Discrimination of temporal information at the cerebellum: functional magnetic resonance imaging of nonverbal auditory memory
Introduction
A classic tenet of clinical neurology, tracing back to the early 19th century, holds that the cerebellum is devoted exclusively to motor functions such as the control of voluntary arm movements, upright posture, and locomotion Dow and Moruzzi, 1958, Gilman et al., 1981. This suggestion has, however, been challenged by a series of studies during the last two decades indicating a contribution of the cerebellum to various non-motor domains such as executive functions and higher-order linguistic operations (for a review, see Ackermann and Daum, 2003). As concerns perceptual processes, Ivry and Keele (1989) documented for the first time compromised time estimation after cerebellar disorders: Patients performed significantly worse than controls when asked to compare the duration of two successive time intervals (about 400 ms) bound by pairs of auditory clicks each. Subsequent investigations found cerebellar subjects also impaired in other tasks requiring precise time estimation such as the judgment of the velocity of moving visual stimuli (Ivry and Diener, 1991) or time bisection (Nichelli et al., 1996). Since at least some cerebellar motor deficits might reflect disrupted central timing mechanisms, Keele and Ivry (1990) suggested that the cerebellum is an “internal clock” prerequisite for explicit temporal computations within both the motor and the perceptual domain (“generalized timing hypothesis;” Ivry and Fiez, 2000).
Within some limits, the various classes of speech sounds (phonemes) of any human language system, that is, the respective inventory of consonants and vowels, can be characterized in terms of rather distinct features of the acoustic signal (Ladefoged and Maddieson, 1997). Among others, durational measures contribute to the specification of phonemes. For example, word pairs like English rapid-rabbit or German Boten–Boden (English: “messengers”–“floor”) may solely differ in the duration of the pause (closure time, CLT) between the first and second syllable. Among others, the “generalized timing hypothesis” (Ivry and Fiez, 2000) predicts participation of cerebellar structures in the encoding of durational speech parameters. In accordance with this suggestion, a previous clinical study found cerebellar patients unable to classify a series of Boten–Boden stimuli exclusively differing in CLT (Ackermann et al., 1997). Furthermore, a subsequent functional magnetic resonance imaging (fMRI) study was able to document significant hemodynamic activation of the right cerebellar hemisphere (Crus I of the neocerebellum; Schmahmann et al., 2000) as well as the left prefrontal cortex (Brodmann area 47) in association with this task (Mathiak et al., 2002a).
Besides speech stimuli, a previous clinical study found cerebellar dysfunctions to compromise the discrimination of non-speech time intervals, extending in duration from 10 to 150 ms and bound by pairs of tones (Ackermann et al., 1999a). This range of stimulus lengths covers the domain of acoustic speech segments relevant for speech. Subjects were asked to decide which of the two pairs of tones marked the longer pause. Some of the patients performed close to chance, and the group as a whole was significantly impaired as compared to their matched controls. Remarkably, categorization of the same items as either a long or a short event was found unimpaired. The shortest and the longest interval served as the anchor stimuli or prototypes of the identification task.
Based on these findings, the present fMRI investigation sought to determine whether the discrimination of non-speech time intervals elicits distinct cerebellar and supratentorial hemodynamic responses in healthy volunteers, using an identification task as a contrast condition. To that means, the study applied pauses bound by tones and varied the task as the contrast of interest. Single-shot double-echo echo-planar imaging (EPI) allowed for fast whole-brain acquisition. Moreover, the high bandwidth minimized image distortions at basal parts of the cerebrum (Jezzard and Clare, 1999) while maintaining a good contrast-to-noise ratio (CNR) Mathiak et al., 2002b, Posse et al., 1999. The resulting activation patterns were compared to previous findings obtained during the processing of durational parameters of linguistic stimuli (Mathiak et al., 2002a) to determine whether time estimation within the speech and non-speech domains share a common neural substrate.
Section snippets
Participants
Twelve German volunteers (six females; age 24–45 years, median 28 years) participated in the present study. Subjects were selected based on right-handedness, according to the Edinburgh handedness scale, and native German language use. None of them presented any medical or neurological dysfunction at clinical examination or an increased hearing threshold at auditory testing.
Stimuli and tasks
The experimental design was comprised of two conditions, each characterized by a set of stimuli systematically varying in
Behavioral data
In line with the previous clinical investigation, subjects produced an σ-shaped identification curve during categorization of short and long pauses (Fig. 1). More than 99% of the trials elicited a button-press as a response to the forced choice paradigm. Furthermore, duration changes of 50 ms and more were discriminated well above chance level (χ2 = 326.6, df = 1, P < 0.001). The discrimination task yielded longer response latencies (median 1373 ms) than the identification condition (1196 ms; P
Discussion
In line with a previous clinical study (Ackermann et al., 1999a), discrimination of time intervals of a similar length as durational speech parameters yielded significant cerebellar hemodynamic activation in contrast to the categorization of stimuli as short or long. The present neuroimaging study allows for a further topographic specification of these processes: Discrimination of successive time intervals, each bound by a pair of tones, was found associated with hemodynamic activation of the
Conclusion
The present study documented cerebellar involvement during an auditory duration short-term memory and comparison task: A distinct right-hemisphere cerebellar activation cluster superior to the horizontal fissure emerged when identification was compared to discrimination of pause durations. These findings accord with previous clinical data demonstrating deficient perception of temporal speech cues in subjects with cerebellar atrophy. The comparison to previous findings on speech perception and
Acknowledgements
This study was supported by the German Research Foundation (SFB 550/B1). The authors thank Nell Zink for revising the manuscript, Timothy Justus for his helpful comments, and Maike Borutta for excellent technical assistance and helpful discussions.
References (70)
- et al.
Cerebellar contributions to the perception of temporal cues within the speech and nonspeech domain
Brain Lang.
(1999) - et al.
Phonemic vowel length contrasts in cerebellar disorders
Brain Lang.
(1999) - et al.
Hemispheric lateralization of the neural encoding of temporal speech features: a whole-head magnetoencephalography study
Cogn. Brain Res.
(1999) - et al.
Differential activation of right superior parietal cortex and intraparietal sulcus by spatial and nonspatial attention
NeuroImage
(1998) - et al.
The basic pattern of activation in motor and sensory temporal tasks: positron emission tomography data
Neurosci. Lett.
(1997) - et al.
The motor theory of speech perception revised
Cognition
(1985) - et al.
Brain activation induced by estimation of duration: a PET study
NeuroImage
(1996) - et al.
Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry
Brain Res.
(1977) - et al.
Perceptual timing in cerebellar degeneration
Neuropsychologia
(1996) - et al.
Hemispheric lateralization effects of rhythm implementation during syllable repetitions: an fMRI study
NeuroImage
(2002)
Functional localization of a “time keeper” function separate from attentional resources and task strategy
NeuroImage
Human brain regions involved in visual categorization
NeuroImage
Auditory attention to space and frequency activates similar cerebral systems
NeuroImage
Neuropsychological deficits in cerebellar syndromes
Categorical speech perception in cerebellar disorders
Brain Lang.
Working memory
Science
Electrodynamic headphones and woofers for application in magnetic resonance imaging scanners
Med. Phys.
The remembering of auditory event durations
J. Exp. Psychol., Learn., Mem., Cogn.
The role of segmentation in phonological processing: an fMRI investigation
J. Cogn. Neurosci.
Imaging cognition II: an empirical review of 275 PET and fMRI studies
J. Cogn. Neurosci.
Auditory association cortex lesions impair auditory short-term memory in monkeys
Science
Control of goal-directed and stimulus-driven attention in the brain
Nat. Rev. Neurosci.
Neural systems for visual orienting and their relationships to spatial working memory
J. Cogn. Neurosci.
Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI
J. Neurosci.
The organization of short-term memory for a single acoustic attribute
Clinical symptoms of cerebellar dysfunction and their topodiagnostical significance
Hum. Neurobiol.
The Physiology and Pathology of the Cerebellum
The Modularity of Mind: An Essay on Faculty Psychology
Human Brain Function
SPM99
Disorders of the Cerebellum
Changing concepts of cortical connectivity: parallel distributed cortical networks
Single unit activity in the auditory cortex of a monkey performing a short term memory task
Exp. Brain Res.
Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization
Hum. Brain Mapp.
Neural underpinnings of temporal processing: a review of focal lesion, pharmacological, and functional imaging research
Rev. Neurosci.
Cited by (86)
A parcellation-based model of the auditory network
2020, Hearing ResearchDisorders of music processing in dementia
2020, Music and the Aging BrainThe role of cerebellum in the child neuropsychological functioning
2020, Handbook of Clinical NeurologyNeural substrates of internally-based and externally-cued timing: An activation likelihood estimation (ALE) meta-analysis of fMRI studies
2019, Neuroscience and Biobehavioral Reviews