temperament, biochemical variables, heredity, preonset lesions, and altered auditory feedback (AAF). An increased level of neuromuscular reactivity in stuttering adults has previously been reported by [Guitar, B. (2003). Acoustic startle responses and temperament in individuals who stutter. Journal of Speech Language and Hearing Research, 46, 233–240], also indicating a link to anxiety and temperament. The present study included a large number of variables in order to enable analysis of subgroups and relations between variables. Totally 32 stuttering adults were compared with nonstuttering controls. The acoustic startle eyeblink response was used as a measure of neuromuscular reactivity. No significant group difference was found regarding startle, and startle was not significantly correlated with trait anxiety, stuttering severity, or AAF. Startle was mainly related to calcium and prolactin. The stuttering group had significantly higher scores for anxiety and childhood ADHD. Two subgroups of stuttering were found, with high versus low traits of childhood ADHD, characterized by indications of preonset lesions versus heredity for stuttering. The study does not support the view that excessive reactivity is a typical characteristic of stuttering. The increased anxiety is suggested to mainly be an effect of experiences of stuttering.

Learning outcomes: As a result of reading this article, the reader will be able to: (a) critically discuss the literature regarding stuttering in relation to acoustic startle, anxiety, and temperament; (b) describe the effect of calcium on neuromuscular reactivity; (c) discuss findings supporting the importance of early neurological incidents in some cases of stuttering, and the relation between such incidents and traits of ADHD or ADD; and (d) discuss the role of genetics in stuttering.

Introduction

Stuttering is a frequent speech disorder which, if persistent, often has far-reaching psychological and social effects for the affected persons. The etiological mechanisms are still unclear, though research has shown the influence of genetical factors in many cases (Ambrose, Cox, & Yairi, 1997; Riaz et al., 2005, Shugart et al., 2004; Viswanath, Lee, & Chakraborty, 2004; Yairi & Ambrose, 2005). There are also indications of non-genetic influence. The nature of such non-genetic factors is not clear, but various types of neurological incidents are likely contributors (Böhme, 1968; Poulos & Webster, 1991; Segalowitz & Brown, 1991; West, Nelson, & Berry, 1939).

The possible roles of psychological factors, such as anxiety and a “sensitive” temperament, are matters of debate (Alm, 2004b; Craig, Hancock, Tran, & Craig, 2003; Ezrati-Vinacour & Levin, 2004; Guitar, 2003; Oyler, 1994). One possible link between temperament and stuttering is that stuttering persons tend to have an increased level of neuromuscular reactivity, resulting in exaggerated muscular reflexes and difficulties to regulate force and speed when talking. This possibility is supported by a recent report of increased “acoustic startle” in stuttering persons, i.e., increased blink reflexes in response to a surprising loud sound (Guitar, 2003).

A physiological factor known to affect the level of neuromuscular reactivity is calcium: the excitability of the nervous system is directly related to the level of calcium in the blood, so that low calcium can lead to tetany (Guyton & Hall, 1996). It is therefore of interest that Costa, Antoniac, Berghianu, and Marinescu (1986) reported low levels of calcium in stuttering children and adults.

Another trace in the search of the causes of stuttering has lead to the neural transmitter dopamine. Wu et al. (1997) reported about 3-times higher cerebral uptake of a precursor of dopamine, in a study of three stuttering adults. Dopamine receptor blockers is the type of medication that has shown the best documented effect on stuttering (Brady, 1991). The level of dopamine in the pituitary serves as the main regulator of the release of the hormone prolactin into the peripheral blood stream (Ben Jonathan & Hnasko, 2001). With this background the plasma level of prolactin has been suggested to be an index of cerebral dopamine activation (Appelberg et al., 2000). As far as we know the level of prolactin has not been investigated in persons who stutter.

A striking aspect of stuttering is the often dramatic improvement of fluency shown during altered auditory feedback (AAF), like frequency altered feedback (FAF) or delayed auditory feedback (DAF) (Kalinowski, Armson, Roland-Mieszkowski, Stuart, & Gracco, 1993). However, the mechanism behind this effect is not well understood. One hypothesis might be that the auditory feedback is too strong in some stuttering persons. If so, this excessive auditory influence might also be shown as exaggerated acoustic startle in stuttering persons, which, as mentioned above, was reported by Guitar (2003). If the fluency-inducing effect of AAF is related to acoustic hyper-sensitivity, then a correlation should exist between the acoustic startle response and the effect of AAF.

To be able to analyze relations between variables, and to analyze subgroups, it is important to study all the relevant variables in the same group of individuals. This paper is an attempt to investigate the aspects mentioned above in adults who stutter, partly as tests of hypotheses and partly as an explorative study. Before continuing to Section 2 a more detailed review and analysis of the literature follows below.

As mentioned above, stuttering has been suggested to be related to an emotionally reactive and sensitive temperament, both in older (Hill, 1944) and in contemporary research (Guitar, 2003, Oyler, 1994). Hill (1944) suggested that the basic mechanism of stuttering is the muscular contraction pattern “of shock, startle or surprise” (p. 319). Startle responses can be elicited by surprising acoustic, tactile, or visual stimuli with sufficient strength. The startle response can be measured either as changes in autonomic measures, such as heart rate, or as muscular contractions like the eyeblink reflex. It has been shown that the amplitude of the startle response is modulated by the current emotional state, with larger response when viewing unpleasant pictures and smaller response when viewing pleasant pictures (Vrana, Spence, & Lang, 1988). Likewise, increased startle responses have been shown during anticipatory anxiety (Grillon, Ameli, Woods, Merikangas, & Davis, 1991). Exaggerated startle responses may occur without signs of other abnormalities, but may also be part of neurological or psychiatric syndromes (Howard & Ford, 1992).

Walker and Walker (1973) found no difference in heart rate changes between stuttering and non-stuttering persons when exposed to bursts of loud white noise (105 dB SPL), but higher response in the stuttering group as a result of bursts of low-level noise (65 dB SPL). In a recent study Guitar (2003) reported 81% higher mean amplitude of eyeblink startle responses, for the first trial, in a group of 14 stuttering adults compared with controls. The stimulus was a burst of 95 dB white noise. Furthermore, the amplitude of the startle eyeblink in this study was reported to correlate with a scale of “Nervous” temperament (r = 0.39). The stuttering group had significantly higher scores on the Nervous scale. Chokroverty, Walczak, and Hening (1992) proposed that individuals showing abnormally strong startle responses also are characterized by reduced habituation. However, on the contrary, Guitar (2003) found somewhat stronger habituation of startle in the stuttering group.

The acoustic startle blink reflex is fast, appearing about 30–50 ms after the sound, with contraction of the orbicularis oculi muscle. The exact pathway from the ear to the motor nuclei is debated, but is suggested to include only two brainstem synapses before the final synapse in the facial motor nucleus. The startle response has been found to be potentiated by fear-related signals from the amygdala and nearby structures, to the brainstem (Davis, Walker, & Lee, 1999). This mechanism may be interesting in relation to stuttering, since it has been suggested that stuttering could be related to increased gain of brainstem reflexes (Zimmermann, 1980). Measurements of the startle eyeblink might possibly reflect the gain of brainstem reflexes related to speech motor control.

As discussed above, a relation might exist between stuttering and low levels of calcium: (a) reduction of the plasma concentration of calcium makes the nervous system progressively more excitable, and (b) Costa et al. (1986a) reported low calcium in a group of stuttering persons, especially for the level of free, ionized calcium. About 50% of the total calcium in the blood plasma exists in a free, ionized, and unbound form. It is this free calcium that is biologically active, and affects the nervous system (Burties & Ashwood, 1999).

It is difficult to evaluate the reliability of the low calcium levels in stuttering persons reported by Costa and coworkers (1986), because the figures for the control persons were taken from the literature and were not analyzed in the same laboratory as the samples from the stuttering persons. Anyhow, it is interesting that Costa et al. found significantly lower mean levels of free calcium in stuttering persons showing grimaces or other involuntary movements, compared with stuttering persons not showing such behaviors (effect size 0.45). This finding suggests that a low level of free calcium may be a relevant factor especially in stuttering persons showing signs of increased muscular activity.

It is easy to imagine that increased neuromuscular excitability can make stuttering worse, as a result of increased muscular tension, more rapid articulatory movements, etc. Furthermore, it might be speculated if low plasma calcium could have cerebral effects increasing the risk of stuttering. In Alm (2004a) a model was suggested where increased gain of the basal ganglia-thalamocortical circuits may be a key aspect in some cases of stuttering, resulting in symptoms of dystonia. The level of plasma calcium might be a factor which directly affects the gain of these circuits. Actually, severe calcium deficiency may cause seizures as a consequence of heightened excitability of the brain (Guyton & Hall, 1996). Another aspect of deficient levels of calcium is that it may result in mental changes, like increased anxiety, but also increased irritability, depression, and paranoia (Morrison, 1999).

Another mineral of relevance for the discussion is magnesium. Reduction of the plasma magnesium concentration results in a decreased threshold for signals in the nervous system, with increased nerve conduction velocity and neuromuscular excitability. Magnesium is also required for the function of more than 300 enzymes (Burties & Ashwood, 1999). In a study by Schleier, Schelhorn, and Groh (1991) 47% of 53 stuttering children were claimed having hypomagnesemia, which, however, has not been confirmed.

The most well-known function of prolactin is to stimulate lactation in mothers, but this hormone is prevalent also in men and non-lactating women, and is involved in the metabolism of calcium and Vitamin D (Burties & Ashwood, 1999).

The plasma level of prolactin is mainly regulated by the inhibiting effect of dopamine released from the hypothalamus to the pituitary (Ben Jonathan & Hnasko, 2001). The plasma level of prolactin thus has been suggested to be an index of cerebral dopamine activation. Based on the dopamine hypothesis of schizophrenia, decreased levels of prolactin would be expected in schizophrenic patients, which, however, several studies have failed to find (Appelberg et al., 2000). Nonetheless, there is some support of a connection between the level of plasma prolactin and the cerebral dopamine activation: Strong correlations have been reported between low serum prolactin and high frequency of hallucinations (Appelberg et al., 2000) and REM sleep (Appelberg et al., 2002) in non-affective psychosis.

It should be noted that the level of plasma prolactin also is affected by acute stress. Parachute jumps (Schedlowski, Wiechert, Wagner, & Tewes, 1992) and academic exams (Armario, Marti, Molina, de Pablo, & Valdes, 1996) have been found to significantly increase prolactin. Other factors reported to increase the level of prolactin are antidepressants (SSRIs) (Emiliano & Fudge, 2004) and estrogen (Oliveira, Moraes, Barros, & Barbosa-Coutinho, 1996).

Are stuttering persons predisposed to anxiety reactions? In line with this suggestion, several studies have reported higher levels of trait anxiety or “nervousness” in stuttering adults (Craig, 1990, Craig et al., 2003; Ezrati-Vinacour & Levin, 2004; Guitar, 2003). However, Miller and Watson (1992) found no difference between stuttering adults and the controls, and Embrechts, Ebben, Franke, and van de Poel (2000) reported somewhat lower scores for shyness, fear and sadness in stuttering preschool children compared with nonstuttering controls, though not statistically significant. An interesting result was reported by Craig (1990). This study showed that the measure of trait anxiety decreased after stuttering therapy, resulting in somewhat lower scores for trait anxiety in the stuttering group compared with the controls. This result indicates that the tendency towards an increased level of “trait” anxiety in stuttering adults mainly is a secondary effect of living with stuttering, and not a constitutional trait.

In this context it is important to examine the content of the questionnaires used in these studies. All of the studies of anxiety mentioned above, except Guitar (2003), have used the Spielberger State and Trait Questionnaires (STAI) (Spielberger, Gorsuch, Lushene, Vagg, & Jacobs, 1983). When looking at the 20 items in the questionnaire for STAI-Trait, a large portion of them can be assumed to be sensitive to the fact that a person is living with stuttering. Stuttering implies an unpredictable impairment of social communication, an impairment that is poorly understood and sometimes stigmatizing. Examples of STAI-Trait items likely to be affected by the problems of stuttering: “I feel nervous and restless”, “I feel satisfied with myself”, “I wish I could be as happy as others seem to be”, “I feel like a failure”, “I am calm, cool and collected”, “I feel that difficulties are pilling up so that I cannot overcome them”, “I am happy”, “I lack self-confidence”, “I feel inadequate”, “I am content”.

In the study by Guitar (2003) the Nervous subscale of the Taylor-Johnson Temperament Analysis (Taylor & Morrison, 1996) was used. Also this scale can be expected to be affected by secondary effects of stuttering, though probably to a lesser degree than the STAI-Trait. Examples of problematic items: “Do you usually feel calm and relaxed”, “Are you usually free from worry”, “Do people think of you as a nervous ‘high-strung’ person?”.

A general conclusion would be that these instruments intended to measure trait anxiety are likely to have problems of validity if applied to groups suffering from conditions which make life situations difficult and unpredictable. For example, it seems likely that also persons with impaired sight or dyslexia would tend to score higher on STAI-Trait, as a result of their difficulties.

A recent study by Messenger, Onslow, Packman, and Menzies (2004) focused expectancy of social harm in stuttering adults. The results indicate that the clinical population of people who stutter tend to have increased anxiety in relation to situations involving social interaction and social evaluation, but not in relation to situations without these social aspects. The key issue seemed to be fear of negative evaluation in social situations, a fear which can be viewed as rational considering the nature of their impediment.

In summary, the studies indicate that stuttering adults, as a group, tend to experience an increased level of anxiety in relation to social situations due to fear of negative evaluation as a result of their speech difficulties. The interpretation that this increased anxiety mainly is a secondary effect of the stuttering is supported by: (a) the result from Craig (1990), that stuttering adults after stuttering therapy showed somewhat lower scores of “trait anxiety” than the control group; (b) the result from Messenger et al. (2004), that the increased anxiety is limited to social situations; and (c) the result from Embrechts et al. (2000), that stuttering preschool children got somewhat lower scores for shyness and fear compared with the non-stuttering controls.

Empirical studies of temperament in persons who stutter have yielded mixed results, sometimes contradictory. Embrechts et al. (2000) investigated the temperament in stuttering children aged 3–7 years. The results indicated that the stuttering group had a significantly higher level of gross motor activity and impulsivity, and significantly lower attentional focusing, inhibitory control (capacity to suppress inappropriate approach responses), and perceptual sensitivity (detection of low intensity stimuli). As mentioned in the previous section, the stuttering group had somewhat lower scores of shyness, fear, and sadness, though not statistically significant. In a study of children aged 7–12 years Oyler (1994) reported higher “sensitivity” in the stuttering group. Other significant differences were higher frequency of problems of learning, language, attention, and motor coordination.

Wakaba (1997) classified 5 of 13 stuttering children aged 2–3 years as “difficult children”, i.e., 38% of the group, to be compared with an expected proportion of about 10%. “Difficult children” were defined as being slow to adapt to new environments, and being irregular in feeding and sleeping. These characteristics were also reported by Anderson, Pellowski, Conture, and Kelly (2003) who studied stuttering preschool children. The stuttering group was found to show less adaptability to change and to have irregular biological functions. This group was also reported to show “less distractibility”, based on low scores on questions like “the child stops an activity because something else catches his/her attention” (p. 1225).1

In summary, these studies of stuttering children seem to describe frequent traits of Attention Deficit Hyperactivity Disorder (ADHD) or Attention Deficit Disorder without hyperactivity (ADD): excessive motor activity, impulsiveness, inattention, problems of learning, and delayed motor development (Schachar & Tannock, 2002). The trait “less distractibility”, reported by Anderson et al. (2003), might possibly reflect attention deficit without hyperactivity.

Other studies do, however, give the opposite picture: that stuttering children are “easy children”, with a high level of mental abilities. Lewis and Golberg (1997) found that a group of 11 stuttering children aged 3–5 years had significantly higher scores for being “easy children” compared with the control group. The typical traits of the stuttering group were “rhythmicity, a positive approach to new stimuli, high adaptability to change, and a mild or moderately intensive mood which is generally positive” (p. 447). Schilling and Weiss (1963) reported that in a study of 50 children aged 10–14 years, the stuttering group actually showed better results than the control group on tests of concentration. Furthermore, Watkins, Yairi, and Ambrose (1999) found that children with early onset stuttering, entering their study at age 2–3, showed language abilities which in some aspects were on level with the norms for children 2 years older. However, children with later onset of stuttering, entering the study at age 4–5, showed language abilities somewhat below the norm.

Also another study should be mentioned in this context, Fowlie and Cooper (1978), as it is still used as an argument for a reactive temperament in persons who stutter. Fowlie and Cooper asked the mothers of 34 stuttering and 34 nonstuttering school-aged male children to choose among adjectives that characterized their sons. The stuttering children were described as being more insecure, sensitive, anxious, withdrawn, fearful, and introverted. The authors concluded that this attribution of characteristic personality traits of persons who stutter was still common, though research had failed to confirm this pattern. Firstly, the reported traits may be secondary to the stuttering, because these children had experienced speech difficulties for several years. Secondly, it is also likely that stuttering per se often is interpreted as a sign of insecurity, etc., even if insecurity is not really a trait of the child. In conclusion, this study cannot be used as support for the existence of basic temperamental traits in persons who stutter.

A reasonable interpretation of the conflicting results reviewed above is that stuttering children constitute a heterogeneous population, consisting of at least two subgroups: one group with traits of ADHD or ADD, and one group that is well adapted, with tendency to be “easy children”, having good skills of concentration, and well developed language abilities. In summary, none of the reviewed studies of temperament have presented convincing arguments for the hypothesis that increased sensitivity or reactivity is a contributing factor in the development of stuttering. Reported temperamental differences can well be explained as either secondary effects of the stuttering or as epiphenomena, i.e., that traits such as impaired attention share a common causal factor with the stuttering (see further discussion in Section 4.5.1). The strongest support for increased reactivity seems to come from the study of the acoustic startle response, by Guitar (2003).

There are several indications in the literature concerning the role of early brain damage in stuttering. Böhme (1968) investigated a group of 802 children and adults with supposed cerebral lesions, related to prenatal, perinatal, or childhood adverse events. He found a very high prevalence of stuttering. Among the 313 persons with normal intelligence 24% were diagnosed as stuttering. Interestingly, the percentage of stuttering cases was positively related to the level of intelligence, with lower prevalence of stuttering in the groups with impaired intelligence (only 2.4% in the group with lowest intelligence). It may be mentioned that five out of five children with the combination of premature birth and forceps delivery stuttered. Six of eleven children who had suffered concussion were reported to stutter (Böhme, 1977).

The possibility of subtle neurological lesions in some cases of stuttering is supported by reports of an increased prevalence of impaired motor coordination. Schilling and Krüger (1960) studied 100 stuttering children and 100 controls, using a comprehensive gross motor test. In the control group 12% were categorized as having a moderate motor delay and 5% as having a severe delay, to be compared with 21 and 18% of the stuttering children., i.e., a 2.3-times higher prevalence of either moderate or severe motor delay in the stuttering group.

In an early study West et al. (1939) analyzed the frequency of certain types of events associated with the onset of stuttering, comparing cases of stuttering with and without stuttering relatives (104 and 100 stuttering cases in respective group). This comparison resulted in the following number of reported events for the two groups2: (a) infectious disease: 24 versus 45 persons, p = 0.001; (b) diseases of the nervous system: 10 versus 27, p = 0.002; (c) injuries: 0 versus 13, p = 0.0001; and (d) surgery: 3 versus 10, p = 0.005.

The same overall tendency was reported by Poulos and Webster (1991). In this study such early childhood factors were found in only 3 of 112 cases with stuttering relatives, to be compared with 21 of 57 cases without family history (p < 0.00005, Fisher's exact test). Most of these factors were physical in nature, such as head injury or birth complications, but also three instances of intense fear were included among the 24 cases with reported incidents.

The difference in absolute figures between the reports by West et al. (1939) and Poulos and Webster (1991) is striking: in 1939 a total of 132 incidents were reported by 204 cases,3 to be compared with 24 incident in 169 cases 1991. We do not know if this reflects a difference in how the investigation was done, or if it indicates a real change in the stuttering population: that stuttering caused by physical incidents has become less common because of improved general health and health care. Anyway, the large difference in frequency of incidents between the groups with and without stuttering relatives, in both studies, strongly supports that this type of events actually were related to the onset of stuttering.

The issue of physical factors related to the onset of stuttering was discussed in Yairi and Ambrose (2005). In a renewed analysis of their recent data they found that 14% of the children were reported to have experienced illness or excessive fatigue just prior to the onset.

As mentioned above, Böhme (1977) reports that 6 of 11 children who had suffered concussion developed stuttering, with onset of stuttering varying from hours up to 2 months after the accident. According to Böhme (1968) was this stuttering mainly characterized by repetitions.

Segalowitz and Brown (1991) investigated the role of head injuries in the etiology of developmental disabilities. In a survey of high-school students 15.6% of 607 nonstuttering adolescents reported head injury with unconsciousness, in contrast to six of the nine stuttering students in the survey (i.e., 67%). The frequency of all reported head injuries, also without unconsciousness, was 30.3% in the nonstuttering group to be compared with eight out of nine stuttering persons.

A case of adult onset stuttering after concussion, with no identifiable brain lesion, was reported by Rousey, Arjunan, and Rousey (1986). A 41-year-old male developed severe stuttering the same day as he had a car accident with brief unconsciousness. Singing and reading in unison were normal. In this case the stuttering almost completely resolved after 3 months, with speech therapy.

If concussion is related to onset of stuttering in some cases, what might be the mechanism? In Alm (2004a) a model was suggested where stuttering is related to disturbances of the basal ganglia motor circuits, caused for example by dysregulation of the dopamine system or by focal lesions. In this context it is interesting that the main mechanism behind the symptoms of concussion, like unconsciousness, is assumed to be rotational forces centered at the brainstem at the level of the midbrain and the subthalamic nucleus (Victor & Ropper, 2001). The concussion often causes a rotational movement of the brain in relation to the skull, and since the brainstem is fixed this movement may result in diffuse axonal injuries (which may be reversible to some extent). Axonal injuries in this region might affect several different basal ganglia pathways, such as the indirect pathway, the output from the basal ganglia to the thalamus, the dopaminergic output from the substantia nigra, or the input to the substantia nigra that regulates the dopamine release. In summary, it would not be surprising if concussion sometimes resulted in diffuse basal ganglia disturbances. This possible mechanism of basal ganglia dysfunction might also be involved in the frequent appearance of ADHD traits after closed head injuries (Max et al., 2004).

The review above clearly indicates that various types of early neurological incidents contribute to the onset of stuttering in a substantial subgroup of stuttering children.

It now seems clear that genetic factors are essential for the development of many cases of stuttering. A detailed understanding of these genes is likely to contribute profoundly to our view of stuttering. There are indications that the genetic basis of recovering childhood stuttering and persistent stuttering is at least partly different (Ambrose et al., 1997). This means that when discussing the genetics of stuttering it is important to consider whether the studies refer to recovering or persistent stuttering. It has also been shown that the risk for persistent stuttering is higher for males, with a reported male-to-female ratio of 3.75:1 in the persistent group to be compared with 2.33: 1 in the recovered group (Yairi & Ambrose, 2005).

The exact mode of genetic transmission is not yet clear, and it is possible that it differs between different populations. The analyses summarized by Yairi and Ambrose (2005) suggest the existence of a major gene that increases the risk for stuttering, in combination with polygenetic factors. Based on segregation analysis of 56 pedigrees with permanent stuttering Viswanath et al. (2004) found a pattern of inheritance that was compatible with one major dominant gene, with Mendelian transmission (the Mendelian inheritance was, however, questioned by Riaz et al. (2005)). According to this model, the penetrance of this gene depends on the sex and whether or not the parents stutter: with no stuttering parent the penetrance for carriers of the gene was 38% for males and 7% for females, but increased to 67% and 19%, respectively, if one parent stuttered. According to Viswanath et al. the risk for persistent stuttering is negligible for persons who do not carry this gene. However, it might be questioned if the sample obtained by Viswanath et al. is representative for the general population of stuttering adults: In the study by Viswanath et al. 84% of the 56 probands reported stuttering relatives, while previous studies tended to have figures scattered around 50%. A result of this high number of probands with stuttering relatives might be that the influence of non-genetic factors is underestimated in this study.

Cox and Yairi (2000) performed a genome-wide linkage analysis of stuttering in the Hutterites, a genetically isolated group. This survey indicated genetic linkage for stuttering on chromosomes 1, 13 and 16. A similar analysis, of population from North America and Europe, reported a major locus on chromosome 18, with weaker linkage on chromosome 1, 2, 10 and 13 (Shugart et al., 2004), i.e., in partial agreement with the results from Cox and Yairi. Still another genetic linkage study, of Pakistani families, found a major locus on chromosome 12, but also showing evidence for linkage on chromosomes 1, 5, and 7 (Riaz et al., 2005). In summary, there are clear indications for a major role of genetic factors in the development of stuttering, but a single major gene has not yet been located. Instead it seems likely that a large number of different genes may contribute to increase the risk of stuttering.

This paper reports an attempt to investigate the possibility of increased sensorimotor reactivity in adults who stutter, by measuring the amplitude of eyeblink responses to an acoustic startle stimulus. Increased startle eyeblink amplitude may reflect temperamental traits or neurological aspects of the sensorimotor functions. Based on the results in Guitar (2003) we hypothesized that the stuttering group would show higher eyeblink amplitude compared with the control group, with the largest difference for the first startle trial.

The study also involved questionnaires for temperamental traits. Based on the results of Craig (1990), Craig et al. (2003), Guitar (2003), Ezrati-Vinacour and Levin (2004) tendencies of increased anxiety were expected in the stuttering group. Other scales of temperament were included as part of an explorative study. An interesting aspect of stuttering is the ability of altered auditory feedback (AAF) to instantly reduce stuttering in many cases (Kalinowski et al., 1993). In order to investigate if the effect of AAF is related to the amplitude of the startle response, an AAF index was determined and included in the explorative study. Blood samples were added by reason of the possibility that motor reactivity and anxiety might be influenced by for example low levels of calcium or magnesium, or by hyperthyroidism (Guyton & Hall, 1996; Morrison, 1999). Prolactin was included as a possible index of cerebral dopamine activation (Appelberg, Katila, & Rimon, 2000; Appelberg, Katila, & Rimon, 2002; Depue, Luciana, Arbisi, Collins, & Leon, 1994; Guyton & Hall, 1996). Furthermore, background factors regarding stuttering relatives and possible preonset neurological lesions were also analyzed in the explorative study.

Section snippets

Age and sex, total group

The total group of participants involved in this study consisted of 32 persons with developmental stuttering (24 males age 21–58, mean 41.0 years; 8 females age 19–47, mean 36.7), and 28 persons without speech problems (17 males age 26–60, mean 41.1; 11 females age 24–49, mean 34.4). For various reasons not all of these individuals were included in all parts of the analysis, see summary of participants in Table 1.

Recruitment and diagnosis

Seventeen of the total of thirty-two stuttering participants were previous

Group differences, startle

The analyses of startle amplitude resulted in only small and statistically nonsignificant group differences. The first of the two planned group comparisons, regarding startle amplitude of the first trial, showed no significant group difference (t(32) = 0.82, p = 0.21 one-tailed test). The study had a power of 0.93 to detect a difference in population means of the size reported by Guitar (2003). The nonsignificant tendency was a 20% higher mean startle amplitude in the stuttering group.

Table 2

Startle response and stuttering

Overall, the present study does not support the hypothesis that increased reactivity and a “sensitive” temperament are core features of stuttering. The mean startle amplitude for the first trial was only 20% higher for the stuttering group, not close to statistical significance (p = 0.42). This means that most stuttering persons in this study showed startle responses well within normal limits. Actually, the mean startle response for the total stuttering group was 7% lower than the average

Summary and conclusions

The following tentative conclusions are suggested, based on the data from this study in combination with the review of literature.

  • (a)

    Startle and stuttering: The analysis of startle amplitude in this study does not support the hypothesis that a reactive temperament is an important factor in stuttering.

  • (b)

    Startle and trait anxiety: The result indicates that startle amplitude is not a valid measure of trait anxiety.

  • (c)

    Determinants of startle: The primary determinant of startle amplitude was the level of

Acknowledgements

Per A. Alm and Jarl Risberg, both at Department of Clinical Neuroscience, Lund University, and Department of Psychology, Lund University.

The preparation of this article has been supported by grants from the Bank of Sweden Tercentenary Foundation, the Swedish Council for Research in the Humanities and Social Sciences, the Crafoord Foundation, the Royal Physiographic Society, and the Sjöbring foundation. We want to thank Ulla Ängqvist for assistance during the data collection and analysis, Jesper

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