Skip to main content
SpringerLink
Log in

Single-cell coding of sensory, spatial and numerical magnitudes in primate prefrontal, premotor and cingulate motor cortices

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The representation of magnitude information enables humans and animal species alike to successfully interact with the external environment. However, how various types of magnitudes are processed by single neurons to guide goal-directed behavior remains elusive. Here, we recorded single-cell activity from the dorsolateral prefrontal (PFC), dorsal premotor (PMd) and cingulate motor (CMA) cortices in monkeys discriminating discrete numerical (numerosity), continuous spatial (line length) and basic sensory (spatial frequency) stimuli. We found that almost exclusively PFC neurons represented the different magnitude types during sample presentation and working memory periods. The frequency of magnitude-selective cells in PMd and CMA did not exceed chance level. The proportion of PFC neurons selectively tuned to each of the three magnitude types were comparable. Magnitude coding was mainly dissociated at the single-neuron level, with individual neurons representing only one of the three tested magnitude types. Neuronal magnitude discriminability, coding strength and temporal evolution were comparable between magnitude types encoded by PFC neuron populations. Our data highlight the importance of PFC neurons in representing various magnitude categories. Such magnitude representations are based on largely distributed coding by single neurons that are anatomically intermingled within the same cortical area.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Asaad WF, Rainer G, Miller EK (2000) Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol 84:451–459

    PubMed  CAS  Google Scholar 

  • Badre D, D’Esposito M (2009) Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci 10:659–669

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 256:211–288

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375

    Article  PubMed  CAS  Google Scholar 

  • Bates JF, Goldman-Rakic PS (1993) Prefrontal connections of medial motor areas in the rhesus monkey. J Comp Neurol 336:211–288

    Article  PubMed  CAS  Google Scholar 

  • Bongard S, Nieder A (2010) Basic mathematical rules are encoded by primate prefrontal cortex neurons. Proc Natl Acad Sci USA 107:2277–2282

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cappelletti M, Freeman ED, Cipolotti L (2009) Dissociations and interactions between time, numerosity and space processing. Neuropsychologia 47:2732–2748

    Article  PubMed  PubMed Central  Google Scholar 

  • Casasanto D, Fotakopoulou O, Boroditsky L (2010) Space and time in the child’s mind: evidence for a cross-dimensional asymmetry. Cogn Sci 34:387–405

    Article  PubMed  Google Scholar 

  • Castelli F, Glaser DE, Butterworth B (2006) Discrete and analogue quantity processing in the parietal lobe: a functional MRI study. Proc Natl Acad Sci USA 103:4693–4698

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chafee MV, Goldman-Rakic PS (2000) Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. J Neurophysiol 83:1550–1566

    PubMed  CAS  Google Scholar 

  • Constantinidis C, Franowics MN, Goldman-Rakic PS (2001) The sensory nature of mnemonic representation in the primate prefrontal cortex. Nat Neurosci 4:311–316

    Article  PubMed  CAS  Google Scholar 

  • de Hevia MD, Girelli L, Bricolo E, Vallar G (2008) The representational space of numerical magnitude: illusions of length. Q J Exp Psychol 61:1496–1514

    Article  Google Scholar 

  • De Valois RL, Albrecht DG, Thorell LG (1982) Spatial frequency selectivity of cells in macaque visual cortex. Vis Res 22:545–559

    Article  PubMed  Google Scholar 

  • Dehaene S, Changeux JP (1993) Development of elementary numerical abilities: a neuronal model. J Cogn Neurosci 5:390–407

    Article  PubMed  CAS  Google Scholar 

  • Dehaene S, Spelke E, Stanescu R, Pinel P, Tsivkin S (1999) Sources of mathematical thinking: behavioral and brain-imaging evidence. Science 284:970–974

    Article  PubMed  CAS  Google Scholar 

  • di Pelligrino G, Wise SP (1991) A neurophysiological comparison of three distinct regions of the primate frontal lobe. Brain 114:951–978

    Article  Google Scholar 

  • Diester I, Nieder A (2008) Complementary contributions of prefrontal neuron classes in abstract numerical categorization. J Neurosci 28:7737–7747

    Article  PubMed  CAS  Google Scholar 

  • Ditz HM, Nieder A (2015) Neurons selective to the number of visual items in the corvid songbird endbrain. Proc Natl Acad Sci USA 112:7827–7832

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dormal V, Pesenti M (2007) Numerosity-length interference: a Stroop experiment. Exp Psychol 54:289–297

    Article  PubMed  Google Scholar 

  • Dormal V, Pesenti M (2009) Common and specific contributions of the intraparietal sulci to numerosity and length processing. Hum Brain Mapp 30:2466–2476

    Article  PubMed  Google Scholar 

  • Eger E, Sterzer P, Russ MO, Giraud AL, Kleinschmidt A (2003) A supramodal number representation in human intraparietal cortex. Neuron 37:719–725

    Article  PubMed  CAS  Google Scholar 

  • Eiselt AK, Nieder A (2013) Representation of abstract quantitative rules applied to spatial and numerical magnitudes in primate prefrontal cortex. J Neurosci 33:7526–7534

    Article  PubMed  CAS  Google Scholar 

  • Eiselt AK, Nieder A (2014) Rule-activity related to spatial and numerical magnitudes: comparison of prefrontal, premotor and cingulate motor cortices. J Cogn Neurosci 26:1000–1012

    Article  PubMed  Google Scholar 

  • Genovesio A, Brasted PJ, Mitz AR, Wise SP (2005) Prefrontal cortex activity related to abstract response strategies. Neuron 47:307–320

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Genovesio A, Tsujimoto S, Wise SP (2009) Feature- and order-based timing representations in the frontal cortex. Neuron 63:254–266

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Genovesio A, Tsujimoto S, Wise SP (2011) Prefrontal cortex activity during the discrimination of relative distance. J Neurosci 31:3968–3980

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Green DM, Swets JA (1966) Signal detection theory and psychophysics. Wiley, New York

    Google Scholar 

  • Hayashi MJ, Kanai R, Tanabe HC, Yoshida Y, Carlson S, Walsh V, Sadato N (2013) Interaction of numerosity and time in prefrontal and parietal cortex. J Neurosci 33:883–893

    Article  PubMed  CAS  Google Scholar 

  • Henik A, Tzelgov H (1982) Is three greater than five: the relation between physical and semantic size in comparison tasks. Mem Cognit 10:389–395

    Article  PubMed  CAS  Google Scholar 

  • Hernadi I, Grabenhorst F, Schultz W (2015) Planning activity for internally generated reward goals in monkey amygdala neurons. Nat Neurosci 18:461–469

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hernandez A, Nacher V, Luna R, Zainos A, Lemus L, Alvarez M, Vazquez Y, Camarillo L, Romo R (2010) Decoding a perceptual decision process across cortex. Neuron 66:300–314

    Article  PubMed  CAS  Google Scholar 

  • Hoshi E, Tanji J (2006) Differential involvement of neurons in the dorsal and ventral premotor cortex during processing of visual signals for action planning. J Neurophysiol 95:3596–3616

    Article  PubMed  Google Scholar 

  • Hoshi E, Shima K, Tanji J (1998) Task-dependent selectivity of movement-related neuronal activity in the primate prefrontal cortex. J Neurophysiol 80:3392–3397

    PubMed  CAS  Google Scholar 

  • Hubbard EM, Piazza M, Pinel P, Dehaene S (2005) Interactions between number and space in parietal cortex. Nat Rev Neurosci 6:435–448

    Article  PubMed  CAS  Google Scholar 

  • Hussar CR, Pasternak T (2009) Flexibility of sensory representations in prefrontal cortex depends on cell type. Neuron 64:730–743

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hussar CR, Pasternak T (2012) Memory-guided sensory comparison in the prefrontal cortex: contribution of putative pyramidal cells and interneurons. J Neurosci 32:2747–2761

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hussar CR, Pasternak T (2013) Common rules guide comparison of speed and direction of motion in the dorsolateral prefrontal cortex. J Neurosci 33:972–986

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Issa NP, Trepel C, Stryker MP (2000) Spatial frequency maps in cat visual cortex. J Neurosci 20:8504–8515

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jacob SN, Nieder A (2009) Tuning to non-symbolic proportions in the human frontoparietal cortex. Eur J Neurosci 30:1432–1442

    Article  PubMed  Google Scholar 

  • Jacob SN, Nieder A (2014) Complementary roles for primate frontal and parietal cortex in guarding working memory from distractor stimuli. Neuron 83:226–237

    Article  PubMed  CAS  Google Scholar 

  • Jacob SN, Vallentin D, Nieder A (2012) Relating magnitudes: the brain’s code for proportions. Trends Cogn Sci 16:157–166

    Article  PubMed  Google Scholar 

  • Kurata K, Tsuji T, Naraki S, Seino M, Abe Y (2000) Activation of the dorsal premotor cortex and pre-supplementary motor area of humans during an auditory conditional motor task. J Neurophysiol 84:1667–1672

    PubMed  CAS  Google Scholar 

  • Lu A, Hodges B, Zhang J, Zhang JX (2009) Contextual effects on number-time interaction. Cognition 113:117–122

    Article  PubMed  Google Scholar 

  • Maffei L, Fiorentini A (1973) The visual cortex as a spatial frequency analyzer. Vis Res 13:1255–1267

    Article  PubMed  CAS  Google Scholar 

  • Merten K, Nieder A (2012) Active encoding of decisions about stimulus absence in primate prefrontal cortex neurons. Proc Natl Acad Sci USA 109:6289–6294

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Merten K, Nieder A (2013) Comparison of abstract decision encoding in the monkey prefrontal cortex, the presupplementary and cingulate motor areas. J Neurophysiol 110:19–32

    Article  PubMed  Google Scholar 

  • Muhammad R, Wallis JD, Miller EK (2006) A comparison of abstract rules in the prefrontal cortex, premotor cortex, the inferior temporal cortex and the striatum. J Cogn Neurosci 18:974–989

    Article  PubMed  Google Scholar 

  • Nieder A (2009) Prefrontal cortex and the evolution of symbolic reference. Curr Opin Neurobiol 19:99–108

    Article  PubMed  CAS  Google Scholar 

  • Nieder A (2013) Coding of abstract quantity by ‘number neurons’ of the primate brain. J Comp Physiol A 199:1–16

    Article  Google Scholar 

  • Nieder A, Dehaene S (2009) Representation of number in the brain. Annu Rev Neurosci 32:185–208

    Article  PubMed  CAS  Google Scholar 

  • Nieder A, Miller EK (2004) A parieto-frontal network for visual numerical information in the monkey. Proc Natl Acad Sci USA 101:7457–7462

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nieder A, Freedman DJ, Miller EK (2002) Representation of the quantity of visual items in the primate prefrontal cortex. Science 297:1708–1711

    Article  PubMed  CAS  Google Scholar 

  • Onoe H, Komori M, Onoe K, Takechi H, Tsukada H, Watanabe Y (2001) Cortical networks recruited for time perception: a monkey positron emission tomography (PET) study. Neuroimage 13:37–45

    Article  PubMed  CAS  Google Scholar 

  • Ott T, Jacob SN, Nieder A (2014) Dopamine receptors differentially enhance rule coding in primate prefrontal cortex neurons. Neuron 84:1317–1328

    Article  PubMed  CAS  Google Scholar 

  • Padoa-Schioppa C, Assad JA (2006) Neurons in the orbitofrontal cortex encode economic value. Nature 441:223–226

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Passingham RE (1988) Premotor cortex and preparation for movement. Exp Brain Res 70:590–596

    Article  PubMed  CAS  Google Scholar 

  • Peng X, van Essen DC (2005) Peaked encoding of relative luminance in macaque areas V1 and V2. J Neurophysiol 93:1620–1632

    Article  PubMed  Google Scholar 

  • Petrides M (2005) Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc Lond B Biol Sci 360:781–795

    Article  PubMed  PubMed Central  Google Scholar 

  • Petrides M, Pandya DN (2007) Efferent association pathways from the rostral prefrontal cortex in the macaque monkey. J Neurosci 27:11573–11586

    Article  PubMed  CAS  Google Scholar 

  • Piazza M, Pinel P, Le Bihan D, Dehaene S (2007) A magnitude code common to numerosities and number symbols in human intraparietal cortex. Neuron 53:293–305

    Article  PubMed  CAS  Google Scholar 

  • Picard N, Strick PL (2001) Imaging the premotor areas. Curr Opin Neurobiol 11:663–672

    Article  PubMed  CAS  Google Scholar 

  • Pinel P, Piazza M, Le Bihan D, Dehaene S (2004) Distributed and overlapping cerebral representation of number, size, and luminance during comparative judgments. Neuron 41:1–20

    Article  Google Scholar 

  • Rao SM, Mayer AR, Harrington DL (2001) The evolution of brain activation during temporal processing. Nat Neurosci 4:317–323

    Article  PubMed  CAS  Google Scholar 

  • Robson JG, Tolhurst DJ, Freeman RD, Ohzawa I (1988) Simple cells in the visual cortex of the cat can be narrowly tuned for spatial frequency. Vis Neurosci 1:415–419

    Article  PubMed  CAS  Google Scholar 

  • Romo R, Brody CD, Hernandez A, Lemus L (1999) Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399:470–473

    Article  PubMed  CAS  Google Scholar 

  • Schumacher EH, Elston PA, D’Esposito M (2003) Neural evidence for representation-specific response selection. J Cogn Neurosci 15:1111–1121

    Article  PubMed  Google Scholar 

  • Schwarz W, Eiselt AK (2009) The perception of temporal order along the mental number line. J Exp Psychol Hum Percept Perform 35:989–1004

    Article  PubMed  Google Scholar 

  • Tanji J, Hoshi E (2008) Role of lateral prefrontal cortex in executive behavioral control. Physiol Rev 88:37–57

    Article  PubMed  Google Scholar 

  • Tudusciuc O, Nieder A (2007) Neuronal population coding of continuous and discrete quantity in the primate posterior parietal cortex. Proc Natl Acad Sci USA 104:14513–14518

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tudusciuc O, Nieder A (2009) Contributions of primate prefrontal and posterior parietal cortices to length and numerosity representation. J Neurophysiol 101:2984–2994

    Article  PubMed  Google Scholar 

  • Turken AU, Swick D (1999) Response selection in the human anterior cingulate cortex. Nat Neurosci 2:920–924

    Article  PubMed  CAS  Google Scholar 

  • Vallentin D, Nieder A (2008) Behavioral and prefrontal representation of spatial proportions in the monkey. Curr Biol 18:1420–1425

    Article  PubMed  CAS  Google Scholar 

  • Vallentin D, Nieder A (2010) Representations of visual proportions in the primate posterior parietal and prefrontal cortices. Eur J Neurosci 32:1380–1387

    Article  PubMed  Google Scholar 

  • Viswanathan P, Nieder A (2013) Neuronal correlates of a visual ‘sense of number’ in primate parietal and prefrontal cortices. Proc Natl Acad Sci USA 110:11187–11192

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Viswanathan P, Nieder A (2015) Differential impact of behavioral relevance on quantity coding in primate frontal and parietal neurons. Curr Biol 25:1259–1269

    Article  PubMed  CAS  Google Scholar 

  • Wallis JD, Miller EK (2003) From rule to response: neuronal processes in the premotor and prefrontal cortex. J Neurophysiol 90:1790–1806

    Article  PubMed  Google Scholar 

  • Wallis JD, Anderson KC, Miller EK (2001) Single neurons in prefrontal cortex encode abstract rules. Nature 411:953–956

    Article  PubMed  CAS  Google Scholar 

  • Walsh V (2003) A theory of magnitude: common cortical metrics of time, space and quantity. Trends Cogn Sci 7:483–488

    Article  PubMed  Google Scholar 

  • White IM, Wise SP (1999) Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res 126:315–335

    Article  PubMed  CAS  Google Scholar 

  • Xuan B, Zhang D, He S, Chen X (2007) Larger stimuli are judged to last longer. J Vis 7(2):1–5

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Supported by the Bernstein Center for Computational Neuroscience, Tuebingen (BMBF; FKZ: 01GQ1002).

Author information

Author notes

  1. Anne-Kathrin Eiselt

    Present address: Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA, 20147, USA

Authors and Affiliations

  1. Animal Physiology, Institute of Neurobiology, University of Tübingen, Auf der Morgenstelle 28, 72076, Tübingen, Germany

    Anne-Kathrin Eiselt & Andreas Nieder

Authors
  1. Anne-Kathrin Eiselt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andreas Nieder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas Nieder.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eiselt, AK., Nieder, A. Single-cell coding of sensory, spatial and numerical magnitudes in primate prefrontal, premotor and cingulate motor cortices. Exp Brain Res 234, 241–254 (2016). https://doi.org/10.1007/s00221-015-4449-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-015-4449-8

Keywords

Search

Navigation