Spike-Timing Precision and Neuronal Synchrony Are Enhanced by an Interaction between Synaptic Inhibition and Membrane Oscillations in the Amygdala
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{"title"=>"Spike-timing precision and neuronal synchrony are enhanced by an interaction between synaptic inhibition and membrane oscillations in the amygdala", "type"=>"journal", "authors"=>[{"first_name"=>"Steven J.", "last_name"=>"Ryan", "scopus_author_id"=>"45761397900"}, {"first_name"=>"David E.", "last_name"=>"Ehrlich", "scopus_author_id"=>"55201430700"}, {"first_name"=>"Aaron M.", "last_name"=>"Jasnow", "scopus_author_id"=>"6603445025"}, {"first_name"=>"Shabrine", "last_name"=>"Daftary", "scopus_author_id"=>"6701426346"}, {"first_name"=>"Teresa E.", "last_name"=>"Madsen", "scopus_author_id"=>"55201242300"}, {"first_name"=>"Donald G.", "last_name"=>"Rainnie", "scopus_author_id"=>"7004363316"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84860364590", "pmid"=>"22563382", "pui"=>"364709179", "isbn"=>"1932-6203 (Electronic) 1932-6203 (Linking)", "scopus"=>"2-s2.0-84860364590", "doi"=>"10.1371/journal.pone.0035320", "issn"=>"19326203"}, "id"=>"c9e55fa9-7029-3fff-8dee-4a20d5145d95", "abstract"=>"The basolateral complex of the amygdala (BLA) is a critical component of the neural circuit regulating fear learning. During fear learning and recall, the amygdala and other brain regions, including the hippocampus and prefrontal cortex, exhibit phase-locked oscillations in the high delta/low theta frequency band (∼2-6 Hz) that have been shown to contribute to the learning process. Network oscillations are commonly generated by inhibitory synaptic input that coordinates action potentials in groups of neurons. In the rat BLA, principal neurons spontaneously receive synchronized, inhibitory input in the form of compound, rhythmic, inhibitory postsynaptic potentials (IPSPs), likely originating from burst-firing parvalbumin interneurons. Here we investigated the role of compound IPSPs in the rat and rhesus macaque BLA in regulating action potential synchrony and spike-timing precision. Furthermore, because principal neurons exhibit intrinsic oscillatory properties and resonance between 4 and 5 Hz, in the same frequency band observed during fear, we investigated whether compound IPSPs and intrinsic oscillations interact to promote rhythmic activity in the BLA at this frequency. Using whole-cell patch clamp in brain slices, we demonstrate that compound IPSPs, which occur spontaneously and are synchronized across principal neurons in both the rat and primate BLA, significantly improve spike-timing precision in BLA principal neurons for a window of ∼300 ms following each IPSP. We also show that compound IPSPs coordinate the firing of pairs of BLA principal neurons, and significantly improve spike synchrony for a window of ∼130 ms. Compound IPSPs enhance a 5 Hz calcium-dependent membrane potential oscillation (MPO) in these neurons, likely contributing to the improvement in spike-timing precision and synchronization of spiking. Activation of the cAMP-PKA signaling cascade enhanced the MPO, and inhibition of this cascade blocked the MPO. We discuss these results in the context of spike-timing dependent plasticity and modulation by neurotransmitters important for fear learning, such as dopamine.", "link"=>"http://www.mendeley.com/research/spiketiming-precision-neuronal-synchrony-enhanced-interaction-between-synaptic-inhibition-membrane-o", "reader_count"=>86, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>8, "Researcher"=>19, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>3, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>8, "Researcher"=>19, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>3, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>4, "Unspecified"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>49, "Medicine and Dentistry"=>4, "Neuroscience"=>16, "Physics and Astronomy"=>1, "Psychology"=>7}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>4}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>16}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>49}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>7, "Japan"=>1, "United Kingdom"=>2, "Chile"=>2}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/647273"], "description"=>"<p>Power spectra of MPOs in BLA PNs in response to a depolarizing step with artificial IPSPs, with mean (solid lines) and 95% confidence intervals (shaded region). Frequencies at which the 95% confidence intervals do not overlap indicate statistically significant differences among the plots. (A) In the presence of TTX, neurons exhibit a weak MPO. (B,C) MPOs were not enhanced by bath application of 100 µM 4-AP (B) but were significantly enhanced by 500 µM 4-AP, with peak power at 4.9 Hz (C). (D) Application of forksolin, an activator of the c-AMP cascade, at 10 µM also enhanced a MPO with peak power at 4.8 Hz. (E) The MPO was significantly enhanced by a combination of 500 µM 4-AP and 10 µM forskolin, with peak power greater than for either drug alone but occurring at a similar frequency. (F) The MPO observed in forskolin and 4-AP was completely abolished by co-application of NiCl (500 µM) to block low-threshold calcium channels.</p>", "links"=>[], "tags"=>["membrane", "oscillation", "was", "modulation", "activation"], "article_id"=>317760, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g007", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_peak_power_of_the_membrane_potential_oscillation_was_sensitive_to_modulation_of_I_A_and_I_T_and_activation_of_PKA_/317760", "title"=>"The peak power of the membrane potential oscillation was sensitive to modulation of I<sub>A</sub> and I<sub>T</sub> and activation of PKA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:57:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/647364"], "description"=>"<p>Intrinsic membrane oscillations of BLA principal neurons, held at −60 mV, in response to a steady depolarizing current injection with and without artificial IPSPs. (A) Shows typical small membrane oscillations in TTX during the depolarizing current injection. In the presence of 1 µM TTX, the introduction of IPSPs evoked a transient depolarizing deflection at the termination of each IPSP, but failed to unmask a MPO. (B) MPOs are not enhanced by application of TEA (500 µM). (C) The addition of 10 µM forskolin had a small enhancing effect on MPOs in the presence of TEA. (D) Application of the inactive isomer dideoxy-forskolin in the presence of 4-AP did not enhance the MPO as observed previously with forskolin.</p>", "links"=>[], "tags"=>["4-ap", "modulation", "membrane", "oscillation", "mimicked", "dideoxy-forskolin"], "article_id"=>317851, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g008", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Forskolin_and_4_AP_modulation_of_the_membrane_potential_oscillation_were_not_mimicked_by_dideoxy_forskolin_and_TEA_respectively_/317851", "title"=>"Forskolin and 4-AP modulation of the membrane potential oscillation were not mimicked by dideoxy-forskolin and TEA, respectively.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:57:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/647094"], "description"=>"<p>(A1–D1) Principal neuron membrane potential response to injection of a sinusoidal current with constant amplitude and linearly changing frequency (0–12 Hz) in the presence of various drug cocktails. All neurons were held at baseline of −60 mV. (A1) Typical voltage response to the sinusoidal current in TTX (1 µM). The resonance of BLA principal neurons can be enhanced by application of 4-AP (B1, 500 µM) and the adenylyl cyclase activator, forskolin (C1, 10 µM), and is abolished by application of NiCl (500 µM, D1). Analysis of power spectra (E) shows that the enhancement of resonance by 4-AP and forskolin is significantly different from baseline (p<0.05). (A2–D3) Intrinsic membrane oscillations of BLA principal neurons, held at −60 mV, in response to a steady depolarizing current injection (A2–D2) and in response to the same current injection with superimposed IPSPs (A3–D3). Similar to resonant properties, membrane oscillations are enhanced by application of 4-AP and forskolin, and abolished in NiCl. Injection of artificial IPSPs in A3–D3 significantly enhanced the amplitude and duration of oscillations (F and G; spectrograms illustrate data from C2 and C3 respectively).</p>", "links"=>[], "tags"=>["neurons", "exhibited", "modifiable", "intrinsic", "resonance", "membrane", "oscillation", "was", "facilitated"], "article_id"=>317571, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g006", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BLA_principal_neurons_exhibited_a_modifiable_intrinsic_resonance_and_a_membrane_potential_oscillation_that_was_facilitated_by_compound_IPSPs_/317571", "title"=>"BLA principal neurons exhibited a modifiable intrinsic resonance and a membrane potential oscillation that was facilitated by compound IPSPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:56:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/646839"], "description"=>"<p>(A) A single sweep recorded from a spiking BLA principal neuron, held at −45 mV by steady-state current injection, displaying a typical regular firing pattern. (B) Multiple sweeps like that in <i>A</i> overlaid and aligned by their first spikes. A raster plot illustrates decay of spike-timing reliability. (C) Injection of artificial IPSPs recovers spike-timing precision.</p>", "links"=>[], "tags"=>["precision", "diminishes", "spike", "trains", "reset"], "article_id"=>317326, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g003", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spike_timing_precision_diminishes_in_spike_trains_and_is_reset_by_compound_IPSPs_/317326", "title"=>"Spike-timing precision diminishes in spike trains and is reset by compound IPSPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:54:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/646902"], "description"=>"<p>(A) Five superimposed traces from a representative principal neuron, held at −60 mV, showing a train of action potentials in response to a depolarizing current step in the presence of DNQX (20 µM), RS-CPP (10 µM) and CGP (2 µM); note the loss of spike-timing precision as the spike train progresses. (B, C) Similar traces to <i>A</i> with the injection of evoked (B) or artificial (C) compound IPSPs to demonstrate improvement of spike-timing precision following a compound IPSP. (D, E, F) Comparisons of spike-timing precision for neurons with no IPSPs (Control, n = 11), evoked IPSPs (n = 11), and artificial IPSPs (n = 11), assessed with a spike correlation metric (see Methods) and plotted as mean ± SEM. Comparisons were made using a two-way ANOVA (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0035320#s3\" target=\"_blank\">Results</a>), and windows of significant differences (p<0.05) in spike correlation are denoted with grey boxes.</p>", "links"=>[], "tags"=>["evoked", "ipsps", "spike-timing", "precision", "bla"], "article_id"=>317392, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Artificial_and_evoked_compound_IPSPs_improved_spike_timing_precision_in_individual_BLA_principal_neurons_/317392", "title"=>"Artificial and evoked compound IPSPs improved spike-timing precision in individual BLA principal neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:55:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/646716"], "description"=>"<p>(A) Spontaneous, compound IPSPs exhibited by a representative pair of primate BLA projection neurons, depolarized to action potential threshold (−45 to −40 mV) using a DC current injection. A raster plot highlights the relative synchrony of spikes following the IPSPs, highlighted in gray boxes. Action potentials are cropped at −30 mV (n = 6). (B) A spike correlation metric (see Methods) is plotted for 6 pairs of primate BLA principal neurons exhibiting compound IPSPs and depolarized to threshold, as in <i>A</i>. Correlation is plotted for each pair as an individual, smoothed trace (thin black lines) representing the mean correlation surrounding every spontaneous, compound IPSP, with the peak of each IPSP aligned to time 0. The mean of all 6 pairs is superimposed as a dotted black line. (C–D) A representative single (C, n = 4) and pair of (D, n = 2) primate BLA principal neurons exhibiting rhythmic firing upon rebound from spontaneous, compound IPSPs. Neurons were depolarized to threshold, as in <i>A</i>. IPSPs and rebound firing are highlighted with gray boxes in <i>C</i>. Action potentials were cropped at −30 mV. (E) A primate BLA principal neuron, depolarized as in <i>A</i>, exhibiting a damped membrane potential oscillation in response to a spontaneous, compound IPSP.</p>", "links"=>[], "tags"=>["ipsps", "coordinated", "spike", "promoted", "rhythmic", "firing", "primate"], "article_id"=>317198, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spontaneous_compound_IPSPs_coordinated_spike_timing_and_promoted_rhythmic_firing_in_the_primate_BLA_/317198", "title"=>"Spontaneous, compound IPSPs coordinated spike timing and promoted rhythmic firing in the primate BLA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:54:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/646632"], "description"=>"<p>(A) A representative pair of primate BLA principal neurons, held at −60 mV, showing compound IPSPs that are rhythmic and highly synchronized, observed during gap-free recordings. (B) A histogram plotting instantaneous frequency of compound IPSPs during 30-second recordings from 12 primate BLA principal neurons. (C) Paired recordings in the primate BLA of a principal neuron receiving compound IPSPs and a burst-firing parvalbumin interneuron, both held at −60 mV. (D) An example of a burst-IPSP pair shown at higher temporal resolution. (E) A compound IPSP can be induced in a BLA principal neuron by using current injection to drive bursting activity in the interneuron.</p>", "links"=>[], "tags"=>["ipsps", "bla", "synchronized", "neurons", "bursts", "inhibitory"], "article_id"=>317110, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spontaneous_compound_IPSPs_in_the_BLA_were_synchronized_across_principal_neurons_and_with_bursts_in_inhibitory_interneurons_/317110", "title"=>"Spontaneous, compound IPSPs in the BLA were synchronized across principal neurons and with bursts in inhibitory interneurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:53:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/647470"], "description"=>"<p>Cumulative power spectra of intrinsic theta frequency MPOs in BLA principal neurons. Responses are plotted as mean (solid lines) and 95% confidence intervals (shaded regions). Frequencies at which the 95% confidence intervals do not overlap indicate statistically significant differences among the plots. (A) BAPTA-containing patch solutions disorganized the frequency tuning of 4-AP- and forskolin-induced MPOs. (B) Inhibiting PKA activation completely abolishes forskolin-induced MPOs. (C) Activation of PKA with the cAMP analog 8Br-cAMP induces MPOs in TTX alone that are similar to those observed in response to forskolin. (D) Activation of mGluR II glutamate receptors with LY379268 completely blocked 4-AP and forskolin-induced theta MPOs.</p>", "links"=>[], "tags"=>["oscillations", "bla", "bi-directionally", "modulated", "adenylyl", "cyclase", "signaling"], "article_id"=>317951, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g009", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Membrane_potential_oscillations_in_the_BLA_were_bi_directionally_modulated_by_the_adenylyl_cyclase_signaling_cascade_/317951", "title"=>"Membrane potential oscillations in the BLA were bi-directionally modulated by the adenylyl cyclase signaling cascade.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:58:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/647018"], "description"=>"<p>(A) Five overlaid, consecutive traces of action potentials during paired recordings of BLA principal neurons, held at −60 mV, in response to a depolarizing current injection without IPSPs and (B) with two IPSPs. (C) Spike correlation metric calculated across pairs of neurons when artificial IPSPs are injected compared to the control condition (n = 6 pairs), plotted against time. Comparisons were made using a two-way ANOVA (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0035320#s3\" target=\"_blank\">Results</a>), and grey boxes denote windows of significant differences (p<0.05) in spike correlation.</p>", "links"=>[], "tags"=>["ipsps", "coordinated", "spike", "pairs", "bla"], "article_id"=>317503, "categories"=>["Physiology", "Neuroscience"], "users"=>["Steven J. Ryan", "David E. Ehrlich", "Aaron M. Jasnow", "Shabrine Daftary", "Teresa E. Madsen", "Donald G. Rainnie"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0035320.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Artificial_compound_IPSPs_coordinated_spike_timing_across_pairs_of_BLA_principal_neurons_/317503", "title"=>"Artificial, compound IPSPs coordinated spike timing across pairs of BLA principal neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:55:50"}

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