Elsevier

Neurobiology of Aging

Volume 32, Issue 8, August 2011, Pages 1505-1513
Neurobiology of Aging

Age-related changes in the functional neuroanatomy of overt speech production

https://doi.org/10.1016/j.neurobiolaging.2009.08.015Get rights and content

Abstract

Alterations of existing neural networks during healthy aging, resulting in behavioral deficits and changes in brain activity, have been described for cognitive, motor, and sensory functions. To investigate age-related changes in the neural circuitry underlying overt non-lexical speech production, functional MRI was performed in 14 healthy younger (21–32 years) and 14 healthy older individuals (62–84 years). The experimental task involved the acoustically cued overt production of the vowel /a/ and the polysyllabic utterance /pataka/. In younger and older individuals, overt speech production was associated with the activation of a widespread articulo-phonological network, including the primary motor cortex, the supplementary motor area, the cingulate motor areas, and the posterior superior temporal cortex, similar in the /a/ and /pataka/ condition. An analysis of variance with the factors age and condition revealed a significant main effect of age. Irrespective of the experimental condition, significantly greater activation was found in the bilateral posterior superior temporal cortex, the posterior temporal plane, and the transverse temporal gyri in younger compared to older individuals. Significantly greater activation was found in the bilateral middle temporal gyri, medial frontal gyri, middle frontal gyri, and inferior frontal gyri in older vs. younger individuals. The analysis of variance did not reveal a significant main effect of condition and no significant interaction of age and condition. These results suggest a complex reorganization of neural networks dedicated to the production of speech during healthy aging.

Introduction

Due to modern advances in healthcare, elderly individuals are a rapidly growing proportion of the population in industrialized nations. Considerable efforts are under way to understand the mechanisms of aging better and to unravel novel approaches to modify the aging process. Traditionally, normal aging has been regarded as an inevitable decline of cognitive, motor, and sensory functions, accompanied by brain atrophy and neuronal loss (Reuter-Lorenz and Lustig, 2005). Recently, converging evidence has suggested that age-related changes in behavior, brain structure, and brain function might be far more complex than previously thought. With the advent of functional brain imaging, in particular positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), it has become possible to compare brain activity associated with cognition (for an early study, see Grady et al., 1994), sensory processing (e.g., Cerf-Ducastel and Murphy, 2003), and motor tasks (e.g., Ward and Frackowiak, 2003, Heuninckx et al., 2005, Riecker et al., 2006) between younger and older individuals. In many of these studies, brain function of older participants has been characterized by overactivation in parts of the neural circuitry under investigation when compared with younger adults. These changes may result from neuroplastic changes in the aging brain that compensate for loss of sensorimotor function and contribute to maintaining of behavioral performance (Reuter-Lorenz and Cappell, 2008).

Speaking is one of the most complex and important human skills. During speaking, phonological plans are formed and executed at 5–10 syllables per second, using approximately 100 different muscles. In a previous study of younger adults, aged 22–32 years, we identified a large-scale articulo-phonologic network that mediates speech production (Sörös et al., 2006b). In younger adults, overt production of the isolated vowel /a/ was associated with the activation in bilateral cortical and subcortical motor centres. Activated cortical motor areas included the primary motor cortex, supplementary motor area, and cingulate motor area. Subcortical activation was found in the thalamus, globus pallidus, and putamen. These areas, together with their extensive interconnections, constitute the neural circuitry that controls initiation and execution of articulatory movements. In addition, production of an isolated vowel was associated with the activation in the bilateral superior temporal gyrus, reflecting phonological processing. The production of the polysyllabic utterance /pataka/ was associated with additional activation in the bilateral cerebellar hemispheres, which are crucial for the control of sequential movements. The production of polysyllabic utterances was also associated with stronger activation of the bilateral temporal cortex, reflecting an increase in phonological processing compared to the production of an isolated vowel.

Many older individuals experience difficulties and breakdowns in speech production, such as reduced speaking rate (Searl et al., 2002) and increased durations of segments, syllables, and sentences compared to younger adults (Smith et al., 1987). These age-related impairments in speech production are likely related to a decline in oro-facial motor control, as shown by decreased accuracy of movement amplitudes and increased temporal variability of movements (Ballard et al., 2001), as well as impairment of phonological processing, in particular the sequencing of phonological units (MacKay and James, 2004). Based on these behavioral findings and the results of previous functional brain imaging studies in younger adults, the aim of the present study was to compare the neural correlates of overt speech production between healthy older and younger adults using simple non-lexical utterances with varying complexity.

To study potential age-related changes in the neural correlates of speech production, whole-brain, blood-oxygenation dependent (BOLD) fMRI at 3 T was used. To minimize artifactual fMRI signal changes due to motion-correlated movements of the head and of the articulatory organs (Birn et al., 1999), clustered image acquisition (Edmister et al., 1999, Sörös et al., 2006b) was performed. Rather than the typical fMRI experimental design in which images are acquired repetitively at fixed time intervals, clustered acquisition leaves an extended silent interval for speech production and permits detailed scanning of the brain 5 s later (Gracco et al., 2005, Sörös et al., 2006b). Not only does the approach separate the rapid onset and offset of articulatory movements (and potential motion artifacts) from the comparatively slow rise of the BOLD signal (Birn et al., 2004), but the acoustic noise associated with imaging is also separated such that it does not have the potential to distract behavioral performance.

Section snippets

Participants

Blood oxygenation level dependent (BOLD) fMRI was acquired in a group of healthy younger volunteers (7 women, 7 men) with an average age of 25 years (range: 21–32 years) and a group of healthy elderly volunteers (7 women, 7 men) with an average age of 71 years (range: 62–84 years). All participants were right-handed and fluent speakers of English. Before inclusion into the study, volunteers were screened during a telephone interview for the past and present medical conditions, medication and

The neural circuitry of speech production in younger and older individuals

Overt speech production was associated with the activation of a distributed and bilateral neural network including the pyramidal and extrapyramidal motor system, both in younger and older individuals. Cortical activation related to the production of /a/ and /pataka/ compared to baseline is illustrated in Fig. 2 (red areas). Activation in the frontal and cingulate cortex included the medial prefrontal gyrus (supplementary motor area, SMA), the anterior cingulate gyrus (cingulate motor area,

The neural circuitry of speech production in younger and older individuals

As expected, speech production in older individuals involves a complex network of motor control and phonological processing, similar to the brain activation found in our previous study that included only younger adults (Sörös et al., 2006b).

Effect of age: overactivation in older individuals

In older individuals, the bilateral medial frontal gyrus, inferior frontal gyrus, and middle temporal gyrus were significantly more active compared to younger individuals. The extent of age-related changes in brain structure and function is not similar

Methodological considerations

FMRI detects local task-related changes in cerebral blood oxygenation, closely reflecting the underlying neural activity (Logothetis et al., 2001). The interpretation of the presented results relies on the assumption that the close coupling between neural activity and the fMRI signal, convincingly shown for younger adults, is also true in older individuals, despite possible age-related changes in the vascular reactivity of the brain (Riecker et al., 2003, D’Esposito et al., 2003). Studies on

Disclosure statement

All authors disclose no actual or potential conflicts of interest.

Acknowledgements

The authors wish to thank Dr. Randy McIntosh for his advice on designing the study and analyzing the data, Dr. Gary Glover for providing his spiral-in/out pulse sequence and Amy Brewer for helpful comments on an earlier version of this paper. This study was supported by the Heart and Stroke Foundation of Ontario and the Posluns Centre for Stroke and Cognition at Baycrest.

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