Feeling for space or for time: Task-dependent modulation of the cortical representation of identical vibrotactile stimuli

Using functional MRI we examined the task-dependency of brain activation patterns evoked by vibrotactile stimulation. For this purpose, we measured activations after identical stimulation of the fingers of the right hand in three different task conditions: passive attention, localization of the vibrations, and discrimination of temporal noise within the vibrations. Further, we investigated whether, regardless of task demands, the characteristics of the vibrations - periodic versus noisy - had an effect on brain topography. Vibrotactile processing was associated with activation in a variety of cortical areas including contralateral primary somatosensory cortex (SI), bilateral posterior parietal cortex, parietal operculum (second somatosensory cortex, SII), insula, and superior temporal gyrus, as well as ipsilateral middle temporal gyrus, precentral, and middle frontal gyrus. However, identical stimuli evoked different brain activity patterns in different task conditions: significantly stronger activity in the hand representation of SI was found for stimulus localization than for noise detection. In contrast, significantly higher activation for noise detection than for finger localization was found in the thalamus. Activation tended to be lower for noisy stimuli in both hemispheres. Significant stimulus-related differences, however, could be found only in the contralateral postcentral and parietal cortex, particularly during noise discrimination. In summary, in response to vibrotactile stimulation, the level of activation in processing circuits ranging across thalamus and many cortical regions is dictated by the perceptual operation carried out on the vibration. We speculate that different nodes in the network carry signals that can be optimally decoded for either spatial or temporal information and that the degree of activation reflects those nodes' relative contributions to the decoding process.

[1]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[2]  Justin A. Harris,et al.  Factors Affecting Frequency Discrimination of Vibrotactile Stimuli: Implications for Cortical Encoding , 2006, PloS one.

[3]  I Hashimoto,et al.  Selective spatial attention induces short-term plasticity in human somatosensory cortex , 2001, Neuroreport.

[4]  R. Romo,et al.  Neural codes for perceptual discrimination in primary somatosensory cortex , 2005, Nature Neuroscience.

[5]  Greg C. Champney,et al.  Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex , 2006, Experimental Brain Research.

[6]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[7]  S. Hochstein,et al.  The reverse hierarchy theory of visual perceptual learning , 2004, Trends in Cognitive Sciences.

[8]  R. Veit,et al.  BOLD adaptation in vibrotactile stimulation: neuronal networks involved in frequency discrimination. , 2007, Journal of neurophysiology.

[9]  Larry E. Roberts,et al.  Functional Organization of Primary Somatosensory Cortex Depends on the Focus of Attention , 2002, NeuroImage.

[10]  Heidi Johansen-Berg,et al.  The physiology and psychology of selective attention to touch. , 2000 .

[11]  Emilio Salinas,et al.  Cognitive neuroscience: Flutter Discrimination: neural codes, perception, memory and decision making , 2003, Nature Reviews Neuroscience.

[12]  R. Ilmoniemi,et al.  Effects of interstimulus interval on somatosensory evoked magnetic fields (SEFs): a hypothesis concerning SEF generation at the primary sensorimotor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[13]  Y. Iwamura Hierarchical somatosensory processing , 1998, Current Opinion in Neurobiology.

[14]  Justin A. Harris,et al.  Transient Storage of a Tactile Memory Trace in Primary Somatosensory Cortex , 2002, The Journal of Neuroscience.

[15]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

[16]  Arno Villringer,et al.  Neural Correlates of Vibrotactile Working Memory in the Human Brain , 2006, The Journal of Neuroscience.

[17]  R. Romo,et al.  Touch and go: decision-making mechanisms in somatosensation. , 2001, Annual review of neuroscience.

[18]  H. Freund,et al.  The role of the inferior parietal cortex in linking the tactile perception and manual construction of object shapes. , 2001, Cerebral cortex.

[19]  Ehsan Arabzadeh,et al.  Enhanced response of neurons in rat somatosensory cortex to stimuli containing temporal noise. , 2008, Cerebral cortex.

[20]  Simon J Graham,et al.  Activation in SI and SII: the influence of vibrotactile amplitude during passive and task-relevant stimulation. , 2004, Brain research. Cognitive brain research.

[21]  Mathew E. Diamond,et al.  The Cortical Distribution of Sensory Memories , 2001, Neuron.

[22]  C Braun,et al.  Differential Activation in Somatosensory Cortex for Different Discrimination Tasks , 2000, The Journal of Neuroscience.

[23]  Francis McGlone,et al.  Functional neuroimaging studies of human somatosensory cortex , 2002, Behavioural Brain Research.

[24]  R. Romo,et al.  Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  P. Haggard Sensory Neuroscience: From Skin to Object in the Somatosensory Cortex , 2006, Current Biology.

[26]  Sandra E. Black,et al.  Task-Relevant Modulation of Contralateral and Ipsilateral Primary Somatosensory Cortex and the Role of a Prefrontal-Cortical Sensory Gating System , 2002, NeuroImage.