Functional properties of putative pyramidal neurons and inhibitory interneurons in the rat gustatory cortex.

In order to address how taste information is modulated by inhibitory neuronal interactions in the rat gustatory cortex, we examined putative pyramidal neurons (PY units) and putative inhibitory interneurons (fast spiking [FS] units) that were distinguished by their spike waveforms and discharge rates. FS units were strikingly different from PY units in that the majority of FS units were N- or NH-best neurons and narrowly tuned to 1 or 2 tastant(s), whereas PY units were broadly tuned to plural tastants. Compared with PY units, FS units were characterized by a shorter response latency and/or a longer response duration. These results suggest that inhibitory modulations in the gustatory cortex are carried out in a taste specific and tonic manner. Sensitivity to tastant concentrations in PY units was similar to that in FS units for NaCl but higher for HCl. FS units may act to enhance concentration sensitivity in PY units by reducing PY units' response activity. High density of FS and PY units was observed in the superficial and middle layers (mainly layers III and IV). Responses in N-best FS units in these layers were significantly larger than those in the deep layers, suggesting the existence of layer-specific inhibitory interactions.

[1]  Zoltan Nusser,et al.  Cell-Type-Dependent Molecular Composition of the Axon Initial Segment , 2008, The Journal of Neuroscience.

[2]  A. Carleton,et al.  Internal body state influences topographical plasticity of sensory representations in the rat gustatory cortex , 2008, Proceedings of the National Academy of Sciences.

[3]  Jude F. Mitchell,et al.  Differential Attention-Dependent Response Modulation across Cell Classes in Macaque Visual Area V4 , 2007, Neuron.

[4]  Y. Dudai,et al.  Role of cortical cannabinoid CB1 receptor in conditioned taste aversion memory , 2007, The European journal of neuroscience.

[5]  K. Eguchi,et al.  Differential taste coding of salt and acid by correlative activities between taste-sensitive neuron types in rat gustatory cortex , 2007, Neuroscience.

[6]  A. Zaitsev,et al.  Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. , 2006, Cerebral cortex.

[7]  Ken Mackie,et al.  Endocannabinoid Signaling in Rat Somatosensory Cortex: Laminar Differences and Involvement of Specific Interneuron Types , 2005, The Journal of Neuroscience.

[8]  Bruce L. McNaughton,et al.  Differential Encoding of Behavior and Spatial Context in Deep and Superficial Layers of the Neocortex , 2005, Neuron.

[9]  G. Buzsáki,et al.  Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. , 2004, Journal of neurophysiology.

[10]  David A Lewis,et al.  Synaptic efficacy during repetitive activation of excitatory inputs in primate dorsolateral prefrontal cortex. , 2004, Cerebral cortex.

[11]  Jose-Manuel Alonso,et al.  Functionally distinct inhibitory neurons at the first stage of visual cortical processing , 2003, Nature Neuroscience.

[12]  Randy M Bruno,et al.  Feedforward Mechanisms of Excitatory and Inhibitory Cortical Receptive Fields , 2002, The Journal of Neuroscience.

[13]  P. Goldman-Rakic,et al.  Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. , 2002, Journal of neurophysiology.

[14]  Emery N. Brown,et al.  A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. , 2001, Journal of neurophysiology.

[15]  T. Satoh,et al.  Three-dimensional estimation of the distribution and size of putative functional units in rat gustatory cortex as assessed from the inter-neuronal distance between two neurons with correlative activity , 2001, Brain Research Bulletin.

[16]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.

[17]  M. Uemura,et al.  An anterograde and retrograde tract-tracing study on the projections from the thalamic gustatory area in the rat: distribution of neurons projecting to the insular cortex and amygdaloid complex , 2000, Neuroscience Research.

[18]  M. Cassell,et al.  Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices , 1998, The Journal of comparative neurology.

[19]  H. Ogawa,et al.  GABAergic inhibition and modifications of taste responses in the cortical taste area in rats , 1998, Neuroscience Research.

[20]  J. Csicsvari,et al.  Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus an Ensemble Approach in the Behaving Rat , 1998, Neuron.

[21]  D. Smith,et al.  Tonic GABAergic inhibition of taste-responsive neurons in the nucleus of the solitary tract. , 1998, Chemical senses.

[22]  Y. Yasoshima,et al.  Short-term and long-term excitability changes of the insular cortical neurons after the acquisition of taste aversion learning in behaving rats , 1998, Neuroscience.

[23]  C. Gray,et al.  Physiological properties of inhibitory interneurons in cat striate cortex. , 1997, Cerebral cortex.

[24]  M. C. Angulo,et al.  Molecular and Physiological Diversity of Cortical Nonpyramidal Cells , 1997, The Journal of Neuroscience.

[25]  J. Winer,et al.  Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI) , 1994, The Journal of comparative neurology.

[26]  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.

[27]  Y. Kawaguchi,et al.  Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. , 1993, Journal of neurophysiology.

[28]  H. Ogawa,et al.  Difference in taste quality coding between two cortical taste areas, granular and dysgranular insular areas, in rats , 1992, Experimental Brain Research.

[29]  C. Saper,et al.  Organization of visceral and limbic connections in the insular cortex of the rat , 1991, The Journal of comparative neurology.

[30]  H. Voigt,et al.  Cross-correlation analysis of inhibitory interactions in dorsal cochlear nucleus. , 1990, Journal of neurophysiology.

[31]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[32]  Clemens Forster,et al.  Automatic classification and analysis of microneurographic spike data using a PC/AT , 1990, Journal of Neuroscience Methods.

[33]  T. Yamamoto,et al.  Taste responses of cortical neurons in freely ingesting rats. , 1989, Journal of neurophysiology.

[34]  C. Saper,et al.  Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat , 1987, The Journal of comparative neurology.

[35]  Alan Peters,et al.  GABA immunoreactive neurons in rat visual cortex , 1987, The Journal of comparative neurology.

[36]  H. Grill,et al.  Gustatory cortex in the rat. I. Physiological properties and cytoarchitecture , 1986, Brain Research.

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

[38]  T. Yamamoto,et al.  Gustatory responses of cortical neurons in rats. II. Information processing of taste quality. , 1985, Journal of neurophysiology.

[39]  T. Yamamoto,et al.  Gustatory responses of cortical neurons in rats. I. Response characteristics. , 1984, Journal of neurophysiology.

[40]  G. Buzsáki,et al.  Direct afferent excitation and long-term potentiation of hippocampal interneurons. , 1982, Journal of neurophysiology.

[41]  Joseph B. Travers,et al.  A metric for the breadth of tuning of gustatory neurons , 1979 .

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

[43]  J. Price,et al.  The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat , 1977, The Journal of comparative neurology.

[44]  M. Frank,et al.  An Analysis of Hamster Afferent Taste Nerve Response Functions , 1973, The Journal of general physiology.

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

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

[47]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[48]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[49]  H. Swadlow Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. , 2003, Cerebral cortex.

[50]  T. R. Scott,et al.  Responses to taste stimulation in the ventroposteromedial nucleus of the thalamus in rats. , 2003, Journal of neurophysiology.

[51]  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .