Abstract
The sensation of flutter is produced when mechanical vibrations in the range of 5–50 Hz are applied to the skin1,2,3. A flutter stimulus activates neurons in the primary somatosensory cortex (S1) that somatotopically map to the site of stimulation4,5. A subset of these neurons — those with quickly adapting properties, associated with Meissner's corpuscles — are strongly entrained by periodic flutter vibrations, firing with a probability that oscillates at the input frequency1,6. Hence, quickly adapting neurons provide a dynamic representation of such flutter stimuli. However, are these neurons directly involved in the perception of flutter? Here we investigate this in monkeys trained to discriminate the difference in frequency between two flutter stimuli delivered sequentially on the fingertips1,7. Microelectrodes were inserted into area 3b of S1 and the second stimulus was substituted with a train of injected current pulses. Animals reliably indicated whether the frequency of the second (electrical) signal was higher or lower than that of the first (mechanical) signal, even though both frequencies changed from trial to trial. Almost identical results were obtained with periodic and aperiodic stimuli of equal average frequencies. Thus, the quickly adapting neurons in area 3b activate the circuit leading to the perception of flutter. Furthermore, as far as can be psychophysically quantified during discrimination, the neural code underlying the sensation of fluttercan be finely manipulated, to the extent that the behavioural responses produced by natural and artificial stimuli are indistinguishable.
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References
Mountcastle, V. B., Steinmetz, M. A. & Romo, R. Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys. J. Neurosci. 10, 3032–3044 (1990).
Talbot, W. H., Darian-Smith, I., Kornhuber, H. H. & Mountcastle, V. B. The sense of flutter vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey's hand. J. Neurophysiol. 31, 301–334 (1968).
Mountcastle, V. B., Talbot, W. H., Sakata, H. & Hyvärinen, J. Cortical neuronal mechanisms in flutter vibration studied in unanesthetized monkeys. J. Neurophysiol. 32, 453–484 (1969).
Kaas, J. H., Nelson, R. J., Sur, M. & Merzenich, M. M. Multiple representation of the body within the primary somatosensory cortex of primates. Science 204, 511–512 (1979).
Sur, M., Wall, J. T. & Kaas, J. H. Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys. J. Neurophysiol. 51, 724–744 (1984).
Recanzone, G. H., Merzenich, M. M. & Schreiner, C. E. Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. J. Neurophysiol. 67, 1071–1091 (1992).
Hernández, A., Salinas, E., García, R. & Romo, R. Discrimination in the sense of flutter: new psychophysical measurements in monkeys. J. Neurosci. 17, 6391–6400 (1997).
Mountcastle, V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20, 408–434 (1957).
Powell, T. P. S. & Mountcastle, V. B. Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull. Johns Hopkins Hosp. 105, 133–162 (1959).
Siegel, S. & Castellan, N. J. Nonparametric Statistics for the Behavioral Sciences(McGraw-Hill, New York, (1988)).
LaMotte, R. H. & Mountcastle, V. B. The capacities of humans and monkeys to discriminate between vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychophysical measurements. J. Neurophysiol. 38, 539–559 (1975).
Bair, W., Koch, C., Newsome, W. & Britten, K. Power spectrum analysis of bursting cells in area MT in the behaving monkey. J. Neurosci. 14, 2870–2892 (1994).
Salzman, C. D., Britten, K. H. & Newsome, W. T. Cortical microstimulation influences perceptual judgments of motion direction. Nature 346, 174–177 (1990).
Salzman, C. D., Murasugi, C. M., Britten, K. H. & Newsome, W. T. Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355 (1992).
Vallbo, A. B. in The Cognitive Neurosciences(ed. Gazzaniga, M. S.) 237–252 (MIT Press, Cambridge, Mass, (1995)).
LaMotte, R. H. & Mountcastle, V. B. Disorders in somesthesis following lesions of parietal lobe. J. Neurophysiol. 42, 400–419 (1979).
Zainos, A., Merchant, H., Hernández, A., Salinas, E. & Romo, R. Role of primary somatic sensory cortex in the categorization of tactile stimuli: effects of lesions. Exp. Brain Res. 115, 357–360 (1997).
Mountcastle, V. B., Reitboek, H. J., Poggio, G. F. & Steinmetz, M. A. Adaptation of the Reitboek method of multiple microelectrode recording to the neocortex of the waking monkey. J. Neurosci. Methods 36, 77–84 (1991).
Acknowledgements
We thank W. T. Newsome for comments and discussions. R.R.'s research was partially supported by an International Research Scholars Award from the HHMI and by grants from DGAPA-UNAM, CONACyT and Fundación Miguel Alemán AC.
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Romo, R., Hernández, A., Zainos, A. et al. Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390 (1998). https://doi.org/10.1038/32891
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DOI: https://doi.org/10.1038/32891
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