Specificity in the functional architecture of primate prefrontal cortex

Multiple lines of evidence indicate that the performance of complex cognitive processes, such as those involving working memory, depend upon the functional properties of the circuitry of the prefrontal cortex (PFC). In primates, working memory has been proposed to be dependent upon the sustained activity of specific populations of PFC pyramidal cells, with this activity regulated by certain types of GABAergic interneurons. Thus, knowledge of the connectivity between PFC pyramidal cells and interneurons is crucial to the understanding the neural mechanisms that subserve working memory. This paper reviews recent findings that reveal specificity in the spatial organization, synaptic targets and postnatal development of pyramidal cells and interneurons in the primate prefrontal cortex, and considers the relevance of these findings for the neural circuitry that subserves working memory.

[1]  J. Lund,et al.  Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics , 1993, The Journal of comparative neurology.

[2]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[3]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[4]  J. DeFelipe Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex , 1997, Journal of Chemical Neuroanatomy.

[5]  German Barrionuevo,et al.  Synaptic targets of the intrinsic axon collaterals of supragranular pyramidal neurons in monkey prefrontal cortex , 2001, The Journal of comparative neurology.

[6]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[7]  V. Meskenaite,et al.  Calretinin‐immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis , 1997, The Journal of comparative neurology.

[8]  D. Lewis,et al.  The functional architecture of the prefrontal cortex and schizophrenia , 1995, Psychological Medicine.

[9]  P. Goldman-Rakic,et al.  Prefrontal Microcircuits: Membrane Properties and Excitatory Input of Local, Medium, and Wide Arbor Interneurons , 2001, The Journal of Neuroscience.

[10]  P. Goldman-Rakic,et al.  A role for inhibition in shaping the temporal flow of information in prefrontal cortex , 2002, Nature Neuroscience.

[11]  S. Funahashi,et al.  Working memory and prefrontal cortex , 1994, Neuroscience Research.

[12]  D. Lewis,et al.  Postnatal development of parvalbumin‐ and GABA transporter‐immunoreactive axon terminals in monkey prefrontal cortex , 2002, The Journal of comparative neurology.

[13]  J. Fuster,et al.  Mnemonic neuronal activity in somatosensory cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Boris S. Gutkin,et al.  Turning On and Off with Excitation: The Role of Spike-Timing Asynchrony and Synchrony in Sustained Neural Activity , 2001, Journal of Computational Neuroscience.

[15]  J. Fuster,et al.  Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. , 1981, Science.

[16]  S. Sesack,et al.  Dopamine innervation of a subclass of local circuit neurons in monkey prefrontal cortex: ultrastructural analysis of tyrosine hydroxylase and parvalbumin immunoreactive structures. , 1998, Cerebral cortex.

[17]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[18]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[19]  P S Goldman-Rakic,et al.  Synaptogenesis in the prefrontal cortex of rhesus monkeys. , 1994, Cerebral cortex.

[20]  James K. Kroger,et al.  Cross-modal and cross-temporal association in neurons of frontal cortex , 2000, Nature.

[21]  D. Pandya,et al.  Prefrontal cortex in relation to other cortical areas in rhesus monkey: architecture and connections. , 1990, Progress in brain research.

[22]  P. Goldman-Rakic,et al.  Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey , 1995, The Journal of comparative neurology.

[23]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[25]  Paul Leonard Gabbott,et al.  Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics , 1996, The Journal of comparative neurology.

[26]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[27]  D. Lewis,et al.  Parvalbumin‐immunoreactive axon terminals in macaque monkey and human prefrontal cortex: Laminar, regional, and target specificity of type I and type II synapses , 1999, The Journal of comparative neurology.

[28]  C. Gilbert Adult cortical dynamics. , 1998, Physiological reviews.

[29]  K. Martin,et al.  Termination of the geniculocortical projection in the striate cortex of macaque monkey: A quantitative immunoelectron microscopic study , 2000, The Journal of comparative neurology.

[30]  A. Sampson,et al.  Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. , 2001, Archives of general psychiatry.

[31]  D. Fitzpatrick,et al.  Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns , 1995, Neuron.

[32]  Françoise Condé,et al.  Local circuit neurons immunoreactive for calretinin, calbindin D‐28k or parvalbumin in monkey prefronatal cortex: Distribution and morphology , 1994, The Journal of comparative neurology.

[33]  A. Diamond Normal development of prefrontal cortex from birth to young adulthood: Cognitive functions, anatomy, and biochemistry. , 2002 .

[34]  J. B. Levitt,et al.  Patterns of intrinsic and associational circuitry in monkey prefrontal cortex , 1996, The Journal of comparative neurology.

[35]  Y. Kubota,et al.  GABAergic cell subtypes and their synaptic connections in rat frontal cortex. , 1997, Cerebral cortex.

[36]  D. Schmechel,et al.  Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory‐motor cortex , 1985, The Journal of comparative neurology.

[37]  P. Goldman-Rakic,et al.  Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[39]  P. Goldman-Rakic,et al.  Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. , 1999, Journal of neurophysiology.

[40]  T. Woo,et al.  A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[42]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[43]  P. Somogyi,et al.  Glutamate decarboxylase‐immunoreactive terminals of Golgi‐impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex , 1983, The Journal of comparative neurology.

[44]  M. L. Pucak,et al.  Synaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cortex , 1998, The Journal of comparative neurology.

[45]  S. Sesack,et al.  Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA‐immunoreactive dendrites in rat and monkey cortex , 1995, The Journal of comparative neurology.

[46]  P. Goldman-Rakic,et al.  Destruction and Creation of Spatial Tuning by Disinhibition: GABAA Blockade of Prefrontal Cortical Neurons Engaged by Working Memory , 2000, The Journal of Neuroscience.

[47]  M. Weliky,et al.  Functional mapping of horizontal connections in developing ferret visual cortex: experiments and modeling , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  P. Goldman-Rakic,et al.  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. , 1993, Cerebral cortex.

[49]  D. Lewis,et al.  Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. , 2000, Cerebral cortex.

[50]  S. Sesack,et al.  Ultrastructural associations between dopamine terminals and local circuit neurons in the monkey prefrontal cortex: a study of calretinin-immunoreactive cells , 1995, Neuroscience Letters.

[51]  P. Goldman-Rakic,et al.  The synaptology of parvalbumin‐immunoreactive neurons in the primate prefrontal cortex , 1992, The Journal of comparative neurology.

[52]  David A Lewis,et al.  Intrinsic excitatory connections in the prefrontal cortex and the pathophysiology of schizophrenia , 2000, Brain Research Bulletin.

[53]  M. L. Pucak,et al.  Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex , 1997, Neuroscience.

[54]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

[55]  D. Lewis,et al.  Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. , 2000, Archives of general psychiatry.

[56]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[57]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  P. Goldman-Rakic Working memory dysfunction in schizophrenia. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[59]  J. S. Lund,et al.  Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex , 1995, Neuroscience.

[60]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.

[61]  A. Sampson,et al.  Reciprocal alterations in pre- and postsynaptic inhibitory markers at chandelier cell inputs to pyramidal neurons in schizophrenia. , 2002, Cerebral cortex.

[62]  E. Callaway,et al.  Cytochrome-oxidase blobs and intrinsic horizontal connections of layer 2/3 pyramidal neurons in primate V1 , 1998, Visual Neuroscience.

[63]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[64]  J. B. Levitt,et al.  Topography of pyramidal neuron intrinsic connections in macaque monkey prefrontal cortex (areas 9 and 46) , 1993, The Journal of comparative neurology.

[65]  T. Sawaguchi,et al.  Catecholaminergic effects on neuronal activity related to a delayed response task in monkey prefrontal cortex. , 1990, Journal of neurophysiology.

[66]  David A Lewis,et al.  Pyramidal neuron local axon terminals in monkey prefrontal cortex: differential targeting of subclasses of GABA neurons. , 2003, Cerebral cortex.