Parvalbumin-Positive Basket Cells Differentiate among Hippocampal Pyramidal Cells

CA1 pyramidal cells (PCs) are not homogeneous but rather can be grouped by molecular, morphological, and functional properties. However, less is known about synaptic sources differentiating PCs. Using paired recordings in vitro, two-photon Ca(2+) imaging in vivo, and computational modeling, we found that parvalbumin-expressing basket cells (PVBCs) evoked greater inhibition in CA1 PCs located in the deep compared to superficial layer of stratum pyramidale. In turn, analysis of reciprocal connectivity revealed more frequent excitatory inputs to PVBCs by superficial PCs, demonstrating bias in target selection by both the excitatory and inhibitory local connections in CA1. Additionally, PVBCs further segregated among deep PCs, preferentially innervating the amygdala-projecting PCs but receiving preferential excitation from the prefrontal cortex-projecting PCs, thus revealing distinct perisomatic inhibitory interactions between separate output channels. These results demonstrate the presence of heterogeneous PVBC-PC microcircuits, potentially contributing to the sparse and distributed structure of hippocampal network activity.

[1]  L. Slomianka,et al.  Hippocampal pyramidal cells: the reemergence of cortical lamination , 2011, Brain Structure and Function.

[2]  N. Bannister,et al.  Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: I. Branching patterns , 1995, The Journal of comparative neurology.

[3]  I. Soltesz,et al.  Target-selective GABAergic control of entorhinal cortex output , 2010, Nature Neuroscience.

[4]  P. Somogyi,et al.  Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus , 1996, Hippocampus.

[5]  I Fariñas,et al.  Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. II. The axon initial segment , 1991, The Journal of comparative neurology.

[6]  E. Callaway,et al.  Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity , 2005, Nature Neuroscience.

[7]  N. Spruston,et al.  Hippocampal Pyramidal Neurons Comprise Two Distinct Cell Types that Are Countermodulated by Metabotropic Receptors , 2012, Neuron.

[8]  Jasper Akerboom,et al.  Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging , 2012, The Journal of Neuroscience.

[9]  I. Soltesz,et al.  Basket cell dichotomy in microcircuit function , 2012, The Journal of physiology.

[10]  Andrew M. Poulos,et al.  The neuroscience of mammalian associative learning. , 2005, Annual review of psychology.

[11]  Y. Kawaguchi,et al.  Cortical Inhibitory Cell Types Differentially Form Intralaminar and Interlaminar Subnetworks withExcitatory Neurons , 2009, The Journal of Neuroscience.

[12]  Edward O. Mann,et al.  Inhibitory Interneuron Deficit Links Altered Network Activity and Cognitive Dysfunction in Alzheimer Model , 2012, Cell.

[13]  Attila Losonczy,et al.  Septo-hippocampal GABAergic signaling across multiple modalities in awake mice , 2013, Nature Neuroscience.

[14]  B. McNaughton,et al.  Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[16]  G. Quirk,et al.  Gating of Fear in Prelimbic Cortex by Hippocampal and Amygdala Inputs , 2012, Neuron.

[17]  H. Mclennan,et al.  Bursting response to current‐evoked depolarization in rat ca1 pyramidal neurons is correlated with lucifer yellow dye coupling but not with the presence of calbindin‐D28k , 1991, Synapse.

[18]  I. Soltesz,et al.  New dimensions of interneuronal specialization unmasked by principal cell heterogeneity , 2012, Trends in Neurosciences.

[19]  I. Soltesz,et al.  Distinct Endocannabinoid Control of GABA Release at Perisomatic and Dendritic Synapses in the Hippocampus , 2010, The Journal of Neuroscience.

[20]  G. Buzsáki,et al.  Hippocampal CA1 pyramidal cells form functionally distinct sublayers , 2011, Nature Neuroscience.

[21]  R. Yuste,et al.  Dense Inhibitory Connectivity in Neocortex , 2011, Neuron.

[22]  P. Caroni,et al.  Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus , 2011, Nature Neuroscience.

[23]  Michael L. Hines,et al.  The NEURON Book , 2006 .

[24]  Karl Deisseroth,et al.  Activation of Specific Interneurons Improves V1 Feature Selectivity and Visual Perception , 2012, Nature.

[25]  S. Trouche,et al.  Fear Extinction Causes Target-Specific Remodeling of Perisomatic Inhibitory Synapses , 2013, Neuron.

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

[27]  R. Yuste,et al.  Dense, Unspecific Connectivity of Neocortical Parvalbumin-Positive Interneurons: A Canonical Microcircuit for Inhibition? , 2011, The Journal of Neuroscience.

[28]  G. Quirk,et al.  Neuronal signalling of fear memory , 2004, Nature Reviews Neuroscience.

[29]  J. Miller,et al.  Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat , 1982, Brain Research.

[30]  N. Spruston,et al.  Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus , 2008, The Journal of comparative neurology.

[31]  T. Südhof,et al.  Neuroligin-2 Deletion Selectively Decreases Inhibitory Synaptic Transmission Originating from Fast-Spiking but Not from Somatostatin-Positive Interneurons , 2009, The Journal of Neuroscience.

[32]  Anatol C. Kreitzer,et al.  Distinct Roles of GABAergic Interneurons in the Regulation of Striatal Output Pathways , 2010, The Journal of Neuroscience.

[33]  Massimo Scanziani,et al.  Routing of spike series by dynamic circuits in the hippocampus , 2004, Nature.

[34]  Ivan Soltesz,et al.  Quantitative assessment of CA1 local circuits: Knowledge base for interneuron‐pyramidal cell connectivity , 2013, Hippocampus.

[35]  Sandra J. Kuhlman,et al.  A disinhibitory microcircuit initiates critical period plasticity in visual cortex , 2013, Nature.

[36]  D. Lewis,et al.  Cortical inhibitory neurons and schizophrenia , 2005, Nature Reviews Neuroscience.

[37]  J. Rubenstein,et al.  Pyramidal Neurons in Prefrontal Cortex Receive Subtype-Specific Forms of Excitation and Inhibition , 2014, Neuron.

[38]  C. Robinet,et al.  Oxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Amygdala , 2011, Science.

[39]  Michael Lagler,et al.  Behavior-dependent specialization of identified hippocampal interneurons , 2012, Nature Neuroscience.

[40]  Hiroyuki Miyamoto,et al.  Nav1.1 Localizes to Axons of Parvalbumin-Positive Inhibitory Interneurons: A Circuit Basis for Epileptic Seizures in Mice Carrying an Scn1a Gene Mutation , 2007, The Journal of Neuroscience.

[41]  G. Tamás,et al.  Excitatory Effect of GABAergic Axo-Axonic Cells in Cortical Microcircuits , 2006, Science.

[42]  L. Swanson,et al.  Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex , 2007, Brain Research Reviews.

[43]  I. Soltesz Diversity in the Neuronal Machine , 2006 .

[44]  P. Golshani,et al.  Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice , 2012, Proceedings of the National Academy of Sciences.