Effects of visual and auditory feedback on sensorimotor circuits in the basal ganglia.

Previous work using visual feedback has identified two distinct sensorimotor circuits in the basal ganglia (BG): one that scaled with the duration of force and one that scaled with the rate of change of force. The present study compared functional MRI signal changes in the BG during a grip force task using either visual or auditory feedback to determine whether the BG nuclei process auditory and visual feedback similarly. We confirmed the same two sensorimotor circuits in the BG. Activation in the striatum and external globus pallidus (GPe) scaled linearly with the duration of force under visual and auditory feedback conditions, with similar slopes and intercepts across feedback type. The pattern of signal change for the internal globus pallidus (GPi) and subthalamic nucleus (STN) was nonlinear and parameters of the exponential function were altered by feedback type. Specifically, GPi and STN activation decreased exponentially with the rate of change of force. The rate constant and asymptote of the exponential functions for GPi and STN were greater during auditory than visual feedback. In a comparison of the BOLD signal between BG regions, GPe had the highest percentage of variance accounted for and this effect was preserved for both feedback types. These new findings suggest that neuronal activity of specific BG nuclei is affected by whether the feedback is derived from visual or auditory inputs. Also, the data are consistent with the hypothesis that the GPe has a high level of information convergence from other BG nuclei, which is preserved across different sensory feedback modalities.

[1]  Alan M. Wing,et al.  Internal models of the motor system that explain predictive grip force control , 2004 .

[2]  Caudate unit activity in freely moving cats: effects of phasic auditory and visual stimuli , 1985, Brain Research.

[3]  Leslie G. Ungerleider,et al.  Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys , 1993, The Journal of comparative neurology.

[4]  N. Murase,et al.  Chapter 37 Abnormal sensorimotor integration in hand dystonia , 2006 .

[5]  Erich O. Richter,et al.  Determining the position and size of the subthalamic nucleus based on magnetic resonance imaging results in patients with advanced Parkinson disease. , 2004, Journal of neurosurgery.

[6]  Mary A. Mayka,et al.  Intermittent visuomotor processing in the human cerebellum, parietal cortex, and premotor cortex. , 2006, Journal of neurophysiology.

[7]  A. Berardelli,et al.  Sensorimotor integration in movement disorders , 2003, Movement disorders : official journal of the Movement Disorder Society.

[8]  Daniel M. Corcos,et al.  Subthalamic nucleus and internal globus pallidus scale with the rate of change of force production in humans , 2004, NeuroImage.

[9]  M. Kimura The role of primate putamen neurons in the association of sensory stimuli with movement , 1986, Neuroscience Research.

[10]  M. D. Crutcher,et al.  Single cell studies of the primate putamen , 2004, Experimental Brain Research.

[11]  N. Murase,et al.  Sensory function of basal ganglia , 2001, Movement disorders : official journal of the Movement Disorder Society.

[12]  B. Jacobs,et al.  Raphe unit activity in freely moving cats: Effects of phasic auditory and visual stimuli , 1982, Brain Research.

[13]  H. Bergman,et al.  Basal ganglia oscillations and pathophysiology of movement disorders , 2006, Current Opinion in Neurobiology.

[14]  P. Strick,et al.  The temporal lobe is a target of output from the basal ganglia. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  H. Kita Responses of globus pallidus neurons to cortical stimulation: intracellular study in the rat , 1992, Brain Research.

[16]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[17]  N. Murase,et al.  Abnormal sensorimotor integration in hand dystonia. , 2006, Supplements to Clinical neurophysiology.

[18]  D. Shibata,et al.  MR volumetric analysis of the human basal ganglia: normative data. , 2000, Academic radiology.

[19]  Edmund T. Rolls,et al.  Delay, discriminatory, and modality specific neurons in striatum and pallidum during short-term memory tasks , 1990, Brain Research.

[20]  M. D. Crutcher,et al.  Primate globus pallidus and subthalamic nucleus: functional organization. , 1985, Journal of neurophysiology.

[21]  L. Hazrati,et al.  Functional anatomy of the basal ganglia , 1995 .

[22]  Scott T Grafton,et al.  Contributions of functional imaging to understanding parkinsonian symptoms , 2004, Current Opinion in Neurobiology.

[23]  Leslie G. Ungerleider,et al.  Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido‐nigral complex in the monkey , 1990, The Journal of comparative neurology.

[24]  C. Marsden,et al.  The behavioural and motor consequences of focal lesions of the basal ganglia in man. , 1994, Brain : a journal of neurology.

[25]  Hong Yu,et al.  Role of the basal ganglia and frontal cortex in selecting and producing internally guided force pulses , 2007, NeuroImage.

[26]  Hong Yu,et al.  Region of interest template for the human basal ganglia: Comparing EPI and standardized space approaches , 2008, NeuroImage.

[27]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[28]  Jean-Louis Thonnard,et al.  The cutaneous contribution to adaptive precision grip , 2004, Trends in Neurosciences.

[29]  R W Cox,et al.  Software tools for analysis and visualization of fMRI data , 1997, NMR in biomedicine.

[30]  G. Benedek,et al.  Multisensory responses and receptive field properties of neurons in the substantia nigra and in the caudate nucleus , 2005, The European journal of neuroscience.

[31]  F. Horak,et al.  Influence of the globus pallidus on arm movements in monkeys. III. Timing of movement-related information. , 1985, Journal of neurophysiology.

[32]  D. Noll,et al.  Bilateral basal ganglia activation associated with sensorimotor adaptation , 2006, Experimental Brain Research.

[33]  K R Thulborn,et al.  Visual feedback to stabilize head position for fMRI , 1999, Magnetic resonance in medicine.

[34]  A. Weindl,et al.  Sensory processing in Parkinson's and Huntington's disease: investigations with 3D H(2)(15)O-PET. , 1999, Brain : a journal of neurology.

[35]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[36]  H. Kita,et al.  Excitatory Cortical Inputs to Pallidal Neurons Via the Subthalamic Nucleus in the Monkey , 2000 .

[37]  J. Schneider Responses of striatal neurons to peripheral sensory stimulation in symptomatic MPTP-exposed cats , 1991, Brain Research.

[38]  R. Reale,et al.  Auditory cortical field projections to the basal ganglia of the cat , 1983, Neuroscience.

[39]  Scott T. Grafton,et al.  Motor subcircuits mediating the control of movement velocity: a PET study. , 1998, Journal of neurophysiology.

[40]  Hong Yu,et al.  Role of individual basal ganglia nuclei in force amplitude generation. , 2007, Journal of neurophysiology.

[41]  Scott T. Grafton,et al.  Motor subcircuits mediating the control of movement extent and speed. , 2003, Journal of neurophysiology.

[42]  Didier Dormont,et al.  Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. , 2004, AJNR. American journal of neuroradiology.

[43]  J. Deniau,et al.  Segregation and Convergence of Information Flow through the Cortico-Subthalamic Pathways , 2001, The Journal of Neuroscience.

[44]  J. Konczak,et al.  Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia. , 2003, Brain : a journal of neurology.

[45]  M. E. Anderson,et al.  A quantitative analysis of pallidal discharge during targeted reaching movement in the monkey , 2004, Experimental Brain Research.

[46]  E. Bézard,et al.  Shaping of Motor Responses by Incentive Values through the Basal Ganglia , 2007, The Journal of Neuroscience.

[47]  E. Vaadia,et al.  Independent Coding of Movement Direction and Reward Prediction by Single Pallidal Neurons , 2004, The Journal of Neuroscience.

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

[49]  Eric H. Chudler,et al.  Multisensory convergence and integration in the neostriatum and globus pallidus of the rat , 1995, Brain Research.

[50]  Peter Redgrave,et al.  A direct projection from superior colliculus to substantia nigra for detecting salient visual events , 2003, Nature Neuroscience.