Involvement of the GABAergic Septo-Hippocampal Pathway in Brain Stimulation Reward
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{"title"=>"Involvement of the gabaergic septo-hippocampal pathway in brain stimulation reward", "type"=>"journal", "authors"=>[{"first_name"=>"Germán", "last_name"=>"Vega-Flores", "scopus_author_id"=>"6503958911"}, {"first_name"=>"Agnès", "last_name"=>"Gruart", "scopus_author_id"=>"7004080075"}, {"first_name"=>"José M.", "last_name"=>"Delgado-GarcÍa", "scopus_author_id"=>"7005221472"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"25415445", "sgr"=>"84912040802", "doi"=>"10.1371/journal.pone.0113787", "scopus"=>"2-s2.0-84912040802", "pui"=>"600550005", "issn"=>"19326203"}, "id"=>"c10ae9ec-5d72-30f8-888a-f62c83486008", "abstract"=>"The hippocampus is a structure related to several cognitive processes, but not very much is known about its putative involvement in positive reinforcement. In its turn, the septum has been related to instrumental brain stimulation reward (BSR) by its electrical stimulation with trains of pulses. Although the anatomical relationships of the septo-hippocampal pathway are well established, the functional relationship between these structures during rewarding behaviors remains poorly understood. To explore hippocampal mechanisms involved in BSR, CA3-evoked field excitatory and inhibitory postsynaptic potentials (fEPSPs, fIPSPs) were recorded in the CA1 area during BSR in alert behaving mice. The synaptic efficiency was determined from changes in fEPSP and fIPSP amplitudes across the learning of a BSR task. The successive BSR sessions evoked a progressive increase of the performance in inverse relationship with a decrease in the amplitude of fEPSPs, but not of fIPSPs. Additionally, we evaluated CA1 local field potentials (LFPs) during a preference task, comparing 8-, 20-, and 100-Hz trains of septal BSR. We corroborate a clear preference for BSR at 100 Hz (in comparison with BSR at 20 Hz or 8 Hz), in parallel with an increase in the spectral power of the low theta band, and a decrease in the gamma. These results were replicated by intrahippocampal injections of a GABAB antagonist. Thus, the GABAergic septo-hippocampal pathway seems to carry information involved in the encoding of reward properties, where GABAB receptors seem to play a key role. With regard to the dorsal hippocampus, fEPSPs evoked at the CA3-CA1 synapse seem to reflect the BSR learning process, while hippocampal rhythmic activities are more related to reward properties.", "link"=>"http://www.mendeley.com/research/involvement-gabaergic-septohippocampal-pathway-brain-stimulation-reward", "reader_count"=>20, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>5, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>5, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Agricultural and Biological Sciences"=>3, "Medicine and Dentistry"=>3, "Neuroscience"=>5, "Psychology"=>4, "Social Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>5}, "Social Sciences"=>{"Social Sciences"=>2}, "Psychology"=>{"Psychology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Austria"=>1, "Netherlands"=>1, "United States"=>2, "Brazil"=>1, "Chile"=>1, "Spain"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1804059"], "description"=>"<p>(<i>A</i>) Schematic representation of the main septo-hippocampal projections. Glutamatergic (red), GABAergic (blue), and cholinergic (gray) projections are indicated. Arrowheads indicate flux direction of neuronal information. (<i>B</i>) Animals were chronically implanted with stimulating (St.) and recording (Rec.) electrodes aimed to activate the CA3-CA1 synapse in the right dorsal hippocampus. In addition (right diagram), a bipolar stimulating electrode was implanted in the medial septum (MS). In some animals a guide cannula was also implanted in the dorsal hippocampus. Abbreviations: DG, dentate gyrus; D, L, A, dorsal, lateral, anterior; LS, lateral septum; LV, lateral ventricle; P, pyramidal cell. (<i>C</i>) The training protocol to learn brain stimulation reward (BSR) started with some shaping (Sh) sessions. A Sh session consisted of i) a baseline (BL) period for evoking fPSPs at the CA3-CA1 synapse with the animal located in a small box; ii) during a Skinner box (SB) session, the animal was presented with a train of stimuli to the medial septum as reinforcement, followed 40 ms later by a single pulse applied to the CA1-CA3 synapse contingent to approaches to the lever; and iii) a recovery recording (R) period under the same conditions as for BL. After Sh sessions, the animal was allowed to carry out BSR by itself (right). For this, we used the same recording periods (BL, SB, and R) as for shaping. Reinforcements could be received at a maximum rate of one/5 s. At the bottom is shown a diagram summarizing the experimental design, where squares represent the shaping training whilst circles represent BSR protocols. This key diagram is reproduced in the following figures, displaying in dark gray the corresponding stage. (<i>D</i>) Illustrative recordings (averaged 10 times) evoked at the CA3-CA1 synapse (arrows) and collected during baseline (BL), 40 ms after a medial septum train (SB), and recovery (R) stages. Examples of how the stage is represented in the following figures by the key diagram are shown. (<i>E</i>) Representative recording (averaged 10 times) collected in the CA1 area following train stimulation of the medial septum (black horizontal bar). The green arrow indicates the point where the fPSP will be evoked (40 ms delay from the train). The green arrow indicates the selected moment to evoke an fPSP at the CA3-CA1 synapse. (<i>F</i>) Here is illustrated how fPSPs evoked at the CA3-CA1 synapse were divided to compute the amplitude (dashed lines) of the fEPSPs (mediated by glutamate, GLU) and the late fIPSPs. The fIPSP components (A, mediated by GABA<sub>A</sub> receptors, B, mediated by GABA<sub>B</sub> receptors) and the stimulus presented to the CA3 area (white arrow) are indicated.</p>", "links"=>[], "tags"=>["CA 1 area", "hz", "reward properties", "fepsp", "brain stimulation reward", "bsr", "lfp", "GABAB"], "article_id"=>1249284, "categories"=>["Uncategorised"], "users"=>["Germán Vega-Flores", "Agnès Gruart", "José M. Delgado-García"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113787.g001", "stats"=>{"downloads"=>3, "page_views"=>245, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anatomical_septo_hippocampal_projections_electrode_placement_and_BSR_protocol_/1249284", "title"=>"Anatomical septo-hippocampal projections, electrode placement and BSR protocol.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-21 03:21:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1804060"], "description"=>"<p>(<i>A</i>) Animals' performance was computed as (number of reinforcements obtained)/(maximum number of available reinforcements) x 100. Data for each mouse (n = 30) were arranged according to their own zero point, labeled as day “0”. Shaping and BSR are indicated by brown or orange edges, respectively. (<i>B</i>) Representative averages (10 times) of fPSPs recorded on three different days during the learning process of BSR. Illustrated fPSPs correspond to the shaping stage (<i>1</i>), the day when animals reached BSR criterion (<i>2</i>), and eight days after BSR criterion was reached (<i>3</i>). White arrows indicate stimulation of the CA3 area (St.). The horizontal black bar indicates a fragment of medial septum stimulation. BL, baseline; SB, recording inside the Skinner box. (<i>C</i>) Changes in fEPSP components across training (n = 28). The polynomial trend lines for the amplitude of fEPSP (or GLU) during shaping and BSR stages are indicated. Statistical comparisons are indicated vs. BL values (horizontal dashed line in 100%). (<i>D</i>) Changes in fIPSP components across training (n = 28). The polynomial trend lines for the amplitude of GABA<sub>B</sub> component during shaping and BSR stages are indicated. Statistical comparisons are indicated vs. BL values (dashed line in 100%). (*) <i>P</i><0.05; (**) <i>P</i><0.01; (***) <i>P</i><0.001. Code bars at the top in each section are defined in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0113787#pone-0113787-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["CA 1 area", "hz", "reward properties", "fepsp", "brain stimulation reward", "bsr", "lfp", "GABAB"], "article_id"=>1249285, "categories"=>["Uncategorised"], "users"=>["Germán Vega-Flores", "Agnès Gruart", "José M. Delgado-García"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113787.g002", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Acquisition_of_the_BSR_protocol_and_changes_evoked_in_fPSPs_/1249285", "title"=>"Acquisition of the BSR protocol and changes evoked in fPSPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-21 03:21:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1804061"], "description"=>"<p>(<i>A</i>) The upper panel shows representative fPSPs (averaged 15 times) evoked at the CA3-CA1 synapse before injection (black solid line), in the presence of vehicle (gray dotted line) or following CGP injection (gray solid line). The bottom histograms illustrate the averaged fPSP amplitudes corresponding to glutamate- (GLU) and GABA-related components (GABA<sub>A</sub> and GABA<sub>B</sub>). Comparisons were made vs. vehicle injection (horizontal dashed line). (<i>B</i>) CGP effects on animals' BSR determined as (number of reinforcements obtained)/(maximum number of available reinforcements) x 100. Illustrated data range from two days before to two days after (white circles) an intrahippocampal single injection (black circle) of CGP. (<i>C</i>) Quantitative effects of CGP injection on fEPSP amplitude. Two sessions prior to (−2, −1) and two sessions after (1, 2) the injection day (black dot) are illustrated. The statistical comparisons are represented vs. BL values (dashed line in 100%). (<i>D</i>) As in <i>C</i>, same quantitative representation of effects induced by CGP injection but for fIPSP (GABA<sub>B</sub>) amplitude. The statistical comparisons are indicated vs. BL values (dashed line in 100%) (*) <i>P</i><0.05; (**) <i>P</i><0.01; (***) <i>P</i><0.001. Code bars at the top in each section are defined in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0113787#pone-0113787-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["CA 1 area", "hz", "reward properties", "fepsp", "brain stimulation reward", "bsr", "lfp", "GABAB"], "article_id"=>1249286, "categories"=>["Uncategorised"], "users"=>["Germán Vega-Flores", "Agnès Gruart", "José M. Delgado-García"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113787.g003", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_intrahippocampal_injection_of_CGP_35348_on_BSR_performance_and_the_associated_fPSP_changes_/1249286", "title"=>"Effects of intrahippocampal injection of CGP 35348 on BSR performance and the associated fPSP changes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-21 03:21:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1804062"], "description"=>"<p>(<i>A</i>) A representative preference test session illustrating the comparison between 100 Hz and 20 Hz of BSR with two available levers. From top to bottom are illustrated the obtained rewards (Rew), LFPs recorded (Rec) in the CA1 area, and presses for lever 1 (L1) and lever 2 (L2). Note how the mouse switched levers across the session to receive septal self-stimulation at 100 Hz (yellow) rather than at 20 Hz (red). (<i>B</i>) Enlarged sections from <i>A</i> for one reinforcement at 100 Hz (left) and one at 20 Hz (right). The LFP channel (Rec.) shows the three time windows (A, blue; B, red, and C, green; each one was 2.2 s long) constructed around each septal self-stimulation. The time that the mouse kept the lever pressed is indicated. The bottom panel illustrates the same recording epochs in a color code for the power spectra. For clarity, only gamma (γ, 60–80 Hz) and low theta (θ, 2–6 Hz) bands are illustrated. Note that the decreased power in gamma and increased power in low theta within window C (dashed ovals) evoked by the reward at 100 Hz were not seen in the reward at 20 Hz. Color scale: green, 100%; red, 200%. (<i>C</i>) Preferences in the frequency of reward from the whole group (n = 9). **, <i>P</i><0.01; and ***, <i>P</i><0.001. (<i>D</i>) Time windows (A, blue; B, red; and C, green) represented as cumulative power for the group during vehicle and CGP 35348 injections. Gamma (upper) and theta (bottom) bands are shown. The vehicle injection evoked the same changes as the 100 Hz rewards of the preference test (n = 8 animals, 16 sessions). The CGP injection abolished the increased power in the theta band, mimicking the effect of the less-preferred frequencies of reward (8 Hz, 20 Hz) (n = 7 animals, 9 sessions). (<i>E</i>, <i>F</i>) As in <i>D</i>, time windows represented as cumulative power for the group during the preference test. In window C, the less-preferred frequencies of reward (20 Hz, 8 Hz) did not induce changes in gamma and theta bands as the preferred frequency (100 Hz) did. The stimulation with 100 Hz as reward was associated with a decrease in the gamma band and an increase in the theta in comparison with both 20 Hz and 8 Hz (n = 9 animals, 20–30 sessions). Code bars at the top in A and C are defined in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0113787#pone-0113787-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["CA 1 area", "hz", "reward properties", "fepsp", "brain stimulation reward", "bsr", "lfp", "GABAB"], "article_id"=>1249287, "categories"=>["Uncategorised"], "users"=>["Germán Vega-Flores", "Agnès Gruart", "José M. Delgado-García"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113787.g004", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_the_spectral_power_of_LFP_recorded_during_animals_BSR_/1249287", "title"=>"Changes in the spectral power of LFP recorded during animals' BSR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-21 03:21:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1804063"], "description"=>"<p>(<i>A</i>) Power spectra values collected from a representative animal. From top to bottom are illustrated lever presses (Lever), the reward train (Reward), and the power value corresponding to the low theta (3–5.8 Hz) band. Two frequencies of reward tested (100 Hz, 20 Hz) are shown in relation to lever-press activity. Each section (panels 4 s long) corresponds to 30 overlapped sweeps (the lever trace remains high for the time that the lever is held down) as well as their corresponding power values in the low theta band. Gray squares indicate time window C. Note the increase in power spectrum values related to the preferred frequency of reinforcement (100 Hz). This increase was not associated with lever activity. (<i>B</i>) Power values collected—always using 100 Hz of reward—from a representative mouse in two different sessions: vehicle and CGP injections. Traces are displayed as in <i>A</i>. Note that the increase in power values during vehicle administration sessions was clearly larger than during CGP sessions. Again, no relationship with lever activity was noticed. Code bars at the top in A and B are defined in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0113787#pone-0113787-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["CA 1 area", "hz", "reward properties", "fepsp", "brain stimulation reward", "bsr", "lfp", "GABAB"], "article_id"=>1249288, "categories"=>["Uncategorised"], "users"=>["Germán Vega-Flores", "Agnès Gruart", "José M. Delgado-García"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113787.g005", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Power_spectra_in_the_low_theta_band_evoked_by_the_different_reinforcement_frequencies_and_by_the_local_injection_of_CGP_35348_during_time_window_C_and_their_relationship_with_the_number_of_lever_presses_/1249288", "title"=>"Power spectra in the low theta band evoked by the different reinforcement frequencies and by the local injection of CGP 35348 during time window C, and their relationship with the number of lever presses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-21 03:21:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1804064"], "description"=>"<p>(<i>A</i>) Ratio for the low theta band (2–6.3 Hz) for the three frequencies of reward (upper, 100 Hz vs. 20 Hz; middle, 100 Hz vs. 8 Hz) as well as for vehicle vs. CGP injections (bottom). The bars on the right represent the total average for the gray band (3–5.8 Hz). (<i>B</i>) The same ratio as in <i>A</i>, but represented for the gamma band (60–80 Hz). *, <i>P</i><0.05; **, <i>P</i><0.01; and ***, <i>P</i><0.001. Code bar at the top in A is defined in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0113787#pone-0113787-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["CA 1 area", "hz", "reward properties", "fepsp", "brain stimulation reward", "bsr", "lfp", "GABAB"], "article_id"=>1249289, "categories"=>["Uncategorised"], "users"=>["Germán Vega-Flores", "Agnès Gruart", "José M. Delgado-García"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113787.g006", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differences_in_the_ratio_time_window_C_after_reward_time_window_B_before_reward_for_power_spectra_computed_from_LFP_evoked_in_the_hippocampal_CA1_area_during_the_preference_test_and_following_CGP_35348_intrahippocampal_injections_/1249289", "title"=>"Differences in the ratio time window C (after reward)/time window B (before reward) for power spectra computed from LFP evoked in the hippocampal CA1 area during the preference test and following CGP 35348 intrahippocampal injections.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-21 03:21:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1804066"], "description"=>"<p>Data collected from a representative mouse during the previously defined time windows (A, B, and C) were analyzed each day along shaping and BSR protocols. From top to bottom, the three time windows are represented in three panels by semi-overlapped averaged spectral power profiles. The upper section of each panel represents high frequencies (60–120 Hz) and the bottom one the lower frequencies (1–40 Hz) during shaping (−2, −1 and 0) and brain stimulation (1–6) sessions. The session in which criterion was reached (day 0) is represented in solid blue. The color code corresponding to each illustrated session (from −2 to 6) is illustrated at the bottom. Code bars at the top are defined in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0113787#pone-0113787-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["CA 1 area", "hz", "reward properties", "fepsp", "brain stimulation reward", "bsr", "lfp", "GABAB"], "article_id"=>1249290, "categories"=>["Uncategorised"], "users"=>["Germán Vega-Flores", "Agnès Gruart", "José M. Delgado-García"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0113787.g007", "stats"=>{"downloads"=>2, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spectral_power_analysis_of_EEGs_recorded_in_the_hippocampal_CA1_area_during_shaping_sessions_and_BSR_performance_/1249290", "title"=>"Spectral power analysis of EEGs recorded in the hippocampal CA1 area during shaping sessions and BSR performance.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-21 03:21:39"}

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Relative Metric

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