Top-down signal from prefrontal cortex in executive control of memory retrieval
Abstract
Knowledge or experience is voluntarily recalled from memory by reactivation of the neural representations in the cerebral association cortex. In inferior temporal cortex, which serves as the storehouse of visual long-term memory, activation of mnemonic engrams through electric stimulation results in imagery recall in humans, and neurons can be dynamically activated by the necessity for memory recall in monkeys. Neuropsychological studies and previous split-brain experiments predicted that prefrontal cortex exerts executive control upon inferior temporal cortex in memory retrieval; however, no neuronal correlate of this process has ever been detected. Here we show evidence of the top-down signal from prefrontal cortex. In the absence of bottom-up visual inputs, single inferior temporal neurons were activated by the top-down signal, which conveyed information on semantic categorization imposed by visual stimulus-stimulus association. Behavioural performance was severely impaired with loss of the top-down signal. Control experiments confirmed that the signal was transmitted not through a subcortical but through a fronto-temporal cortical pathway. Thus, feedback projections from prefrontal cortex to the posterior association cortex appear to serve the executive control of voluntary recall.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Research in non-human primates demonstrated that top-down signals from the frontal cortex are important for the executive control of voluntary recall from long-term memory.
“Research in non-human primates demonstrated that top-down signals from the frontal cortex are important for the executive control of voluntary recall from long-term memory (Tomita et al., 1999).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Tomita et al., 1999
Cites
Plum, F. (1960) · Archives of Neurology · doi:10.1001/archneur.1960.03840090124020 · Cited by 10,377 · see citing works
Neural Mechanisms of Selective Visual Attention
Desimone, R., & Duncan, J. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.001205 · Cited by 8,388 · see citing works
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
Berti, A. (1992) · Neuropsychologia · doi:10.1016/0028-3932(92)90076-x · Cited by 4,190 · see citing works
The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe
Fuster, J. M. (1980) · Cited by 2,367 · see citing works
THE BRAIN’S RECORD OF AUDITORY AND VISUAL EXPERIENCE: A FINAL SUMMARY AND DISCUSSION
PENFIELD, W., & PEROT, P. (1963) · Brain · doi:10.1093/brain/86.4.595 · Cited by 1,230 · see citing works
The prefrontal cortex: Anatomy, physiology, and neuropsychology of the frontal lobe
Holmes, G. L. (1989) · Journal of Epilepsy · doi:10.1016/0896-6974(89)90035-2 · Cited by 1,210 · see citing works
Eling, P. (1993) · Acta Psychologica · doi:10.1016/0001-6918(93)90027-o · Cited by 1,198 · see citing works
Mishkin, M. (1982) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1982.0074 · Cited by 1,129 · see citing works
The problem of the frontal lobe: A reinterpretation
Nauta, W. J. H. (1971) · Journal of Psychiatric Research · doi:10.1016/0022-3956(71)90017-3 · Cited by 912 · see citing works
Regional and cellular fractionation of working memory
Goldman‐Rakic, P. S. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13473 · Cited by 810 · see citing works
Neural organization for the long-term memory of paired associates
Sakai, K., & Miyashita, Y. (1991) · Nature · doi:10.1038/354152a0 · Cited by 743 · see citing works
Self-citationChafee, M. V., & Goldman, P. S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.6.2919 · Cited by 655 · see citing works
Inferior Temporal Cortex: Where Visual Perception Meets Memory
Miyashita, Y. (1993) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.16.030193.001333 · Cited by 446 · see citing works
Self-citationProspective coding for objects in primate prefrontal cortex
Rainer, G., Rao, S. C., & Miller, E. K. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05493.1999 · Cited by 432 · see citing works
The functional roles of prefrontal cortex in episodic memory
Fletcher, P. C., Shallice, T., & Dolan, R. J. (1998) · Cited by 389 · see citing works
Functional interactions between inferotemporal and prefrontal cortex in a cognitive task
Fuster, J. M., Bauer, R. H., & Jervey, J. P. (1985) · Brain Research · doi:10.1016/0006-8993(85)90689-4 · Cited by 377 · see citing works
Functional Anatomic Studies of Memory Retrieval for Auditory Words and Visual Pictures
Buckner, R. L., Raichle, M. E., Miezin, F. M., & Petersen, S. E. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06219.1996 · Cited by 319 · see citing works
Cue-Invariant Shape Selectivity of Macaque Inferior Temporal Neurons
Sáry, G., Vogels, R., & Orban, G. A. (1993) · Science · doi:10.1126/science.8493538 · Cited by 311 · see citing works
Principles of human brain organization derived from split-brain studies
Gazzaniga, M. S. (1995) · Neuron · doi:10.1016/0896-6273(95)90280-5 · Cited by 287 · see citing works
The functional roles of prefrontal cortex in episodic memory. II. Retrieval
Fletcher, P. C. (1998) · Brain · doi:10.1093/brain/121.7.1249 · Cited by 272 · see citing works
Cognitive Interaction After Staged Callosal Section: Evidence for Transfer of Semantic Activation
Sidtis, J. J., Volpe, B. T., Holtzman, J. D., Wilson, D. H., & Gazzaniga, M. S. (1981) · Science · doi:10.1126/science.6782673 · Cited by 176 · see citing works
Eacott, M. J., & Gaffan, D. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00157.x · Cited by 152 · see citing works
Gross, C. G., Bender, D. B., & Mishkin, M. (1977) · Brain Research · doi:10.1016/0006-8993(77)90517-0 · Cited by 141 · see citing works
Callosal Window Between Prefrontal Cortices: Cognitive Interaction to Retrieve Long-Term Memory
Hasegawa, I., Fukushima, T., Ihara, T., & Miyashita, Y. (1998) · Science · doi:10.1126/science.281.5378.814 · Cited by 136 · see citing works
Self-citationActivity of primate inferotemporal neurons related to a sought target in pair-association task.
Naya, Y., Sakai, K., & Miyashita, Y. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.7.2664 · Cited by 119 · see citing works
Self-citationA quantitative method of computer analysis of spike train data collected from behaving animals
Macpherson, J. M., & Aldridge, J. W. (1979) · Brain Research · doi:10.1016/0006-8993(79)90530-4 · Cited by 94 · see citing works
Neural organization of higher visual functions
Rolls, E. T. (1991) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(91)90090-t · Cited by 86 · see citing works
Gutnikov, S. A., Ma, Y., & Gaffan, D. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01507.x · Cited by 64 · see citing works
Forebrain commissures and visual memory: A new approach
Doty, R. W., Ringo, J. L., & Lewine, J. D. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90031-9 · Cited by 23 · see citing works
Interhemispheric transfer of visual learning in monkeys with intact optic chiasm
Eacott, M. J., & Gaffan, D. (1989) · Experimental Brain Research · doi:10.1007/bf00248868 · Cited by 22 · see citing works
Ringo, J. L., & O’NEILL, S. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.6.2215 · Cited by 17 · see citing works
Miller, E. K. (1999) · Nature · doi:10.1038/44291 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices
Buschman, T. J., & Miller, E. K. (2007) · Science · doi:10.1126/science.1138071 · Cited by 2,380 · see citing works
The organization of recent and remote memories
Frankland, P. W., & Bontempi, B. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1607 · Cited by 2,138 · see citing works
The prefontral cortex and cognitive control
Miller, E. K. (2000) · Nature Reviews Neuroscience · doi:10.1038/35036228 · Cited by 2,016 · see citing works
Top-down facilitation of visual recognition
Bar, M., Kassam, K. S., Ghuman, A. S., Boshyan, J., Schmid, A. M., Dale, A. M., Hämäläinen, M. S., Marinkovic, K., Schacter, D. L., Rosen, B. R., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507062103 · Cited by 1,489 · see citing works
Left ventrolateral prefrontal cortex and the cognitive control of memory
Badre, D., & Wagner, A. D. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.06.015 · Cited by 1,471 · see citing works
Language‐specific tuning of visual cortex? Functional properties of the Visual Word Form Area
Cohen, L., Lehéricy, S., Chochon, F., Lemer, C., Rivaud, S., & Dehaene, S. (2002) · Brain · doi:10.1093/brain/awf094 · Cited by 1,254 · see citing works
Categorical Representation of Visual Stimuli in the Primate Prefrontal Cortex
Freedman, D. J., Riesenhuber, M., Poggio, T., & Miller, E. K. (2001) · Science · doi:10.1126/science.291.5502.312 · Cited by 1,123 · see citing works
Prefrontal and medial temporal lobe interactions in long-term memory
Simons, J. S., & Spiers, H. J. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1178 · Cited by 961 · see citing works
An adaptive coding model of neural function in prefrontal cortex
Duncan, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35097575 · Cited by 874 · see citing works
A cortical mechanism for triggering top-down facilitation in visual object recognition
Bar, M. (2003) · Journal of Cognitive Neuroscience · doi:10.1162/089892903321662976 · Cited by 900 · see citing works
Prefrontal–hippocampal interactions in episodic memory
Eichenbaum, H. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.74 · Cited by 870 · see citing works
Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex
Markov, N. T., Vezoli, J., Chameau, P., Falchier, A., Quilodran, R., Huissoud, C., Lamy, C., Misery, P., Giroud, P., Ullman, S., et al. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23458 · Cited by 759 · see citing works
Fast Readout of Object Identity from Macaque Inferior Temporal Cortex
Hung, C. P., Kreiman, G., Poggio, T., & DiCarlo, J. J. (2005) · Science · doi:10.1126/science.1117593 · Cited by 854 · see citing works
A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex
Larkum, M. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.11.006 · Cited by 755 · see citing works
Kar, K., Kubilius, J., Schmidt, K., Issa, E. B., & DiCarlo, J. J. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0392-5 · Cited by 496 · see citing works
Pollak, S. D., & Kistler, D. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.142165999 · Cited by 475 · see citing works
Dissociable contributions of prefrontal and parietal cortices to response selection
Bunge, S. A., Hazeltine, E., Scanlon, M. D., Rosen, A. C., & Gabrieli, J. D. E. (2002) · NeuroImage · doi:10.1006/nimg.2002.1252 · Cited by 468 · see citing works
Mechanisms of top-down attention
Baluch, F., & Itti, L. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.02.003 · Cited by 437 · see citing works
A Top-Down Cortical Circuit for Accurate Sensory Perception
Manita, S., Suzuki, T., Homma, C., Matsumoto, T., Odagawa, M., Yamada, K., Ota, K., Matsubara, C., Inutsuka, A., Sato, M., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.006 · Cited by 365 · see citing works
Neuronal correlates of decision-making in secondary somatosensory cortex
Romo, R., Hernández, A., Zainos, A., Lemus, L., & Brody, C. D. (2002) · Nature Neuroscience · doi:10.1038/nn950 · Cited by 387 · see citing works
Prefrontal modulation of visual processing in humans
Barceló, F., Suwazono, S., & Knight, R. T. (2000) · Nature Neuroscience · doi:10.1038/73975 · Cited by 374 · see citing works
Functional connectivity during working memory maintenance
GAZZALEY, A., RISSMAN, J., & D'ESPOSITO, M. (2004) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.4.4.580 · Cited by 337 · see citing works
Top-Down Control of Motor Cortex Ensembles by Dorsomedial Prefrontal Cortex
Narayanan, N. S., & Laubach, M. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.021 · Cited by 311 · see citing works
Recent advances in the neuropsychopharmacology of serotonergic hallucinogens
Halberstadt, A. L. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.07.016 · Cited by 312 · see citing works
“The PFC exerts top-down executive control over processing in temporal and parietal cortices (Tomita et al., 1999; Simons and Spiers, 2003; Merchant et al., 2011; Crowe et al., 2013).”
BackgroundDecomposing components of task preparation with functional magnetic resonance imaging.
Brass, M., & Cramon, D. Y. V. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/089892904323057335 · Cited by 302 · see citing works
Gazzaley, A., Rissman, J., Cooney, J., Rutman, A., Seibert, T., Clapp, W., & D'Esposito, M. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm113 · Cited by 287 · see citing works
Who Comes First? The Role of the Prefrontal and Parietal Cortex in Cognitive Control
Brass, M., Ullsperger, M., Knoesche, T. R., Cramon, D. Y. V., & Phillips, N. A. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929054985400 · Cited by 236 · see citing works
Hamker, F. H. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhh146 · Cited by 217 · see citing works
Specializations for reward-guided decision-making in the primate ventral prefrontal cortex
Murray, E. A., & Rudebeck, P. H. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0013-4 · Cited by 169 · see citing works
Task-dependent changes in short-term memory in the prefrontal cortex
Warden, M. R., & Miller, E. K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1569-10.2010 · Cited by 171 · see citing works
Krawczyk, D. C., Gazzaley, A., & D'Esposito, M. (2007) · Brain Research · doi:10.1016/j.brainres.2007.01.052 · Cited by 156 · see citing works
Frontal lobes and attention: Processes and networks, fractionation and integration
STUSS, D. T. (2006) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617706060358 · Cited by 150 · see citing works
Causal neural network of metamemory for retrospection in primates
Miyamoto, K., Osada, T., Setsuie, R., Takeda, M., Tamura, K., Adachi, Y., & Miyashita, Y. (2017) · Science · doi:10.1126/science.aal0162 · Cited by 106 · see citing works
Self-citationLenka, A., Jhunjhunwala, K. R., Saini, J., & Pal, P. K. (2015) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2015.04.005 · Cited by 106 · see citing works
Lee, A. J., Wang, G., Jiang, X., Johnson, S. M., Hoang, E. T., Lanté, F., Stornetta, R. L., Beenhakker, M. P., Shen, Y., & Julius Zhu, J. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu020 · Cited by 94 · see citing works
van Wingen, G. A., van Eijndhoven, P., Cremers, H. R., Tendolkar, I., Verkes, R. J., Buitelaar, J. K., & Fernández, G. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2009.11.009 · Cited by 63 · see citing works
Prefrontal feature representations drive memory recall
Yadav, N., Noble, C., Niemeyer, J. E., Terceros, A., Victor, J., Liston, C., & Rajasethupathy, P. (2022) · Nature · doi:10.1038/s41586-022-04936-2 · Cited by 61 · see citing works
Forgotten frontal lobe syndrome or “Executive Dysfunction Syndrome”
Lyketsos, C. G., Rosenblatt, A., & Rabins, P. (2004) · Psychosomatics · doi:10.1176/appi.psy.45.3.247 · Cited by 53 · see citing works
A bird-brain view of episodic memory
Rattenborg, N. C., & Martinez-Gonzalez, D. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.030 · Cited by 45 · see citing works
Age-related effects in working memory recognition modulated by retroactive interference.
Solesio-Jofre, E., Lorenzo-Lopez, L., Gutierrez, R., Lopez-Frutos, J. M., Ruiz-Vargas, J. M., & Maestu, F. (2012) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glr199 · Cited by 35 · see citing works
Linking unfounded beliefs to genetic dopamine availability
Schmack, K., Rössler, H., Sekutowicz, M., Brandl, E. J., Müller, D. J., Petrovic, P., & Sterzer, P. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00521 · Cited by 24 · see citing works
Attentional Recruitment of Inter-Areal Recurrent Networks for Selective Gain Control
Hahnloser, R. H. R., Douglas, R. J., & Hepp, K. (2002) · Neural Computation · doi:10.1162/08997660260028665 · Cited by 18 · see citing works
Computational model of visual hallucination in dementia with Lewy bodies
Tsukada, H., Fujii, H., Aihara, K., & Tsuda, I. (2015) · Neural Networks · doi:10.1016/j.neunet.2014.09.001 · Cited by 17 · see citing works
Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice
Marin-Garcia, E., Mattfeld, A. T., & Gabrieli, J. D. E. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.584560 · Cited by 11 · see citing works
- Authors
- Tomita, H., Ohbayashi, M., Nakahara, K., Hasegawa, I., & Miyashita, Y.
- Affiliations
- The University of Tokyo (JP)
- Japan Science and Technology Agency (JP)
- Corresponding author
- Tomita, Hyoe
- Miyashita, Yasushi
- Venue
- Nature
- Published
- 1999-10
- Volume
- 401
- Issue
- 6754
- Pages
- 699-703
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2012252610
- Cited by
- 615
- References
- 33
- Citations by year
- 2026: 11 · 2025: 14 · 2024: 18 · 2023: 7 · 2022: 18 · 2021: 21 · 2020: 14 · 2019: 22 · 2018: 20 · 2017: 21 · 2016: 21 · 2015: 20 · 2014: 25 · 2013: 25 · 2012: 19
- FWCI
- 13.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- top-down signals, prefrontal cortex, executive function, memory retrieval, inferior temporal cortex, visual long-term memory, single-unit recording, semantic classification, stimulus-stimulus associations, voluntary recall, feedback projections
- MeSH terms
- Animals, Cues, Macaca, Models, Neurological, Neural Pathways, Neurons, Mental Recall, Prefrontal Cortex
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review