Skip to main content
NCBI home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2002 Aug 29;357(1424):1039–1051. doi: 10.1098/rstb.2002.1100

Exploring the cortical evidence of a sensory-discrimination process.

Ranulfo Romo 1, Adrián Hernández 1, Antonio Zainos 1, Carlos Brody 1, Emilio Salinas 1
PMCID: PMC1693008  PMID: 12217172

Abstract

Humans and monkeys have similar abilities to discriminate the difference in frequency between two consecutive mechanical vibrations applied to their fingertips. This task can be conceived as a chain of neural operations: encoding the two consecutive stimuli, maintaining the first stimulus in working memory, comparing the second stimulus with the memory trace left by the first stimulus and communicating the result of the comparison to the motor apparatus. We studied this chain of neural operations by recording and manipulating neurons from different areas of the cerebral cortex while monkeys performed the task. The results indicate that neurons of the primary somatosensory cortex (S1) generate a neural representation of vibrotactile stimuli which correlates closely with psychophysical performance. Discrimination based on microstimulation patterns injected into clusters of S1 neurons is indistinguishable from that produced by natural stimuli. Neurons from the secondary somatosensory cortex (S2), prefrontal cortex and medial premotor cortex (MPC) display at different times the trace of the first stimulus during the working-memory component of the task. Neurons from S2 and MPC appear to show the comparison between the two stimuli and correlate with the behavioural decisions. These neural operations may contribute to the sensory-discrimination process studied here.

Full Text

The Full Text of this article is available as a PDF (387.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Britten K. H., Shadlen M. N., Newsome W. T., Movshon J. A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci. 1992 Dec;12(12):4745–4765. doi: 10.1523/JNEUROSCI.12-12-04745.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Britten K. H., van Wezel R. J. Electrical microstimulation of cortical area MST biases heading perception in monkeys. Nat Neurosci. 1998 May;1(1):59–63. doi: 10.1038/259. [DOI] [PubMed] [Google Scholar]
  3. Burton H., Fabri M., Alloway K. Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: a revised interpretation of the second somatosensory area in macaque monkeys. J Comp Neurol. 1995 May 15;355(4):539–562. doi: 10.1002/cne.903550405. [DOI] [PubMed] [Google Scholar]
  4. Burton H., Fabri M. Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: projections in the vicinity of the central sulcus. J Comp Neurol. 1995 May 15;355(4):508–538. doi: 10.1002/cne.903550404. [DOI] [PubMed] [Google Scholar]
  5. Burton H., Sinclair R. J., Hong S. Y., Pruett J. R., Jr, Whang K. C. Tactile-spatial and cross-modal attention effects in the second somatosensory and 7b cortical areas of rhesus monkeys. Somatosens Mot Res. 1997;14(4):237–267. doi: 10.1080/08990229770971. [DOI] [PubMed] [Google Scholar]
  6. Carmichael S. T., Price J. L. Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol. 1995 Dec 25;363(4):642–664. doi: 10.1002/cne.903630409. [DOI] [PubMed] [Google Scholar]
  7. Cavada C., Goldman-Rakic P. S. Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J Comp Neurol. 1989 Sep 22;287(4):393–421. doi: 10.1002/cne.902870402. [DOI] [PubMed] [Google Scholar]
  8. Dodd J. V., Krug K., Cumming B. G., Parker A. J. Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT. J Neurosci. 2001 Jul 1;21(13):4809–4821. doi: 10.1523/JNEUROSCI.21-13-04809.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fuster J. M. Network memory. Trends Neurosci. 1997 Oct;20(10):451–459. doi: 10.1016/s0166-2236(97)01128-4. [DOI] [PubMed] [Google Scholar]
  10. Godschalk M., Lemon R. N., Kuypers H. G., Ronday H. K. Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study. Exp Brain Res. 1984;56(3):410–424. doi: 10.1007/BF00237982. [DOI] [PubMed] [Google Scholar]
  11. Gold J. I., Shadlen M. N. Representation of a perceptual decision in developing oculomotor commands. Nature. 2000 Mar 23;404(6776):390–394. doi: 10.1038/35006062. [DOI] [PubMed] [Google Scholar]
  12. Hernández A., Salinas E., García R., Romo R. Discrimination in the sense of flutter: new psychophysical measurements in monkeys. J Neurosci. 1997 Aug 15;17(16):6391–6400. doi: 10.1523/JNEUROSCI.17-16-06391.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hernández Adrián, Zainos Antonio, Romo Ranulfo. Temporal evolution of a decision-making process in medial premotor cortex. Neuron. 2002 Mar 14;33(6):959–972. doi: 10.1016/s0896-6273(02)00613-x. [DOI] [PubMed] [Google Scholar]
  14. Horwitz G. D., Newsome W. T. Separate signals for target selection and movement specification in the superior colliculus. Science. 1999 May 14;284(5417):1158–1161. doi: 10.1126/science.284.5417.1158. [DOI] [PubMed] [Google Scholar]
  15. Hsiao S. S., O'Shaughnessy D. M., Johnson K. O. Effects of selective attention on spatial form processing in monkey primary and secondary somatosensory cortex. J Neurophysiol. 1993 Jul;70(1):444–447. doi: 10.1152/jn.1993.70.1.444. [DOI] [PubMed] [Google Scholar]
  16. Jiang W., Tremblay F., Chapman C. E. Neuronal encoding of texture changes in the primary and the secondary somatosensory cortical areas of monkeys during passive texture discrimination. J Neurophysiol. 1997 Mar;77(3):1656–1662. doi: 10.1152/jn.1997.77.3.1656. [DOI] [PubMed] [Google Scholar]
  17. Johnson K. O., Hsiao S. S. Neural mechanisms of tactual form and texture perception. Annu Rev Neurosci. 1992;15:227–250. doi: 10.1146/annurev.ne.15.030192.001303. [DOI] [PubMed] [Google Scholar]
  18. Jones E. G., Coulter J. D., Hendry S. H. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol. 1978 Sep 15;181(2):291–347. doi: 10.1002/cne.901810206. [DOI] [PubMed] [Google Scholar]
  19. Jones E. G., Powell T. P. Connexions of the somatic sensory cortex of the rhesus monkey. I. Ipsilateral cortical connexions. Brain. 1969;92(3):477–502. doi: 10.1093/brain/92.3.477. [DOI] [PubMed] [Google Scholar]
  20. Jürgens U. The efferent and afferent connections of the supplementary motor area. Brain Res. 1984 May 21;300(1):63–81. doi: 10.1016/0006-8993(84)91341-6. [DOI] [PubMed] [Google Scholar]
  21. Kaas J. H., Nelson R. J., Sur M., Lin C. S., Merzenich M. M. Multiple representations of the body within the primary somatosensory cortex of primates. Science. 1979 May 4;204(4392):521–523. doi: 10.1126/science.107591. [DOI] [PubMed] [Google Scholar]
  22. Kim J. N., Shadlen M. N. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat Neurosci. 1999 Feb;2(2):176–185. doi: 10.1038/5739. [DOI] [PubMed] [Google Scholar]
  23. Krubitzer L., Clarey J., Tweedale R., Elston G., Calford M. A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J Neurosci. 1995 May;15(5 Pt 2):3821–3839. doi: 10.1523/JNEUROSCI.15-05-03821.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. LaMotte R. H., Mountcastle V. B. Capacities of humans and monkeys to discriminate vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychological measurements. J Neurophysiol. 1975 May;38(3):539–559. doi: 10.1152/jn.1975.38.3.539. [DOI] [PubMed] [Google Scholar]
  25. Lee L. F., Wu P., Sui D., Ren D., Kamil J., Kung H. J., Witter R. L. The complete unique long sequence and the overall genomic organization of the GA strain of Marek's disease virus. Proc Natl Acad Sci U S A. 2000 May 23;97(11):6091–6096. doi: 10.1073/pnas.97.11.6091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Leichnetz G. R. Afferent and efferent connections of the dorsolateral precentral gyrus (area 4, hand/arm region) in the macaque monkey, with comparisons to area 8. J Comp Neurol. 1986 Dec 22;254(4):460–492. doi: 10.1002/cne.902540403. [DOI] [PubMed] [Google Scholar]
  27. Luppino G., Matelli M., Camarda R., Rizzolatti G. Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol. 1993 Dec 1;338(1):114–140. doi: 10.1002/cne.903380109. [DOI] [PubMed] [Google Scholar]
  28. MOUNTCASTLE V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol. 1957 Jul;20(4):408–434. doi: 10.1152/jn.1957.20.4.408. [DOI] [PubMed] [Google Scholar]
  29. Macefield G., Gandevia S. C., Burke D. Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J Physiol. 1990 Oct;429:113–129. doi: 10.1113/jphysiol.1990.sp018247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Merchant H., Zainos A., Hernández A., Salinas E., Romo R. Functional properties of primate putamen neurons during the categorization of tactile stimuli. J Neurophysiol. 1997 Mar;77(3):1132–1154. doi: 10.1152/jn.1997.77.3.1132. [DOI] [PubMed] [Google Scholar]
  31. Mishkin M. Analogous neural models for tactual and visual learning. Neuropsychologia. 1979;17(2):139–151. doi: 10.1016/0028-3932(79)90005-8. [DOI] [PubMed] [Google Scholar]
  32. Mountcastle V. B., Atluri P. P., Romo R. Selective output-discriminative signals in the motor cortex of waking monkeys. Cereb Cortex. 1992 Jul-Aug;2(4):277–294. doi: 10.1093/cercor/2.4.277. [DOI] [PubMed] [Google Scholar]
  33. Mountcastle V. B., LaMotte R. H., Carli G. Detection thresholds for stimuli in humans and monkeys: comparison with threshold events in mechanoreceptive afferent nerve fibers innervating the monkey hand. J Neurophysiol. 1972 Jan;35(1):122–136. doi: 10.1152/jn.1972.35.1.122. [DOI] [PubMed] [Google Scholar]
  34. 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. 1990 Sep;10(9):3032–3044. doi: 10.1523/JNEUROSCI.10-09-03032.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mountcastle V. B., Talbot W. H., Sakata H., Hyvärinen J. Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol. 1969 May;32(3):452–484. doi: 10.1152/jn.1969.32.3.452. [DOI] [PubMed] [Google Scholar]
  36. Murray E. A., Mishkin M. Relative contributions of SII and area 5 to tactile discrimination in monkeys. Behav Brain Res. 1984 Jan;11(1):67–83. doi: 10.1016/0166-4328(84)90009-3. [DOI] [PubMed] [Google Scholar]
  37. Nelson R. J., Sur M., Felleman D. J., Kaas J. H. Representations of the body surface in postcentral parietal cortex of Macaca fascicularis. J Comp Neurol. 1980 Aug 15;192(4):611–643. doi: 10.1002/cne.901920402. [DOI] [PubMed] [Google Scholar]
  38. Newsome W. T., Britten K. H., Movshon J. A. Neuronal correlates of a perceptual decision. Nature. 1989 Sep 7;341(6237):52–54. doi: 10.1038/341052a0. [DOI] [PubMed] [Google Scholar]
  39. Ochoa J., Torebjörk E. Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. J Physiol. 1983 Sep;342:633–654. doi: 10.1113/jphysiol.1983.sp014873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. POWELL T. P., 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. 1959 Sep;105:133–162. [PubMed] [Google Scholar]
  41. Pandya D. N., Kuypers H. G. Cortico-cortical connections in the rhesus monkey. Brain Res. 1969 Mar;13(1):13–36. doi: 10.1016/0006-8993(69)90141-3. [DOI] [PubMed] [Google Scholar]
  42. Pearson R. C., Powell T. P. The projection of the primary somatic sensory cortex upon area 5 in the monkey. Brain Res. 1985 Apr;356(1):89–107. doi: 10.1016/0165-0173(85)90020-7. [DOI] [PubMed] [Google Scholar]
  43. Phillips J. R., Johnson K. O. Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. J Neurophysiol. 1981 Dec;46(6):1192–1203. doi: 10.1152/jn.1981.46.6.1192. [DOI] [PubMed] [Google Scholar]
  44. Pons T. P., Garraghty P. E., Friedman D. P., Mishkin M. Physiological evidence for serial processing in somatosensory cortex. Science. 1987 Jul 24;237(4813):417–420. doi: 10.1126/science.3603028. [DOI] [PubMed] [Google Scholar]
  45. Pons T. P., Garraghty P. E., Mishkin M. Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys. J Neurophysiol. 1992 Aug;68(2):518–527. doi: 10.1152/jn.1992.68.2.518. [DOI] [PubMed] [Google Scholar]
  46. Preuss T. M., Goldman-Rakic P. S. Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: anatomical evidence for somatic representation in primate frontal association cortex. J Comp Neurol. 1989 Apr 8;282(2):293–316. doi: 10.1002/cne.902820210. [DOI] [PubMed] [Google Scholar]
  47. 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. 1992 May;67(5):1071–1091. doi: 10.1152/jn.1992.67.5.1071. [DOI] [PubMed] [Google Scholar]
  48. Romo R., Brody C. D., Hernández A., Lemus L. Neuronal correlates of parametric working memory in the prefrontal cortex. Nature. 1999 Jun 3;399(6735):470–473. doi: 10.1038/20939. [DOI] [PubMed] [Google Scholar]
  49. Romo R., Hernández A., Zainos A., Brody C. D., Lemus L. Sensing without touching: psychophysical performance based on cortical microstimulation. Neuron. 2000 Apr;26(1):273–278. doi: 10.1016/s0896-6273(00)81156-3. [DOI] [PubMed] [Google Scholar]
  50. Romo R., Hernández A., Zainos A., Salinas E. Somatosensory discrimination based on cortical microstimulation. Nature. 1998 Mar 26;392(6674):387–390. doi: 10.1038/32891. [DOI] [PubMed] [Google Scholar]
  51. Romo R., Merchant H., Zainos A., Hernández A. Categorical perception of somesthetic stimuli: psychophysical measurements correlated with neuronal events in primate medial premotor cortex. Cereb Cortex. 1997 Jun;7(4):317–326. doi: 10.1093/cercor/7.4.317. [DOI] [PubMed] [Google Scholar]
  52. Romo R., Merchant H., Zainos A., Hernández A. Categorization of somaesthetic stimuli: sensorimotor performance and neuronal activity in primary somatic sensory cortex of awake monkeys. Neuroreport. 1996 May 17;7(7):1273–1279. [PubMed] [Google Scholar]
  53. Romo R., Ruiz S., Crespo P., Zainos A., Merchant H. Representation of tactile signals in primate supplementary motor area. J Neurophysiol. 1993 Dec;70(6):2690–2694. doi: 10.1152/jn.1993.70.6.2690. [DOI] [PubMed] [Google Scholar]
  54. Romo R., Salinas E. Sensing and deciding in the somatosensory system. Curr Opin Neurobiol. 1999 Aug;9(4):487–493. doi: 10.1016/S0959-4388(99)80073-7. [DOI] [PubMed] [Google Scholar]
  55. Romo R., Salinas E. Touch and go: decision-making mechanisms in somatosensation. Annu Rev Neurosci. 2001;24:107–137. doi: 10.1146/annurev.neuro.24.1.107. [DOI] [PubMed] [Google Scholar]
  56. Salinas E., Hernandez A., Zainos A., Romo R. Periodicity and firing rate as candidate neural codes for the frequency of vibrotactile stimuli. J Neurosci. 2000 Jul 15;20(14):5503–5515. doi: 10.1523/JNEUROSCI.20-14-05503.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Salinas E., Romo R. Conversion of sensory signals into motor commands in primary motor cortex. J Neurosci. 1998 Jan 1;18(1):499–511. doi: 10.1523/JNEUROSCI.18-01-00499.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Salzman C. D., Britten K. H., Newsome W. T. Cortical microstimulation influences perceptual judgements of motion direction. Nature. 1990 Jul 12;346(6280):174–177. doi: 10.1038/346174a0. [DOI] [PubMed] [Google Scholar]
  59. Seidemann E., Zohary E., Newsome W. T. Temporal gating of neural signals during performance of a visual discrimination task. Nature. 1998 Jul 2;394(6688):72–75. doi: 10.1038/27906. [DOI] [PubMed] [Google Scholar]
  60. Shadlen M. N., Newsome W. T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J Neurophysiol. 2001 Oct;86(4):1916–1936. doi: 10.1152/jn.2001.86.4.1916. [DOI] [PubMed] [Google Scholar]
  61. Shadlen M. N., Newsome W. T. Noise, neural codes and cortical organization. Curr Opin Neurobiol. 1994 Aug;4(4):569–579. doi: 10.1016/0959-4388(94)90059-0. [DOI] [PubMed] [Google Scholar]
  62. Shanks M. F., Pearson R. C., Powell T. P. The ipsilateral cortico-cortical connexions between the cytoarchitectonic subdivisions of the primary somatic sensory cortex in the monkey. Brain Res. 1985 Apr;356(1):67–88. doi: 10.1016/0165-0173(85)90019-0. [DOI] [PubMed] [Google Scholar]
  63. Sinclair R. J., Burton H. Neuronal activity in the second somatosensory cortex of monkeys (Macaca mulatta) during active touch of gratings. J Neurophysiol. 1993 Jul;70(1):331–350. doi: 10.1152/jn.1993.70.1.331. [DOI] [PubMed] [Google Scholar]
  64. Singer W., Gray C. M. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci. 1995;18:555–586. doi: 10.1146/annurev.ne.18.030195.003011. [DOI] [PubMed] [Google Scholar]
  65. 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. 1984 Apr;51(4):724–744. doi: 10.1152/jn.1984.51.4.724. [DOI] [PubMed] [Google Scholar]
  66. 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 hand. J Neurophysiol. 1968 Mar;31(2):301–334. doi: 10.1152/jn.1968.31.2.301. [DOI] [PubMed] [Google Scholar]
  67. Tokuno H., Tanji J. Input organization of distal and proximal forelimb areas in the monkey primary motor cortex: a retrograde double labeling study. J Comp Neurol. 1993 Jul 8;333(2):199–209. doi: 10.1002/cne.903330206. [DOI] [PubMed] [Google Scholar]
  68. Vallbo A. B., Johansson R. S. Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. Hum Neurobiol. 1984;3(1):3–14. [PubMed] [Google Scholar]
  69. Vogels R., Orban G. A. How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey. J Neurosci. 1990 Nov;10(11):3543–3558. doi: 10.1523/JNEUROSCI.10-11-03543.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES