Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC.

Studies on the cellular mechanisms of working memory demonstrated that neurons in dorsolateral prefrontal cortex (dPFC) exhibit directionally tuned activity during an oculomotor delayed response. To determine the particular contributions of pyramidal cells and interneurons to spatial tuning in dPFC, we examined both individually and in pairs the tuning properties of regular-spiking (RS) and fast-spiking (FS) units that represent putative pyramidal cells and interneurons, respectively. Our main finding is that FS units possess spatially tuned sensory, motor, and delay activity (i. e., "memory fields") similar to those found in RS units. Furthermore, when recorded simultaneously at the same site, the majority of neighboring neurons, whether FS or RS, displayed isodirectional tuning, i.e., they shared very similar tuning angles for the sensory and delay phases of the task. As the trial entered the response phase of the task, many FS units shifted their direction of tuning and became cross-directional to adjacent RS units by the end of the trial. These results establish that a large part of inhibition in prefrontal cortex is spatially oriented rather than being untuned and simply regulating the threshold response of pyramidal cell output. Moreover, the isodirectional tuning between adjacent neurons supports a functional microcolumnar organization in dPFC for spatial memory fields similar to that found in other areas of cortex for sensory receptive fields.

[1]  A. Hodgkin Evidence for electrical transmission in nerve , 1937, The Journal of physiology.

[2]  H. Brooks,et al.  Medical physiology , 1961 .

[3]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[4]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[5]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[6]  Joan Welkowitz,et al.  Introductory Statistics for the Behavioral Sciences , 1971 .

[7]  W. J. Conover,et al.  Practical Nonparametric Statistics , 1972 .

[8]  References , 1971 .

[9]  H. L. Bryant,et al.  Correlations of neuronal spike discharges produced by monosynaptic connections and by common inputs. , 1973, Journal of neurophysiology.

[10]  John Cotton Introductory statistics for the behavioral sciences. 2nd ed. , 1976 .

[11]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[12]  W. Nauta,et al.  Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey , 1977, Brain Research.

[13]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[14]  D. Simons Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[15]  M. Armstrong‐James,et al.  Carbon fibre microelectrodes , 1979, Journal of Neuroscience Methods.

[16]  M. Armstrong‐James,et al.  The electrical characteristics of carbon fibre microelectrodes , 1980, Journal of Neuroscience Methods.

[17]  G. Leichnetz,et al.  An intrahemispheric columnar projection between two cortical multisensory convergence areas (inferior parietal lobule and prefrontal cortex): An anterograde study in macaque using HRP gel , 1980, Neuroscience Letters.

[18]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  P. Goldman-Rakic,et al.  Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. , 1982, Science.

[20]  M. Armstrong‐James,et al.  Effects of ionophoresed noradrenaline on the spontaneous activity of neurones in rat primary somatosensory cortex. , 1983, The Journal of physiology.

[21]  A. Sillito Functional Considerations of the Operation of GABAergic Inhibitory Processes in the Visual Cortex , 1984 .

[22]  A. Aertsen,et al.  Evaluation of neuronal connectivity: Sensitivity of cross-correlation , 1985, Brain Research.

[23]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[24]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[25]  D. Ferster Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  A. Peters,et al.  The neuronal composition of area 17 of rat visual cortex. IV. The organization of pyramidal cells , 1987, The Journal of comparative neurology.

[27]  E E Fetz,et al.  Cross‐correlation assessment of synaptic strength of single Ia fibre connections with triceps surae motoneurones in cats. , 1987, The Journal of physiology.

[28]  ML Schwartz,et al.  Periodicity of GABA-containing cells in primate prefrontal cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  K. Martin,et al.  The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. , 1988, Quarterly journal of experimental physiology.

[30]  H. Tamura,et al.  Inhibition contributes to orientation selectivity in visual cortex of cat , 1988, Nature.

[31]  J. T. Massey,et al.  Mental rotation of the neuronal population vector. , 1989, Science.

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

[33]  A. B. Bonds Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex , 1989, Visual Neuroscience.

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

[35]  E. G. Jones,et al.  A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons , 1990, Neuroscience.

[36]  R. Matthews,et al.  A comparison of extracellular and intracellular recordings from medial septum/diagonal band neurons in vitro , 1991, Neuroscience.

[37]  E Ahissar,et al.  Neural interactions in the frontal cortex of a behaving monkey: signs of dependence on stimulus context and behavioral state. , 1991, Journal fur Hirnforschung.

[38]  P. Goldman-Rakic,et al.  Interhemispheric integration: I. Symmetry and convergence of the corticocortical connections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) in the rhesus monkey. , 1991, Cerebral cortex.

[39]  P. Goldman-Rakic,et al.  Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. , 1991, Cerebral cortex.

[40]  P. Goldman-Rakic,et al.  Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. , 1991, Journal of neurophysiology.

[41]  C. Koch,et al.  A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[43]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[44]  P. Goldman-Rakic,et al.  Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task , 1993, Nature.

[45]  T. Bonhoeffer,et al.  Relationship Between Lateral Inhibitory Connections and the Topography of the Orientation Map in Cat Visual Cortex , 1994, The European journal of neuroscience.

[46]  P. Goldman-Rakic,et al.  The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. , 1994, Journal of neurophysiology.

[47]  P S Goldman-Rakic,et al.  Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[49]  Y. Kawaguchi Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  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.

[51]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[53]  H. Swadlow,et al.  Influence of VPM afferents on putative inhibitory interneurons in S1 of the awake rabbit: evidence from cross-correlation, microstimulation, and latencies to peripheral sensory stimulation. , 1995, Journal of neurophysiology.

[54]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[55]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[56]  Paul Leonard Gabbott,et al.  Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions , 1996, The Journal of comparative neurology.

[57]  D J Simons,et al.  Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels. , 1996, Journal of neurophysiology.

[58]  D J Simons,et al.  Spatial gradients and inhibitory summation in the rat whisker barrel system. , 1996, Journal of neurophysiology.

[59]  E. Fetz,et al.  Synaptic Interactions between Primate Precentral Cortex Neurons Revealed by Spike-Triggered Averaging of Intracellular Membrane Potentials In Vivo , 1996, The Journal of Neuroscience.

[60]  Larry E. Toothaker,et al.  Introductory statistics for the behavioral sciences, 2nd ed. , 1996 .

[61]  J Deuchars,et al.  Neocortical local synaptic circuitry revealed with dual intracellular recordings and biocytin-filling , 1996, Journal of Physiology-Paris.

[62]  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.

[63]  U. Eysel,et al.  GABA-induced inactivation of functionally characterized sites in cat striate cortex: Effects on orientation tuning and direction selectivity , 1997, Visual Neuroscience.

[64]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[65]  J. Deuchars,et al.  Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. , 1997, Cerebral cortex.

[66]  Dario L. Ringach,et al.  Dynamics of orientation tuning in macaque primary visual cortex , 1997, Nature.

[67]  M. Sirota,et al.  Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. , 1998, Journal of neurophysiology.

[68]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[69]  David J. Groggel,et al.  Practical Nonparametric Statistics , 2000, Technometrics.

[70]  J. Bullier,et al.  Cross-Correlograms for Neuronal Spike Trains. Different Types of Temporal Correlation in Neocortex, their Origin and Significance , 2000 .