Functional activation in the cerebellum during working memory and simple speech tasks

Verbal working memory is the ability to temporarily store and manipulate verbal information. This study tested the predictions of a neuroanatomical model of how the cerebellum contributes to verbal working memory (Desmond et al., 1997). In this model, a large bilateral region in the superior cerebellum is associated with articulatory rehearsal and a right-lateralized region in the inferior cerebellum is associated with the correction of errors within the working memory system. The Desmond et al. (1997) model was based on neuroimaging findings using item recognition tasks and comparisons between working memory and covert rehearsal tasks, whereas in this functional magnetic resonance imaging (fMRI) study we used a delayed serial recall (DSR) task because it relies more heavily on articulatory rehearsal, and our comparison tasks included both overt and covert speech tasks. Our results provide some support for the Desmond et al. (1997) model. In particular, we found multiple activation foci within the superior and inferior sectors of the cerebellum and evidence that these regions show different patterns of activation across working memory and speech tasks. However, the specific patterns of activation were not fully consistent with those reported by Desmond et al. (1997). Namely, our results indicate that activation in the superior sector should be functionally subdivided into a medial focus involved in speech processing and a lateral focus more specific to verbal working memory; the results also indicate that activation in the inferior sector is not uniquely right lateralized. These complex findings speak to the need for future studies to consider the speech-motor aspects of tasks, to investigate the functional significance of adjacent peaks of activation within large regions of cerebellar activation, and to use analysis procedures that support regional distinctions through direct statistical tests. Such studies would help to refine our understanding of how the cerebellum contributes to speech and verbal working memory.

[1]  Anthony R. McIntosh,et al.  Clustered functional MRI of overt speech production , 2006, NeuroImage.

[2]  Julie A Fiez,et al.  Cerebellar damage produces selective deficits in verbal working memory. , 2006, Brain : a journal of neurology.

[3]  Frank H. Guenther,et al.  An fMRI investigation of syllable sequence production , 2006, NeuroImage.

[4]  John E. Desmond,et al.  Cerebrocerebellar networks during articulatory rehearsal and verbal working memory tasks , 2005, NeuroImage.

[5]  J. Fiez,et al.  Functional heterogeneity within Broca's area during verbal working memory , 2002, Physiology & Behavior.

[6]  Dorothy V. M. Bishop,et al.  Unimpaired Short-term Memory and Rhyme Judgement in Congenitally Speechless Individuals: Implications for the Notion of “Articulatory Coding” , 1989 .

[7]  J. Desmond,et al.  Lobular Patterns of Cerebellar Activation in Verbal Working-Memory and Finger-Tapping Tasks as Revealed by Functional MRI , 1997, The Journal of Neuroscience.

[8]  M. Erb,et al.  The influence of syllable onset complexity and syllable frequency on speech motor control , 2008, Brain and Language.

[9]  W. Grodd,et al.  Cerebellum and Speech Perception: A Functional Magnetic Resonance Imaging Study , 2002, Journal of Cognitive Neuroscience.

[10]  N. Dronkers,et al.  Lesion analysis of the brain areas involved in language comprehension , 2004, Cognition.

[11]  N. Burgess,et al.  Selective Interference with Verbal Short-Term Memory for Serial Order Information: A New Paradigm and Tests of a Timing-Signal Hypothesis , 2003, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[12]  Douglas C. Noll,et al.  Overt Verbal Responding during fMRI Scanning: Empirical Investigations of Problems and Potential Solutions , 1999, NeuroImage.

[13]  Hermann Ackermann,et al.  Cerebellar contributions to cognition , 1995, Behavioural Brain Research.

[14]  Alan D. Baddeley,et al.  Disruption of short-term memory by unattended speech : Implications for the structure of working memory , 1982 .

[15]  Greg Allen,et al.  Magnetic resonance imaging of cerebellar–prefrontal and cerebellar–parietal functional connectivity , 2005, NeuroImage.

[16]  J. Fiez,et al.  Functional Magnetic Resonance Imaging (fmri) Was Used to Investigate the Neural Substrates of Component Processes in Verbal Working Memory. Based on Behavioral Research Using , 2022 .

[17]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[18]  Walter Schneider,et al.  Fiswidgets - A graphical computing environment for neuroimaging analysis , 2003, Neuroinformatics.

[19]  A. Benton Aphasia, Alexia and Agraphia , 1980 .

[20]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[21]  Jeremy D. Schmahmann,et al.  Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies , 2009, NeuroImage.

[22]  Irene Daum,et al.  Cerebellar contributions to cognitive functions: A progress report after two decades of research , 2008, The Cerebellum.

[23]  A. Baddeley The episodic buffer: a new component of working memory? , 2000, Trends in Cognitive Sciences.

[24]  John E. Desmond,et al.  Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task , 2005, Neuropsychologia.

[25]  W Grodd,et al.  Opposite hemispheric lateralization effects during speaking and singing at motor cortex, insula and cerebellum , 2000, Neuroreport.

[26]  E E Smith,et al.  Components of verbal working memory: evidence from neuroimaging. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  B. Mazoyer,et al.  A Common Language Network for Comprehension and Production: A Contribution to the Definition of Language Epicenters with PET , 2000, NeuroImage.

[28]  S E Petersen,et al.  A positron emission tomography study of the short-term maintenance of verbal information , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  P. Strick,et al.  Cerebellum and nonmotor function. , 2009, Annual review of neuroscience.

[30]  T. Carr,et al.  Comparing cortical activations for silent and overt speech using event‐related fMRI , 2002, Human brain mapping.

[31]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

[32]  John E. Desmond,et al.  Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study , 2005, NeuroImage.

[33]  Wolfgang Grodd,et al.  The cerebral control of speech tempo: Opposite relationship between speaking rate and BOLD signal changes at striatal and cerebellar structures , 2006, NeuroImage.

[34]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[35]  N Burgess,et al.  Recoding, storage, rehearsal and grouping in verbal short-term memory: an fMRI study , 2000, Neuropsychologia.

[36]  Tatiana V. Chernigovskaya,et al.  Prosodic clues to syntactic processing—a PET and ERP study , 2006, NeuroImage.

[37]  John R Anderson,et al.  Extraction of overt verbal response from the acoustic noise in a functional magnetic resonance imaging scan by use of segmented active noise cancellation , 2005, Magnetic resonance in medicine.

[38]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[39]  W. Grodd,et al.  Does the cerebellum contribute to cognitive aspects of speech production? A functional magnetic resonance imaging (fMRI) study in humans , 1998, Neuroscience Letters.

[40]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[41]  Fenna M. Krienen,et al.  Segregated Fronto-Cerebellar Circuits Revealed by Intrinsic Functional Connectivity , 2009, Cerebral cortex.

[42]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[43]  Richard N. Henson,et al.  Serial order in short-term memory , 2001 .

[44]  L. Shuster,et al.  An fMRI investigation of covertly and overtly produced mono- and multisyllabic words , 2005, Brain and Language.