Identification of single neurons in a forebrain network.

Behaviors are generated from complex interactions among networks of neurons. Single-unit ensemble recording has been used to identify multiple neurons in functioning networks. These recordings have provided insight into interactions among neurons in local and distributed circuits. Recorded units in these ensembles have been classed based on waveform type, firing pattern, and physical location. To identify individual projection neurons in a cortical network, we have paired tetrode recording with antidromic stimulation. We developed techniques that enable antidromic identification of single units and study of functional interactions between these neurons and other circuit elements. These methods have been developed in the zebra finch and should be applicable, with potential modifications that we discuss here, to any neural circuit with defined subpopulations based on projection target. This methodology will enable elucidation of the functional roles of single identified neurons in complex vertebrate circuits.

[1]  R. Mooney.  Different Subthreshold Mechanisms Underlie Song Selectivity in Identified HVc Neurons of the Zebra Finch , 2000, The Journal of Neuroscience.

[2]  G. Buzsáki,et al.  Temporal Interaction between Single Spikes and Complex Spike Bursts in Hippocampal Pyramidal Cells , 2001, Neuron.

[3]  P. Church,et al.  Activity of multiple identified motor neurons recorded intracellularly during evoked feedinglike motor programs in Aplysia. , 1994, Journal of neurophysiology.

[4]  Richard Hans Robert Hahnloser,et al.  Sleep-related neural activity in a premotor and a basal-ganglia pathway of the songbird. , 2006, Journal of neurophysiology.

[5]  F. Nottebohm,et al.  Central control of song in the canary, Serinus canarius , 1976, The Journal of comparative neurology.

[6]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[7]  Michael Brecht,et al.  Whisker movements evoked by stimulation of single motor neurons in the facial nucleus of the rat. , 2008, Journal of neurophysiology.

[8]  D. Margoliash.  Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  R. Mooney,et al.  Calcium‐binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata) , 2005, The Journal of comparative neurology.

[10]  Hubert H. Lim,et al.  Antidromic activation reveals tonotopically organized projections from primary auditory cortex to the central nucleus of the inferior colliculus in guinea pig. , 2007, Journal of neurophysiology.

[11]  J. Csicsvari,et al.  Replay and Time Compression of Recurring Spike Sequences in the Hippocampus , 1999, The Journal of Neuroscience.

[12]  Michale S Fee,et al.  A Specialized Forebrain Circuit for Vocal Babbling in the Juvenile Songbird , 2008, Science.

[13]  Daniel Margoliash,et al.  Sleep and sensorimotor integration during early vocal learning in a songbird , 2008, Nature.

[14]  D. Perkel,et al.  Multiple cell types distinguished by physiological, pharmacological, and anatomic properties in nucleus HVc of the adult zebra finch. , 1998, Journal of neurophysiology.

[15]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

[16]  K. D. Punta,et al.  An ultra-sparse code underlies the generation of neural sequences in a songbird , 2002 .

[17]  Dezhe Z. Jin,et al.  Support for a synaptic chain model of neuronal sequence generation , 2010, Nature.

[18]  D. Oliver,et al.  Visualization of neurons filled with biotinylated-Lucifer yellow following identification of efferent connectivity with retrograde transport , 1993, Journal of Neuroscience Methods.

[19]  R. Harris-Warrick,et al.  Modulation of neural networks for behavior. , 1991, Annual review of neuroscience.

[20]  E. Kandel,et al.  MORPHOLOGICAL AND FUNCTIONAL PROPERTIES OF IDENTIFIED NEURONS IN THE ABDOMINAL GANGLION OF APLYSIA CALIFORNICA , 1967 .

[21]  Harvey A Swadlow,et al.  Neocortical efferent neurons with very slowly conducting axons: strategies for reliable antidromic identification , 1998, Journal of Neuroscience Methods.

[22]  S. Baker,et al.  Network oscillations and intrinsic spiking rhythmicity do not covary in monkey sensorimotor areas , 2007, The Journal of physiology.

[23]  Pierre Giraud,et al.  Paired-recordings from synaptically coupled cortical and hippocampal neurons in acute and cultured brain slices , 2008, Nature Protocols.

[24]  Masakazu Konishi,et al.  Gating of auditory responses in the vocal control system of awake songbirds , 1998, Nature Neuroscience.

[25]  M. Nicolelis,et al.  Reconstructing the Engram: Simultaneous, Multisite, Many Single Neuron Recordings , 1997, Neuron.

[26]  R. Mooney,et al.  The HVC Microcircuit: The Synaptic Basis for Interactions between Song Motor and Vocal Plasticity Pathways , 2005, The Journal of Neuroscience.

[27]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate primary visual cortex. I. Stimulus-response relations. , 1990, Journal of neurophysiology.

[28]  A. Selverston,et al.  The stomatogastric nervous system: Structure and function of a small neural network , 1976, Progress in Neurobiology.

[29]  D. Margoliash,et al.  Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

[31]  Adam Johnson,et al.  Cognitive Neural Ensembles in CA 3 Transiently Encode Paths Forward of the Animal at a Decision Point , 2007 .

[32]  W. O. Friesen,et al.  Neuronal generation of the leech swimming movement. , 1978, Science.

[33]  S. Baker,et al.  Cortico-cerebellar coherence during a precision grip task in the monkey. , 2006, Journal of neurophysiology.

[34]  M. Fee,et al.  Singing-related activity of identified HVC neurons in the zebra finch. , 2007, Journal of neurophysiology.

[35]  E.C.L. Vu,et al.  Identification of a forebrain motor programming network for the learned song of zebra finches , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[37]  D. Vicario,et al.  Brain pathways for learned and unlearned vocalizations differ in zebra finches , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Jadin C. Jackson,et al.  Quantitative measures of cluster quality for use in extracellular recordings , 2005, Neuroscience.

[39]  Shane R. Crandall,et al.  HVC neural sleep activity increases with development and parallels nightly changes in song behavior. , 2007, Journal of neurophysiology.

[40]  R. H. Steinberg,et al.  Identification of horizontal cells as S-potential generators in the cat retina by intracellular dye injection. , 1970, Vision research.

[41]  J. Lipski,et al.  Antidromic activation of neurones as an analytic tool in the study of the central nervous system , 1981, Journal of Neuroscience Methods.

[42]  J. F. Prather,et al.  Precise auditory–vocal mirroring in neurons for learned vocal communication , 2008, Nature.

[43]  Jadin C. Jackson,et al.  Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential Experience , 2006, The Journal of Neuroscience.

[44]  T. Nick,et al.  Daily and developmental modulation of “premotor” activity in the birdsong system , 2009, Developmental neurobiology.

[45]  Bruce L. McNaughton,et al.  The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records , 1983, Journal of Neuroscience Methods.