Skip to main content

Cellular Mechanisms of Working Memory and its Modulation by Dopamine in the Prefrontal Cortex of Primates and Rats

  • Chapter
Book cover Monoaminergic Modulation of Cortical Excitability

In this chapter we first present a simplified and abbreviated view of the complex organization of the PFC in rodents and primates with an emphasis on those properties that might represent the substrate of putative WM functions. We will then compare the primate dorsolateral and rat medial PFC modulation by dopaminergic afferents. Finally, we give an overview of the properties of PFC neurons in primate and rat PFC during WM tasks.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alexander, G.E., Crutcher, M.D., and DeLong, M.R. (1990). Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85, 119-146.

    PubMed  CAS  Google Scholar 

  • Amemori, K. and Sawaguchi, T. (2006) Contrasting effects of reward expectation on sensory and motor memories in primate prefrontal neurons. Cereb Cortex 16, 1002-1015.

    PubMed  Google Scholar 

  • Anderson, S.A., Classey, J.D., Conde, F., Lund, J.S., and Lewis, D.A. (1995) Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex. Neuroscience 67, 7-22.

    PubMed  CAS  Google Scholar 

  • Ariano, M.A., Wang, J., Noblett, K.L., Larson, E.R., and Sibley, D.R. (1997) Cellular distribu-tion of the rat D4 dopamine receptor protein in the CNS using anti-receptor antisera. Brain Res 752, 26-34.

    PubMed  CAS  Google Scholar 

  • Baeg, E.H., Kim, Y.B., Huh, K., Mook-Jung, I., Kim, H.T., and Jung, M.W. (2003) Dynamics of population code for working memory in the prefrontal cortex. Neuron 40, 177-188.

    PubMed  CAS  Google Scholar 

  • Barch, D.M. (2006) What can research on schizophrenia tell us about the cognitive neurosci-ence of working memory? Neuroscience 139, 73-84.

    PubMed  CAS  Google Scholar 

  • Batuev, A.S., Kursina, N.P., and Shutov, A.P. (1990) Unit activity of the medial wall of the frontal cortex during delayed performance in rats. Behav Brain Res 41, 95-102.

    PubMed  CAS  Google Scholar 

  • Berendse, H.W., Galis -de Graaf, Y., and Groenewegen, H.J. (1992) Topographical organiza-tion and relationship with ventral striatal compartments of prefrontal corticostriatal pro-jections in the rat. J Comp Neurol 316, 314-347.

    PubMed  CAS  Google Scholar 

  • Berger, B., Gaspar, P., and Verney, C. (1991) Dopaminergic innervation of the cerebral cor-tex: unexpected differences between rodents and primates. Trends Neurosci 14, 21-27.

    PubMed  CAS  Google Scholar 

  • Bergson, C., Mrzljak, L., Smiley, J.F., Pappy, M., and Goldman-Rakic, P.S. (1995) Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J Neurosci 15, 7821-7836.

    PubMed  CAS  Google Scholar 

  • Berridge, K.C. (2006) The debate over dopamine’s role in reward: the case for incentive sali-ence. Psychopharmacol (Berl) 191 (3): 391-431.

    Google Scholar 

  • Brozoski, T.J., Brown, R.M., Rosvold, H.E., and Goldman, P.S. (1979) Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205, 929-932.

    PubMed  CAS  Google Scholar 

  • Brunel, N. and Wang, X.J. (2001) Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. J Comp Neurosci 11, 63-85.

    CAS  Google Scholar 

  • Carr, D.B. and Sesack, S.R. (1996) Hippocampal afferents to the rat prefrontal cortex: synap-tic targets and relation to dopamine terminals. J Comp Neurol 369, 1-15.

    PubMed  CAS  Google Scholar 

  • Chafee, M.V. and Goldman-Rakic, P.S. (1998) Matching patterns of activity in primate pre-frontal area 8a and parietal area 7ip neurons during a spatial working memory task. J Neurophysiol 79, 2919-2940.

    PubMed  CAS  Google Scholar 

  • Chang, J.Y., Chen, L., Luo, F., Shi, L.H., and Woodward, D.J. (2002) Neuronal responses in the frontal cortico-basal ganglia system during delayed matching-to-sample task: ensem-ble recording in freely moving rats. Exp Brain Res 142, 67-80.

    PubMed  Google Scholar 

  • Chang, Y.M., Rosene, D.L., Killiany, R.J., Mangiamele, L.A., and Luebke, J.I. (2005) Increased action potential firing rates of layer 2/3 pyramidal cells in the prefrontal cortex are significantly related to cognitive performance in aged monkeys. Cereb Cortex 15, 409-418.

    PubMed  Google Scholar 

  • Compte, A., Brunel, N., Goldman-Rakic, P.S., and Wang, X.J. (2000) Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10, 910-923.

    PubMed  CAS  Google Scholar 

  • Conde, F., Lund, J.S., Jacobowitz, D.M., Baimbridge, K.G., and Lewis, D.A. (1994) Local circuit neurons immunoreactive for calretinin, calbindin D- 28k or parvalbumin in mon-key prefrontal cortex: distribution and morphology. J Comp Neurol 341, 95-116.

    PubMed  CAS  Google Scholar 

  • Conde, F., Maire-Lepoivre, E., Audinat, E., and Crepel, F. (1995) Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J Comp Neurol 352, 567-593.

    CAS  Google Scholar 

  • Constantinidis, C. and Procyk, E. (2004) The primate working memory networks. Cogn Affect. Behav Neurosci 4, 444-465.

    Google Scholar 

  • Constantinidis, C. and Steinmetz, M.A. (1996) Neuronal activity in posterior parietal area 7a during the delay periods of a spatial memory task. J Neurophysiol 76, 1352-1355.

    PubMed  CAS  Google Scholar 

  • Constantinidis, C., Franowicz, M.N., and Goldman-Rakic, P.S. (2001) Coding specificity in cortical microcircuits: a multiple -electrode analysis of primate prefrontal cortex. J Neu-rosci 21, 3646-3655.

    CAS  Google Scholar 

  • DeFelipe, J., Alonso-Nanclares, L., and Arellano, J.I. (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31, 299-316.

    PubMed  Google Scholar 

  • Degenetais, E., Thierry, A.M., Glowinski, J., and Gioanni, Y. (2002) Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Cortex 12, 1-16.

    PubMed  Google Scholar 

  • Duan, H., Wearne, S.L., Rocher, A.B., Macedo, A., Morrison, J.H., and Hof, P.R. (2003) Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex 13, 950-961.

    PubMed  Google Scholar 

  • Durstewitz, D., Kelc, M., and Gunturkun, O. (1999) A neurocomputational theory of the dopaminergic modulation of working memory functions. J Neurosci 19, 2807-2822.

    PubMed  CAS  Google Scholar 

  • Durstewitz, D., Seamans, J.K., and Sejnowski, T.J. (2000a) Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83, 1733-1750.

    PubMed  CAS  Google Scholar 

  • Durstewitz, D., Seamans, J.K., and Sejnowski, T.J. (2000b) Neurocomputational models of working memory. Nature Neurosci 3, 1184-1191.

    PubMed  CAS  Google Scholar 

  • Elston, G.N., Benavides-Piccione, R., and DeFelipe, J. (2001) The pyramidal cell in cognition: a comparative study in human and monkey. J Neurosci 21, RC163.

    PubMed  CAS  Google Scholar 

  • Erickson, S.L. and Lewis, D.A. (2004) Cortical connections of the lateral mediodorsal thala-mus in cynomolgus monkeys. J Comp Neurol 473, 107-127.

    PubMed  Google Scholar 

  • Fisk, G.D. and Wyss, J.M. (1999) Associational projections of the anterior midline cortex in the rat: intracingulate and retrosplenial connections. Brain Res 825, 1-13.

    PubMed  CAS  Google Scholar 

  • Friedman, H.R. and Goldman-Rakic, P.S. (1994) Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey. J Neurosci 14, 2775-2788.

    PubMed  CAS  Google Scholar 

  • Funahashi, S., Bruce, C.J., and Goldman-Rakic, P.S. (1989) Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61, 331-349.

    PubMed  CAS  Google Scholar 

  • Fuster, J.M. (1973) Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol 36, 61-78.

    PubMed  CAS  Google Scholar 

  • Fuster, J.M. (1997) The Prefrontal Cortex: anatomy, physiology and neuropsychology of the frontal lobe, 3rd ed. Raven Press, New York, NY.

    Google Scholar 

  • Fuster, J.M. and Alexander, G.E. (1971) Neuron activity related to short-term memory. Sci-ence 173, 652-654.

    CAS  Google Scholar 

  • Fuster, J.M., Bodner, M., and Kroger, J.K. (2000) Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405, 347-351.

    PubMed  CAS  Google Scholar 

  • Gabbott, P.L. and Bacon, S.J. (1996) Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics. J Comp Neurol 364, 567-608.

    PubMed  CAS  Google Scholar 

  • Gabbott, P.L., Jays, P.R., and Bacon, S.J. (1997) Calretinin neurons in human medial prefron-tal cortex (areas 24a,b,c, 32', and 25) J Comp Neurol 381, 389-410.

    PubMed  CAS  Google Scholar 

  • Gabbott, P.L., Warner, T.A., Jays, P.R., and Bacon, S.J. (2003) Areal and synaptic intercon-nectivity of prelimbic (area 32), infralimbic (area 25) and insular cortices in the rat. Brain Res 993, 59-71.

    PubMed  CAS  Google Scholar 

  • Gabbott, P.L., Warner, T.A., Jays, P.R., Salway, P., and Busby, S.J. (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492, 145-177.

    PubMed  Google Scholar 

  • Gao, W.J. and Goldman-Rakic, P.S. (2003) Selective modulation of excitatory and inhibitory microcircuits by dopamine. Proc Natl Acad Sci USA 100, 2836-2841.

    PubMed  CAS  Google Scholar 

  • Gao, W.J., Krimer, L.S., and Goldman-Rakic, P.S. (2001) Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. Proc Natl Acad Sci USA 98, 295-300.

    PubMed  CAS  Google Scholar 

  • Gao, W.J., Wang, Y., and Goldman-Rakic, P.S. (2003) Dopamine modulation of perisomatic and peridendritic inhibition in prefrontal cortex. J Neurosci 23, 1622-1630.

    PubMed  CAS  Google Scholar 

  • Garris, P.A., Collins, L.B., Jones, S.R., and Wightman, R.M. (1993) Evoked extracellular dopamine in vivo in the medial prefrontal cortex. J Neurochem 61, 637-647.

    Article  PubMed  CAS  Google Scholar 

  • Gaspar, P., Bloch, B., and Le Moine, C. (1995) D1 and D2 receptor gene expression in the rat frontal cortex: cellular localization in different classes of efferent neurons. Eur J Neurosci 7, 1050-1063.

    PubMed  CAS  Google Scholar 

  • Geijo-Barrientos, E. and Pastore, C. (1995) The effects of dopamine on the subthreshold electrophysiological responses of rat prefrontal cortex neurons in vitro. Eur J Neurosci 7, 358-366.

    PubMed  CAS  Google Scholar 

  • Giguere, M. and Goldman-Rakic, P.S. (1988) Mediodorsal nucleus: areal, laminar, and tan-gential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 277, 195-213.

    PubMed  CAS  Google Scholar 

  • Goldman-Rakic, P.S. (1995) Cellular basis of working memory. Neuron 14, 477-485.

    PubMed  CAS  Google Scholar 

  • Goldman-Rakic, P.S., Leranth, C., Williams, S.M., Mons, N., and Geffard, M. (1989) Dopa-mine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc Natl Acad Sci USA 86, 9015-9019.

    PubMed  CAS  Google Scholar 

  • Goldman-Rakic, P.S., Lidow, M.S., and Gallager, D.W. (1990) Overlap of dopaminergic, adrenergic, and serotoninergic receptors and complementarity of their subtypes in pri-mate prefrontal cortex. J Neurosci 10, 2125-2138.

    PubMed  CAS  Google Scholar 

  • Gonzalez-Burgos, G., Barrionuevo, G., and Lewis, D.A. (2000) Horizontal synaptic connec-tions in monkey prefrontal cortex: an in vitro electrophysiological study. Cereb Cortex 10, 82-92.

    PubMed  CAS  Google Scholar 

  • Gonzalez-Burgos, G., Krimer, L.S., Povysheva, N.V., Barrionuevo, G., and Lewis, D.A. (2005a) Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93, 942-953.

    PubMed  Google Scholar 

  • Gonzalez-Burgos, G., Krimer, L.S., Urban, N.N., Barrionuevo, G., and Lewis, D.A. (2004) Synaptic efficacy during repetitive activation of excitatory inputs in primate dorsolateral prefrontal cortex. Cereb Cortex 14, 530-542.

    PubMed  Google Scholar 

  • Gonzalez-Burgos, G., Kroener, S., Krimer, L.S., Seamans, J.K., Urban, N.N., Henze, D.A., Lewis, D.A., and Barrionuevo, G. (2002) Dopamine modulation of neuronal function in the monkey prefrontal cortex. Physiol Behav 77, 537-543.

    PubMed  CAS  Google Scholar 

  • Gonzalez-Burgos, G., Kroener, S., Seamans, J.K., Lewis, D.A., and Barrionuevo, G. (2005b) Dopaminergic modulation of short-term synaptic plasticity in fast-spiking interneurons of primate dorsolateral prefrontal cortex. J Neurophysiol 94, 4168-4177.

    PubMed  CAS  Google Scholar 

  • Gorelova, N., Seamans, J.K., and Yang, C.R. (2002) Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J Neurophysiol 88, 3150-3166.

    PubMed  CAS  Google Scholar 

  • Gulledge, A.T. and Jaffe, D.B. (2001) Multiple effects of dopamine on layer V pyramidal cell excitability in rat prefrontal cortex. J Neurophysiol 86, 586-595.

    PubMed  CAS  Google Scholar 

  • Gulledge, A.T. and Stuart, G.J. (2003) Action potential initiation and propagation in layer 5 pyramidal neurons of the rat prefrontal cortex: absence of dopamine modulation. J Neu-rosci 23, 11363-11372.

    CAS  Google Scholar 

  • Gulledge, A.T., and Jaffe, D.B. (1998) Dopamine decreases the excitability of layer V pyramidal cells in the rat prefrontal cortex. J Neurosci 18, 9131-9151.

    Google Scholar 

  • Hempel, C.M., Hartman, K.H., Wang, X.J., and Turrigiano, G.G. (2000) Multiple forms of short-term plasticity at excitatory synapses in rat medial prefrontal cortex. J Neurophysiol 83, 3031-3041.

    PubMed  CAS  Google Scholar 

  • Henze, D.A., Gonzalez-Burgos, G.R., Urban, N.N., Lewis, D.A., and Barrionuevo, G. (2000) Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. J Neurophysiol 84, 2799-2809.

    PubMed  CAS  Google Scholar 

  • Howard, A., Tamas, G., and Soltesz, I. (2005) Lighting the chandelier: new vistas for axo-axonic cells. Trends Neurosci 28, 310-316.

    PubMed  CAS  Google Scholar 

  • Inoue, M., Oomura, Y., Aou, S., Nishino, H., and Sikdar, S.K. (1985) Reward related neuronal activity in monkey dorsolateral pre frontal cortex during feeding behavior. Brain Res 326, 307-312.

    PubMed  CAS  Google Scholar 

  • Jacobs, B., Schall, M., Prather, M., Kapler, E., Driscoll, L., Baca, S., Jacobs, J., Ford, K., Wainwright, M., and Treml, M. (2001) Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Cereb Cortex 11, 558-571.

    PubMed  CAS  Google Scholar 

  • Joyce, J.N., Goldsmith, S., and Murray, A. (1993) Neuroanatomical localization of D1 versus D2 receptors: Similar organization in the basal ganglia of the rat, cat and human and dis-parate organization in the cortex and limbic system. In D1:D2 Dopamine Receptor Inter-actions, ed. Waddington, J.L., pp. 23-49. Academic press, London.

    Google Scholar 

  • Jung, M.W., Qin, Y., McNaughton, B.L., and Barnes, C.A. (1998) Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb Cortex 8, 437-450.

    PubMed  CAS  Google Scholar 

  • Kawaguchi, Y. (1995) Physiological subgroups of nonpyramidal cells with specific morpho-logical characteristics in layer II/III of rat frontal cortex. J Neurosci 15, 2638-2655.

    PubMed  CAS  Google Scholar 

  • Kawaguchi, Y. and Kubota, Y. (1997) GABAergic cell subtypes and their synaptic connec-tions in rat frontal cortex. Cereb Cortex 7, 476-486.

    PubMed  CAS  Google Scholar 

  • Kobayashi, S., Nomoto, K., Watanabe, M., Hikosaka, O., Schultz, W., and Sakagami, M. (2006) Influences of rewarding and aversive outcomes on activity in macaque lateral pre-frontal cortex. Neuron 51, 861-870.

    PubMed  CAS  Google Scholar 

  • Krimer, L.S., Jakab, R.L., and Goldman-Rakic, P.S. (1997) Quantitative three-dimensional analysis of the catecholaminergic innervation of identified neurons in the macaque pre-frontal cortex. J Neurosci 17, 7450-7461.

    PubMed  CAS  Google Scholar 

  • Krimer, L.S., Zaitsev, A.V., Czanner, G., Kroener, S., Gonzalez-Burgos, G., Povysheva, N.V., Iyengar, S., Barrionuevo, G., and Lewis, D.A. (2005) Cluster analysis-based physiologi-cal classification and morphological properties of inhibitory neurons in layers 2-3 of monkey dorsolateral prefrontal cortex. J Neurophysiol 94, 3009-3022.

    PubMed  Google Scholar 

  • Kritzer, M.F. and Goldman-Rakic, P.S. (1995) Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey. J Comp Neurol 359, 131-143.

    PubMed  CAS  Google Scholar 

  • Kroener, S., Krimer, L.S., Lewis, D.A., and Barrionuevo, G. (2006) Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modula-tion of interneurons. Cereb Cortex Epub June 13, 2006. doi:10.1093/cercor/bhl012.

    Google Scholar 

  • Kubota, K. and Niki, H. (1971) Prefrontal cortical unit activity and delayed alternation per-formance in monkeys. J Neurophysiol 34, 337-347.

    PubMed  CAS  Google Scholar 

  • Kuroda, M., Yokofujita, J., and Murakami, K. (1998) An ultrastructural study of the neural circuit between the prefrontal cortex and the mediodorsal nucleus of the thalamus. Prog Neurobiol 54, 417-458.

    PubMed  CAS  Google Scholar 

  • Le Moine, C. and Gaspar, P. (1998) Subpopulations of cortical GABAergic interneurons differ by their expression of D1 and D2 dopamine receptor subtypes. Brain Res Mol Brain Res 58, 231-236.

    PubMed  CAS  Google Scholar 

  • Letinic, K., Zoncu, R., and Rakic P. (2002) Origin of GABAergic neurons in the human neo-cortex. Nature 417, 645-649.

    PubMed  CAS  Google Scholar 

  • Levitt, J.B., Lewis, D.A., Yoshioka, T., and Lund, J.S. (1993) Topography of pyramidal neu-ron intrinsic connections in macaque monkey prefrontal cortex (areas 9 and 46) J Comp Neurol 338, 360-376.

    PubMed  CAS  Google Scholar 

  • Lewis, D.A. and Sesack, S.R. (1997) Dopamine systems in the primate brain. In Handbook of Chemical Neuroanatomy, Vol. 13 The Primate Nervous System, eds. Bloom, F.E., Bjork-lund, A., and Hokfelt, T., pp. 263-375. Elsevier, New York.

    Google Scholar 

  • Lewis, D.A., Melchitzky, D.S., Sesack, S.R., Whitehead, R.E., Auh, S., and Sampson, A.R. (2001) Dopamine transporter immunoreactivity in monkey cerebral cortex: regional, laminar, and ultrastructural localization. J Comp Neurol 432, 119-136.

    PubMed  CAS  Google Scholar 

  • Lidow, M.S., Goldman-Rakic, P.S., Gallager, D.W., Rakic P. (1991) Distribution of dopa-minergic receptors in the primate cerebral cortex: quantitative autoradiographic analysis using [3H]raclopride, [3H]spiperone and [3H]SCH23390. Neuroscience 40, 657-671.

    PubMed  CAS  Google Scholar 

  • Lidow, M.S., Wang, F., Cao, Y., and Goldman-Rakic, P.S. (1998) Layer V neurons bear the majority of mRNAs encoding the five distinct dopamine receptor subtypes in the primate prefrontal cortex. Synapse 28, 10-20.

    PubMed  CAS  Google Scholar 

  • Ljungberg, T., Apicella, P., and Schultz, W. (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67, 145-163.

    PubMed  CAS  Google Scholar 

  • Lund, J.S. and Lewis, D.A. (1993) Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328, 282-312.

    PubMed  CAS  Google Scholar 

  • Mainen, Z.F., Joerges, J., Huguenard, J.R., and Sejnowski, T.J. (1995) A model of spike initia-tion in neocortical pyramidal neurons. Neuron 15, 1427-1439.

    PubMed  CAS  Google Scholar 

  • Melchitzky, D.S., Sesack, S.R., Pucak, M.L., and Lewis, D.A. (1998) Synaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cor-tex. J Comp Neurol 390, 221-224.

    Google Scholar 

  • Miller, E.K., Erickson, C.A., and Desimone, R. (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16, 5154-5167.

    PubMed  CAS  Google Scholar 

  • Missale, C., Nass, S.R., Robinson, S.W., Jaber, M., and Caron, M.G. (1998) Dopamine recep-tors: From structure to function. Physiol Rev 78, 189-225.

    PubMed  CAS  Google Scholar 

  • Mrzljak, L., Bergson, C., Pappy, M., Huff, R., Levenson, R., and Goldman-Rakic, P.S. (1996) Localization of dopamine D4 receptors in GABAergic neurons of the primate brain. Nature 381, 245-248.

    PubMed  CAS  Google Scholar 

  • Muly, E.C., Szigeti, K., and Goldman-Rakic, P.S. (1998) D1 receptor in interneurons of ma-caque prefrontal cortex: distribution and subcellular localization. J Neurosci 18, 10553-10565.

    PubMed  CAS  Google Scholar 

  • Mushiake, H., Saito, N., Sakamoto, K., Itoyama, Y., and Tanji, J. (2006) Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans. Neuron 50, 631-641.

    PubMed  CAS  Google Scholar 

  • Orlov, A.A., Kurzina, N.P., and Shutov, A.P. (1988) Activity of medial wall neurons in frontal cortex of rat brain during delayed response reactions. Neurosci and Behav Physiol 18, 31-37.

    CAS  Google Scholar 

  • Pandya, D.N. and Yeterian, E.H. (1990) Prefrontal cortex in relation to other cortical areas in rhesus monkey: architecture and connections. Prog Brain Res 85, 63-94.

    PubMed  CAS  Google Scholar 

  • Parent, A. and Hazrati, L.N. (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo -cortical loop. Brain Res Brain Res Rev 20, 91-127.

    PubMed  CAS  Google Scholar 

  • Paspalas, C.D. and Goldman-Rakic, P.S. (2004) Microdomains for dopamine volume neuro-transmission in primate prefrontal cortex. J Neurosci 24, 5292-5300.

    PubMed  CAS  Google Scholar 

  • Paspalas, C.D. and Goldman-Rakic, P.S. (2005) Presynaptic D1 dopamine receptors in pri-mate prefrontal cortex: target-specific expression in the glutamatergic synapse. J Neuro-sci 25, 1260-1267.

    CAS  Google Scholar 

  • Petrides, M. (2000) Impairments in working memory after frontal cortical excisions. Adv Neurol 84, 111-118.

    PubMed  CAS  Google Scholar 

  • Petrides, M. and Pandya, D.N. (1999) Dorsolateral prefrontal cortex: comparative cytoarchi-tectonic analysis in the human and the macaque brain and corticocortical connection pat-terns. Eur J Neurosci 11, 1011-1036.

    PubMed  CAS  Google Scholar 

  • Povysheva, N.V., Gonzalez-Burgos, G., Zaitsev, A.V., Kroener, S., Barrionuevo, G., Lewis, D.A., and Krimer, L.S. (2006) Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cereb Cortex 16, 541-552.

    PubMed  CAS  Google Scholar 

  • Povysheva, N.V., Zaitsev, A.V., Kroener, S., Krimer, O.A., Rotaru, D.C., Gonzalez-Burgos, G., Lewis, D.A., and Krimer, L.S. (2007) Electrophysiological differences between neu-rogliaform cells from monkey and rat prefrontal cortex. J Neurophysiol 97(2): 1030-9.

    PubMed  CAS  Google Scholar 

  • Pratt, W.E. and Mizumori, S.J. (2001) Neurons in rat medial prefrontal cortex show anticipa-tory rate changes to predictable differential rewards in a spatial memory task. Behav Brain Res 123, 165-183.

    PubMed  CAS  Google Scholar 

  • Preuss, T.M. (1995) Do rats have prefrontal cortex? The Rose-Woolsey-Akert program recon-sidered. J Cog Neurosci 7, 1-24.

    Google Scholar 

  • Pucak, M.L., Levitt, J.B., Lund, J.S., and Lewis, D.A. (1996) Patterns of intrinsic and associa-tional circuitry in monkey prefrontal cortex. J Comp Neurol 376, 614-630.

    PubMed  CAS  Google Scholar 

  • Quintana, J. and Fuster, J.M. (1999) From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cereb Cortex 9, 213-221.

    PubMed  CAS  Google Scholar 

  • Quintana, J., Yajeya, J., and Fuster, J.M. (1988) Prefrontal representation of stimulus attrib-utes during delay tasks. I. Unit activity in cross-temporal integration of sensory and sensory-motor information. Brain Res 474, 211-221.

    PubMed  CAS  Google Scholar 

  • Rainer, G. and Miller, E.K. (2002) Timecourse of object-related neural activity in the primate prefrontal cortex during a short-term memory task. Eur J Neurosci 15, 1244-1254.

    PubMed  Google Scholar 

  • Rainer, G., Asaad, W.F., and Miller, E.K. (1998) Memory fields of neurons in the primate prefrontal cortex. Proc Natl Acad Sci USA 95, 15008-15013.

    PubMed  CAS  Google Scholar 

  • Rainer, G., Rao, S.C., and Miller, E.K. (1999) Prospective coding for objects in primate pre-frontal cortex. J Neurosci 19, 5493-5505.

    PubMed  CAS  Google Scholar 

  • Rao, S.C., Rainer, G., and Miller, E.K. (1997) Integration of what and where in the primate prefrontal cortex. Science 276, 821-824.

    PubMed  CAS  Google Scholar 

  • Rao, S.G., Williams, G.V., and Goldman-Rakic, P.S. (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81, 1903-1916.

    PubMed  CAS  Google Scholar 

  • Repovs, G. and Baddeley, A. (2006) The multi-component model of working memory: explo-rations in experimental cognitive psychology. Neuroscience 139, 5-21.

    PubMed  CAS  Google Scholar 

  • Roesch, M.R. and Olson, C.R. (2003) Impact of expected reward on neuronal activity in pre-frontal cortex, frontal and supplementary eye fields and premotor cortex. J Neurophysiol 90, 1766-1789.

    PubMed  Google Scholar 

  • Romo, R., Brody, C.D., Hernandez, A., and Lemus, L. (1999) Neuronal correlates of para-metric working memory in the prefrontal cortex. Nature 399, 470-473.

    PubMed  CAS  Google Scholar 

  • Rotaru, D.C., Barrionuevo, G., and Sesack, S.R. (2005) Mediodorsal thalamic afferents to layer III of the rat prefrontal cortex: synaptic relationships to subclasses of interneurons. J Comp Neurol 490, 220-238.

    PubMed  Google Scholar 

  • Salamone, J.D., Correa, M., Mingote, S.M., and Weber, S.M. (2005) Beyond the reward hy-pothesis: alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5, 34-41.

    PubMed  CAS  Google Scholar 

  • Sawaguchi, T. (2001) The effects of dopamine and its antagonists on directional delay-period activity of prefrontal neurons in monkeys during an oculomotor delayed-response task. Neurosci Res 41, 115-128.

    PubMed  CAS  Google Scholar 

  • Sawaguchi, T. and Goldman-Rakic, P.S. (1991) D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 251, 947-950.

    PubMed  CAS  Google Scholar 

  • Schultz, W. (1997) Dopamine neurons and their role in reward mechanisms. Curr Opin Neurobiol 7, 191-197.

    PubMed  CAS  Google Scholar 

  • Schultz, W. and Romo, R. (1990) Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. J Neurophysiol 63, 607-624.

    PubMed  CAS  Google Scholar 

  • Seamans, J.K. and Yang, C.R. (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74, 1-58.

    PubMed  CAS  Google Scholar 

  • Seamans, J.K., Durstewitz, D., Christie, B., Stevens, C.F., and Sejnowski, T.J. (2001a) Dopa-mine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cor-tex neurons. Proc Natl Acad Sci USA 98, 301-306.

    PubMed  CAS  Google Scholar 

  • Seamans, J.K., Gorelova, N., Durstewitz, D., and Yang, C.R. (2001b) Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21, 3628-3638.

    PubMed  CAS  Google Scholar 

  • Seamans, J.K., Nogueira, L., and Lavin, A. (2003) Synaptic basis of persistent activity in prefrontal cortex in vivo and in organotypic cultures. Cereb Cortex 13, 1242-1250.

    PubMed  Google Scholar 

  • Seguela, P., Watkins, K.C., and Descarries, L. (1988) Ultrastructural features of dopamine axon terminals in the anteromedial and the suprarhinal cortex of adult rat. Brain Res 442, 11-22.

    PubMed  CAS  Google Scholar 

  • Sesack, S.R., Hawrylak, V.A., Matus, C., Guido, M.A., and Levey, A.I. (1998a) Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 18, 2697-2708.

    PubMed  CAS  Google Scholar 

  • Sesack, S.R., Hawrylak, V.A., Melchitzky, D.S., and Lewis, D.A. (1998b) Dopamine innerva-tion of a subclass of local circuit neurons in monkey prefrontal cortex: ultrastructural analysis of tyrosine hydroxylase and parvalbumin immunoreactive structures. Cereb Cortex 8, 614-622.

    PubMed  CAS  Google Scholar 

  • Shallice, T. and Burgess, P. (1996) The domain of supervisory processes and temporal organi-zation of behaviour. Philos Trans R Soc Lond B Biol Sci 351, 1405-1411.

    PubMed  CAS  Google Scholar 

  • Smiley, J.F. and Goldman-Rakic, P.S. (1993) Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. Cereb Cortex 3, 223-238.

    PubMed  CAS  Google Scholar 

  • Smiley, J.F., Levey, A.I., Ciliax, B.J., and Goldman-Rakic, P.S. (1994) D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. Proc Natl Acad Sci USA 91, 5720-5724.

    PubMed  CAS  Google Scholar 

  • Soloway, A.S., Pucak, M.L., Melchitzky, D.S., and Lewis, D.A. (2002) Dendritic morphology of callosal and ipsilateral projection neurons in monkey prefrontal cortex. Neuroscience 109, 461-471.

    PubMed  CAS  Google Scholar 

  • Somogyi, P., Kisvarday, Z.F., Freund, T.F., and Cowey, A. (1984) Characterization by Golgi impregnation of neurons that accumulate 3H-GABA in the visual cortex of monkey. Exp Brain Res 53, 295-303.

    PubMed  CAS  Google Scholar 

  • Steriade, M. (2001) Impact of network activities on neuronal properties in corticothalamic systems. J Neurophysiol 86, 1-39.

    PubMed  CAS  Google Scholar 

  • Trantham-Davidson, H., Neely, L.C., Lavin, A., and Seamans, J.K. (2004) Mechanisms under-lying differential D1 versus D2 dopamine receptor regulation of inhibition in prefrontal cortex. J Neurosci 24, 10652-10659.

    PubMed  CAS  Google Scholar 

  • Tseng, K.Y. and O’Donnell, P. (2006) Dopamine modulation of prefrontal cortical interneu-rons changes during adolescence. Cereb Cortex 17 (5): 1235-40.

    PubMed  Google Scholar 

  • Tsujimoto, S. and Sawaguchi, T. (2005) Neuronal activity representing temporal prediction of reward in the primate prefrontal cortex. J Neurophysiol 93, 3687-3692.

    PubMed  Google Scholar 

  • Urban, N.N., Gonzalez-Burgos, G., Henze, D.A., Lewis, D.A., and Barrionuevo, G. (2002) Selective reduction by dopamine of excitatory synaptic inputs to pyramidal neurons in primate prefrontal cortex. J Physiol 539, 707-712.

    PubMed  CAS  Google Scholar 

  • Uylings, H.B., Groenewegen, H.J., and Kolb, B. (2003) Do rats have a prefrontal cortex? Behav Brain Res 146, 3-17.

    PubMed  Google Scholar 

  • van Eden, C.G., Hoorneman, E.M., Buijs, R.M., Matthijssen, M.A., Geffard, M., and Uylings, H.B. (1987) Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light and electron microscopical level. Neuroscience 22, 849-862.

    PubMed  CAS  Google Scholar 

  • van Eden, C.G., Lamme, V.A., and Uylings, H.B. (1992) Heterotopic cortical afferents to the medial prefrontal cortex in the rat. A combined retrograde and anterograde tracer study. Eur J Neurosci 4, 77-97.

    PubMed  Google Scholar 

  • Vincent, S.L., Khan, Y., and Benes, F.M. (1993) Cellular distribution of dopamine D1 and D2 receptors in rat medial prefrontal cortex. J Neurosci 13, 2551-2564.

    PubMed  CAS  Google Scholar 

  • Vysokanov, A., Flores-Hernandez, J., and Surmeier, D.J. (1998) mRNAs for clozapine-sensitive receptors co-localize in rat prefrontal cortex neurons. Neurosci Lett 258, 179-182.

    PubMed  CAS  Google Scholar 

  • Wallis, J.D. and Miller, E.K. (2003) Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 18, 2069-2081.

    PubMed  Google Scholar 

  • Wang, Y., Markram, H., Goodman, P.H., Berger, T.K., Ma, J., and Goldman-Rakic, P.S. (2006) Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neu-rosci 9, 534-542.

    CAS  Google Scholar 

  • Watanabe, M. (1990) Prefrontal unit activity during associative learning in the monkey. Exp Brain Res 80, 296-309.

    PubMed  CAS  Google Scholar 

  • Watanabe, M. (1996) Reward expectancy in primate prefrontal neurons. Nature 382, 629-632.

    PubMed  CAS  Google Scholar 

  • Watanabe, M., Hikosaka, K., Sakagami, M., and Shirakawa, S. (2002) Coding and monitoring of motivational context in the primate prefrontal cortex. J Neurosci 22, 2391-2400.

    PubMed  CAS  Google Scholar 

  • Watanabe, M., Hikosaka, K., Sakagami, M., and Shirakawa, S. (2005) Functional significance of delay-period activity of primate prefrontal neurons in relation to spatial working mem-ory and reward/omission-of-reward expectancy. Exp Brain Res 166, 263-276.

    PubMed  Google Scholar 

  • Waters, J. and Helmchen, F. (2006) Background synaptic activity is sparse in neocortex. J Neurosci 26, 8267-8277.

    PubMed  CAS  Google Scholar 

  • Wayment, H.K., Schenk, J.O., and Sorg, B.A. (2001) Characterization of extracellular dopa-mine clearance in the medial prefrontal cortex: role of monoamine uptake and monoam-ine oxidase inhibition. J Neurosci 21, 35-44.

    PubMed  CAS  Google Scholar 

  • Williams, G.V. and Goldman-Rakic, P.S. (1995) Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376, 572-575.

    PubMed  CAS  Google Scholar 

  • Williams, S.M. and Goldman-Rakic, P.S. (1998) Widespread origin of the primate mesofron-tal dopamine system. Cereb Cortex 8, 321-345.

    PubMed  CAS  Google Scholar 

  • Wilson, F.A., O'Scalaidhe, S.P., and Goldman-Rakic, P.S. (1994) Functional synergism between putative gamma-aminobutyrate- containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci USA 91, 4009-4013.

    PubMed  CAS  Google Scholar 

  • Xu, Q., Cobos, I., De La, C.E., Rubenstein, J.L., and Anderson, S.A. (2004) Origins of corti-cal interneuron subtypes. J Neurosci 24, 2612-2622.

    PubMed  CAS  Google Scholar 

  • Yajeya, J., Quintana, J., and Fuster, J.M. (1988) Prefrontal representation of stimulus attrib-utes during delay tasks. II. The role of behavioral significance. Brain Res 474, 222-230.

    PubMed  CAS  Google Scholar 

  • Yanez, I.B., Munoz, A., Contreras, J., Gonzalez, J., Rodriguez-Veiga, E., and DeFelipe, J. (2005) Double bouquet cell in the human cerebral cortex and a comparison with other mammals. J Comp Neurol 486, 344-360.

    PubMed  Google Scholar 

  • Yang, C.R. and Seamans, J.K. (1996) Dopamine D1 receptor actions in layers V-VI rat pre-frontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J Neu-rosci 16, 1922-1935.

    CAS  Google Scholar 

  • Yang, C.R., Seamans, J.K., and Gorelova, N. (1996) Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro. J Neu-rosci 16, 1904-1921.

    CAS  Google Scholar 

  • Zaitsev, A.V., Gonzalez-Burgos, G., Povysheva, N.V., Kroener, S., Lewis, D.A., and Krimer, L.S. (2005) Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex 15, 1178-1186.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Gonzalez-Burgos, G., Kröner, S., Seamans, J.K. (2007). Cellular Mechanisms of Working Memory and its Modulation by Dopamine in the Prefrontal Cortex of Primates and Rats. In: Tseng, KY., Atzori, M. (eds) Monoaminergic Modulation of Cortical Excitability. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-72256-6_8

Download citation

Publish with us

Policies and ethics