Abstract
Humans and monkeys have similar abilities to discriminate the difference in frequency between two mechanical vibrations applied sequentially to the fingertips1,2,3. A key component of this sensory task is that the second stimulus is compared with the trace left by the first (base) stimulus, which must involve working memory. Where and how is this trace held in the brain? This question was investigated by recording from single neurons in the prefrontal cortex of monkeys while they performed the somatosensory discrimination task. Here we describe neurons in the inferior convexity of the prefrontal cortex whose discharge rates varied, during the delay period between the two stimuli, as a monotonic function of the base stimulus frequency. We describe this as ‘monotonic stimulus encoding’, and we suggest that the result may generalize: monotonic stimulus encoding may be the basic representation of one-dimensional sensory stimulus quantities in working memory. Thus we predict that other behavioural tasks that require ordinal comparisons between scalar analogue stimuli would give rise to monotonic responses similar to those reported here.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Mountcastle, V. B., Steinmetz, M. A. & Romo, R. Frequency discrimination in the sense of the flutter: psychophysical measurements correlated with postcentral events in behaving monkeys. J. Neurosci. 10, 3032–3044 (1990).
Hernandez, A., Salinas, E., Garcia, R. & Romo, R. Discrimination in the sense of flutter: new psychophysical measurements in monkeys. J. Neurosci. 17, 6391–6400 (1997).
Romo, R., Hernandez, A., Zainos, A. & Salinas, E. Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390 (1998).
Mountcastle, V. B., Reitboeck, H. J., Poggio, G. F. & Steinmetz, M. A. Adaptation of the Reitboeck method of multiple microelectrode recording to the neocortex of the waking monkey. J. Neurosci. Methods. 36, 77–84 (1991).
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. 31, 301–334 (1968).
Wilson, F. A. W., O'Scalaidhe, S. P. & Goldman-Rakic, P. S. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 1955–1958 (1993).
Fuster, J. M. The Prefrontal Cortex 2nd edn(Raven, New York, (1989).
Chafee, M. V. & Goldman-Rakic, P. S. Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working-memory task. J. Neurophysiol. 79, 2919–2940 (1998).
Kojima, S. & Goldman-Rakic, P. S. Delay-related activity of prefrontal neurons in rhesus-monkeys performing delayed-response. Brain Res. 248, 43–49 (1982).
Bruce, C. J. & Goldberg, M. E. Primate frontal eye fields. I. Single neurons discharging before saccades. J. Neurophysiol. 53, 603–635 (1985).
Funahashi, S., Bruce, C. J. & Goldman-Rakic, P. S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331–349 (1989).
Funahashi, S., Bruce, C. J. & Goldman-Rakic, P. S. Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. J. Neurophysiol. 63, 814–831 (1990).
Hoshi, E., Shima, K. & Tanji, J. Task-dependent selectivity of movement-related neuronal activity in the primate prefrontal cortex. J. Neurophysiol. 80, 3392–3397 (1998).
Quintana, J. & Fuster, J. M. Mnemonic and predictive functions of cortical neurons in a memory task. Neuroreport 3, 721–724 (1992).
Asaad, W. A., Rainer, G. & Miller, E. K. Neural activity in the primate prefrontal cortex during associative learning. Neuron 21, 1399–1407 (1998).
Schultz, W. & Romo, R. Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum. Exp. Brain Res. 91, 363–384 (1992).
Seung, H. S. How the brain keeps the eyes still. Proc. Natl Acad. Sci. USA 93, 13339–13344 (1996).
Pandya, D. N. & Barnes, C. L. in The Frontal Lobes Revisited(ed. Perecman, E.) 41–72 (IRBN, New York, (1987).
Preuss, T. M. & Goldman-Rakic, P. S. Connections of the ventral granular frontal cortex of macaques with persylvian premotor and somatosensory areas: anatomical evidence for somatic representation in primate frontal association cortex. J. Comp. Neurol. 282, 293–316 (1989).
Salinas, E., Hernández, A., Zainos, A., Lemus, L. & Romo, R. Cortical recoding of sensory stimuli during somatosensory discrimination. Soc. Neurosci. Abstr. 24, 1126 (1998).
Zhou, Y. & Fuster, J. M. Mnemonic neuronal activity in somatosensory cortex. Proc. Natl Acad. Sci. USA 93, 10533–10537 (1996).
Rao, S. C., Rainer, G. & Miller, E. K. Integration of what and where in the primate prefrontal cortex. Science 276, 821–824 (1997).
Rainer, G., Asaad, W. F. & Miller, E. K. Memory fields of neurons in the primate prefrontal cortex. Proc. Natl Acad. Sci. USA 95, 15008–15013 (1998).
Bodner, M., Kroger, J. & Fuster, J. M. Auditory memory cells in dorsolateral prefrontal cortex. Neuroreport 96, 1905–1908 (1996).
Miller, E. K., Erickson, C. A. & Desimone, R. Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J. Neurosci. 16, 5154–5167 (1996).
Ross, S. M. Introduction to Probability for Scientists and Engineers(Wiley, New York, (1987).
Press, W., Teukolsky, S. A., Vettering, W. T. & Flannery, B. P. Numerical Recipes in C 2nd edn(Cambridge Univ. Press, Cambridge, U.K., (1992).
Acknowledgements
The research of R.R. was partially supported by an International Research Scholars Award from the Howard Hughes Medical Institute and grants from DGAPA-UNAM, CONA-CyT and Fundación Miguel Alemán A.C. We thank W. Newsome, M. Shadlen, their research groups, and V.Mountcastle and E. Salinas for extensive comments and discussion; A. Zainos for help during the experiments; and F. Jandete and S. Méndez for technical assistance. R.R. conceived the experiment, and together with A.H. and L.L. carried it out; C.D.B. designed and carried out the data analysis; R.R. and C.D.B. co-wrote the paper.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Romo, R., Brody, C., Hernández, A. et al. Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399, 470–473 (1999). https://doi.org/10.1038/20939
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/20939
This article is cited by
-
Dataset of human-single neuron activity during a Sternberg working memory task
Scientific Data (2024)
-
Diminished activation of excitatory neurons in the prelimbic cortex leads to impaired working memory capacity in mice
BMC Biology (2023)
-
Geometry of visuospatial working memory information in miniature gaze patterns
Nature Human Behaviour (2023)
-
A unifying perspective on neural manifolds and circuits for cognition
Nature Reviews Neuroscience (2023)
-
Multitask computation through dynamics in recurrent spiking neural networks
Scientific Reports (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.