The Topography of Tactile Working Memory

To investigate the contribution of topographically organized brain areas to tactile working memory, we asked human subjects to compare the frequency of two vibrations presented to the same fingertip or to different fingertips. The vibrations ranged from 14 to 24 Hz and were separated by a retention interval of variable length. For intervals <1 sec, subjects were accurate when both vibrations were delivered to the same fingertip but were less accurate when the two vibrations were delivered to different fingertips. For 1 or 2 sec intervals, subjects performed equally well when comparing vibrations delivered either to the same finger or to corresponding fingers on opposite hands, but they performed poorly when the vibrations were delivered to distant fingers on either hand. These results suggest that working memory resides within a topographic framework. As a further test, we performed an experiment in which the two comparison vibrations were presented to the same fingertip but an interference vibration was presented during the retention interval. The interpolated vibration disrupted accuracy most when delivered to the same finger as the comparison vibrations and had progressively less effect when delivered to more distant fingers. We conclude that topographically organized regions of somatosensory cortex contribute to tactile working memory, possibly by holding the memory trace across the retention interval. One stimulus can be accurately compared with the memory of a previous stimulus if they engage overlapping representations, but activation of the common cortical territory by an interpolated stimulus can disrupt the memory trace.

[1]  Mathew E. Diamond,et al.  Sensory Learning and the Brain‚Äôs Body Map , 2001 .

[2]  L. Krubitzer,et al.  Evidence for interhemispheric processing of inputs from the hands in human S2 and PV. , 2001, Journal of neurophysiology.

[3]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

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

[5]  Justin A. Harris,et al.  The Topography of Tactile Learning in Humans , 2001, The Journal of Neuroscience.

[6]  M. Petrides Dissociable Roles of Mid-Dorsolateral Prefrontal and Anterior Inferotemporal Cortex in Visual Working Memory , 2000, The Journal of Neuroscience.

[7]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[8]  R. Romo,et al.  Neuronal correlates of sensory discrimination in the somatosensory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[9]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[10]  M. Petrides The role of the mid-dorsolateral prefrontal cortex in working memory , 2000, Experimental Brain Research.

[11]  B. Postle,et al.  An fMRI Investigation of Cortical Contributions to Spatial and Nonspatial Visual Working Memory , 2000, NeuroImage.

[12]  R. Romo,et al.  Sensing without Touching Psychophysical Performance Based on Cortical Microstimulation , 2000, Neuron.

[13]  W.J.R. Dunseath,et al.  fMRI of the Responses to Vibratory Stimulation of Digit Tips , 2000, NeuroImage.

[14]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[15]  B. Postle,et al.  WhatThenWhere in Visual Working Memory: An Event-Related fMRI Study , 1999, Journal of Cognitive Neuroscience.

[16]  B. Postle,et al.  Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[17]  David C. Alsop,et al.  The Sensory Somatotopic Map of the Human Hand Demonstrated at 4 Tesla , 1999, NeuroImage.

[18]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[19]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Nikolaus M. Szeverenyi,et al.  Fingertip Representation in the Human Somatosensory Cortex: An fMRI Study , 1998, NeuroImage.

[21]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

[22]  Leslie G. Ungerleider,et al.  A neural system for human visual working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Emilio Salinas,et al.  Discrimination in the Sense of Flutter: New Psychophysical Measurements in Monkeys , 1997, The Journal of Neuroscience.

[24]  M. Fahle,et al.  The role of visual field position in pattern–discrimination learning , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  S. Hochstein,et al.  Task difficulty and the specificity of perceptual learning , 1997, Nature.

[26]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[27]  W. Jiang,et al.  Neuronal encoding of texture changes in the primary and the secondary somatosensory cortical areas of monkeys during passive texture discrimination. , 1997, Journal of neurophysiology.

[28]  A Baddeley,et al.  The fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Hochstein,et al.  Learning Pop-out Detection: Specificities to Stimulus Characteristics , 1996, Vision Research.

[30]  J. Fuster,et al.  Mnemonic neuronal activity in somatosensory cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[31]  G A Orban,et al.  Interocular transfer in perceptual learning of a pop-out discrimination task. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

[33]  M. Fahle Human Pattern Recognition: Parallel Processing and Perceptual Learning , 1994, Perception.

[34]  L. Kaufman,et al.  Behavioral lifetime of human auditory sensory memory predicted by physiological measures. , 1992, Science.

[35]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[36]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Harold Burton,et al.  Second somatosensory cortical area in macaque monkeys: 2. Neuronal responses to punctate vibrotactile stimulation of glabrous skin on the hand , 1991, Brain Research.

[38]  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.

[39]  P. Barbaresi,et al.  Callosal mechanism for the interhemispheric transfer of hand somatosensory information in the monkey , 1984, Behavioural Brain Research.

[40]  J. Kaas,et al.  The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys , 1983, The Journal of comparative neurology.

[41]  J. Kaas,et al.  Double representation of the body surface within cytoarchitectonic area 3b and 1 in “SI” in the owl monkey (aotus trivirgatus) , 1978, The Journal of comparative neurology.

[42]  V. Mountcastle,et al.  Capacities of humans and monkeys to discriminate vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychological measurements. , 1975, Journal of neurophysiology.

[43]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[44]  M. D’Esposito,et al.  Activity in fusiform face area modulated as a function of working memory load. , 2001, Brain research. Cognitive brain research.

[45]  M. Fahle,et al.  Limited translation invariance of human visual pattern recognition , 1998, Perception & psychophysics.

[46]  J. Kaas,et al.  Evolution of multiple areas and modules within neocortex. , 1993, Perspectives on developmental neurobiology.

[47]  T. Yoshioka,et al.  Neural mechanisms of tactual form and texture perception. , 1992, Annual review of neuroscience.