Scaling of Neural Responses to Visual and Auditory Motion in the Human Cerebellum

The human cerebellum contains approximately half of all the neurons within the cerebrum, yet most experimental work in human neuroscience over the last century has focused exclusively on the structure and functions of the forebrain. The cerebellum has an undisputed role in a range of motor functions (Thach et al., 1992), but its potential contributions to sensory and cognitive processes are widely debated (Stoodley and Schmahmann, 2009). Here we used functional magnetic resonance imaging to test the hypothesis that the human cerebellum is involved in the acquisition of auditory and visual sensory data. We monitored neural activity within the cerebellum while participants engaged in a task that required them to discriminate the direction of a visual or auditory motion signal in noise. We identified a distinct set of cerebellar regions that were differentially activated for visual stimuli (vermal lobule VI and right-hemispheric lobule X) and auditory stimuli (right-hemispheric lobules VIIIA and VIIIB and hemispheric lobule VI bilaterally). In addition, we identified a region in left crus I in which activity correlated significantly with increases in the perceptual demands of the task (i.e., with decreasing signal strength), for both auditory and visual stimuli. Our results support suggestions of a role for the cerebellum in the processing of auditory and visual motion and suggest that parts of cerebellar cortex are concerned with tracking movements of objects around the animal, rather than with controlling movements of the animal itself (Paulin, 1993).

[1]  Hubertus Maximilian Mehdorn,et al.  Does the cerebellum contribute to specific aspects of attention? , 2003, Neuropsychologia.

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

[3]  C. Woody,et al.  Identification of short latency auditory responsive neurons in the cat dentate nucleus. , 1994, Neuroreport.

[4]  James M Bower,et al.  The Organization of Cerebellar Cortical Circuitry Revisited , 2002, Annals of the New York Academy of Sciences.

[5]  R. Ivry,et al.  Impaired Velocity Perception in Patients with Lesions of the Cerebellum , 1991, Journal of Cognitive Neuroscience.

[6]  J M Bower,et al.  Control of sensory data acquisition. , 1997, International review of neurobiology.

[7]  D. A. Suzuki,et al.  Visual and pursuit eye movement-related activity in posterior vermis of monkey cerebellum. , 1981, Journal of neurophysiology.

[8]  N Ramnani,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[9]  N. Troje,et al.  Differential involvement of the cerebellum in biological and coherent motion perception , 2005, The European journal of neuroscience.

[10]  Jeremy D. Schmahmann,et al.  Pitch discrimination in cerebellar patients: Evidence for a sensory deficit , 2009, Brain Research.

[11]  J. Grey Multidimensional perceptual scaling of musical timbres. , 1977, The Journal of the Acoustical Society of America.

[12]  P. Thier,et al.  Absence of a common functional denominator of visual disturbances in cerebellar disease. , 1999, Brain : a journal of neurology.

[13]  V. Henn,et al.  Visual-vestibular interaction in the flocculus of the alert monkey , 2004, Experimental Brain Research.

[14]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[15]  G. Orban,et al.  Many areas in the human brain respond to visual motion. , 1994, Journal of neurophysiology.

[16]  X. Hu,et al.  4 T-fMRI study of nonspatial shifting of selective attention: cerebellar and parietal contributions. , 1998, Journal of neurophysiology.

[17]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[18]  Michael Erb,et al.  Cerebral Processing of Timbre and Loudness: fMRI Evidence for a Contribution of Broca’s Area to Basic Auditory Discrimination , 2008, Brain Imaging and Behavior.

[19]  J. Schmahmann From movement to thought: Anatomic substrates of the cerebellar contribution to cognitive processing , 1996, Human brain mapping.

[20]  J. Schmahmann The cerebrocerebellar system: anatomic substrates of the cerebellar contribution to cognition and emotion , 2001 .

[21]  Jörn Diedrichsen,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[22]  Angela R Laird,et al.  Cerebellum and auditory function: An ALE meta‐analysis of functional neuroimaging studies , 2005, Human brain mapping.

[23]  S Zeki,et al.  Conscious visual perception without V1. , 1993, Brain : a journal of neurology.

[24]  K. H. Britten,et al.  Responses of neurons in macaque MT to stochastic motion signals , 1993, Visual Neuroscience.

[25]  D. Zee,et al.  Effects of ablation of flocculus and paraflocculus of eye movements in primate. , 1981, Journal of neurophysiology.

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

[27]  M. Paulin The role of the cerebellum in motor control and perception. , 1993, Brain, behavior and evolution.

[28]  H. Mehdorn,et al.  Evidence for distinct cognitive deficits after focal cerebellar lesions , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[29]  Clare Howarth,et al.  The Energy Use Associated with Neural Computation in the Cerebellum , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[30]  J. Konczak,et al.  Depth perception in cerebellar and basal ganglia disease , 2006, Experimental Brain Research.

[31]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[32]  E. Courchesne,et al.  Attentional Activation of the Cerebellum Independent of Motor Involvement , 1997, Science.

[33]  Jörn Diedrichsen,et al.  A spatially unbiased atlas template of the human cerebellum , 2006, NeuroImage.

[34]  W T Thach,et al.  The cerebellum and the adaptive coordination of movement. , 1992, Annual review of neuroscience.

[35]  D. A. Suzuki,et al.  The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity. , 1988, Journal of neurophysiology.