F1000Research F1000Research 2046-1402 F1000 Research Limited London, UK 10.12688/f1000research.3895.2 Data Note Articles Behavioral Neuroscience Data Sharing Neuronal & Glial Cell Biology Neurosharing: large-scale data sets (spike, LFP) recorded from the hippocampal-entorhinal system in behaving rats

[version 2; peer review: 4 approved]

 Mizuseki Kenji a 1 2 3 Diba Kamran 2 4 Pastalkova Eva 2 5 Teeters Jeff 6 Sirota Anton 2 7 Buzsáki György b 1 2 8 NYU Neuroscience Institute, Langone Medical Center, New York University, New York, NY, USA Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, NJ, USA Allen Institute for Brain Science, Seattle, WA, USA Department of Psychology, University of Wisconsin at Milwaukee, Milwaukee, WI, USA Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA Redwood Center for Theoretical Neuroscience, University of California, Berkeley, Berkeley, CA, USA Centre for Integrative Neuroscience, University of Tübingen, Tübingen, Germany Center for Neural Science, New York University, New York, NY, USA kenjim@alleninstitute.org Gyorgy.Buzsaki@nyumc.org

KM, KD, EP and GB designed the experiments. KM, KD and EP carried out experiments and collected the data. KM collected data from rats ec012, ec013, ec014 and ec016. KD collected data from rats gor01, pin01 and vvp01. EP collected data from rats f01_m, g01_m, i01_m and j01_m. KM carried out all spike sorting and classification of cell types in this dataset. JT prepared documentations for public data release (data sets hc-2 and hc-3) at CRCNS.org. AS prepared an earlier version of documentations for data set hc-2 at CRCNS.org. KM, JT and GB wrote the paper. All authors were involved in the revision of the draft manuscript and have agreed to the final content.

Competing interests: No competing interests were disclosed.

 18 7 2014 2014 3 98 16 7 2014 Copyright: © 2014 Mizuseki K et al. 2014 This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Using silicon-based recording electrodes, we recorded neuronal activity of the dorsal hippocampus and dorsomedial entorhinal cortex from behaving rats. The entorhinal neurons were classified as principal neurons and interneurons based on monosynaptic interactions and wave-shapes. The hippocampal neurons were classified as principal neurons and interneurons based on monosynaptic interactions, wave-shapes and burstiness. The data set contains recordings from 7,736 neurons (6,100 classified as principal neurons, 1,132 as interneurons, and 504 cells that did not clearly fit into either category) obtained during 442 recording sessions from 11 rats (a total of 204.5 hours) while they were engaged in one of eight different behaviours/tasks. Both original and processed data (time stamp of spikes, spike waveforms, result of spike sorting and local field potential) are included, along with metadata of behavioural markers. Community-driven data sharing may offer cross-validation of findings, refinement of interpretations and facilitate discoveries.

 The research was supported by Uehara Memorial Foundation Research Fellowship (KM), Astellas Foundation for Research on Metabolic Disorders Research Fellowship (KM), Japan Society for the Promotion of Science’s Postdoctoral Fellowship for Research Abroad (KM), NIH NS034994 (GB), NIH MH54671 (GB), NS074015 (GB), National Science Foundation Grant S E 0542013 (GB), The Human Frontier Science Program(GB), the James S. McDonnell Foundation (GB), the Kavli Foundation (GB), General Electric, Inc. (GB), HHMI (EP), Patterson Trust (EP), National Science Foundation Grant 0855272 (JT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Amendments from Version 1

We revised our manuscript following the comments of the reviewers.

 Introduction

The hippocampus and entorhinal cortex are essential structures for memory and spatial navigation 1– 8 . Position-tuned cells (‘place cells’) are present in CA1, CA3 and dentate gyrus regions 1, 9 . Grid cells, head direction cells, and border cells have been described in the dorsomedial entorhinal cortex, and are critical ingredients of navigation systems 5, 7, 8, 10– 13 . The temporal coordination across the entorhinal cortex and hippocampus is secured by various oscillations, especially theta, gamma and sharp wave ripples 14– 21 .

We recorded activity of neurons in these brain regions while animals performed various tasks, such as linear track, open maze, T-maze with wheel running delay, plus maze and zigzag maze, as well as recordings during sleep in the home cage. Extensive technical descriptions of the data sets described in this document are available in several published papers 6, 21– 27 .

Several questions related to memory, navigation, spike time patterns, population coding, neuronal interactions, neuronal classification, replay, sleep homeostasis and oscillations have been studied based on this dataset 6, 21– 43 . However, this dataset may provide valuable information if subjected to yet further analyses. Improved spike sorting, neuron classification and more sophisticated analyses may extend and refine the initial conclusions and offer insights that were previously missed. For these reasons we provide both unprocessed (wide band) and processed versions of our data. In our experience, all methods have limitations and must undergo continuous revision.

We believe that community-driven data sharing, cross-validation of data, unified data formats and large collaborative efforts will facilitate discovery and benefit future progress in neuroscience. We are well aware of the potential risks and arguments against data sharing 44 but are of the opinion that the benefits of sharing countervail the risks.

 Material and methods Animal surgery

All protocols were approved by the Institutional Animal Care and Use Committee of Rutgers University (protocol No. 90-042), and all experiments were performed at Rutgers University. Before surgery, one to four rats were housed in a single home cage (made of plastic; size L = 45 cm, W = 23.5 cm, H = 20 cm). Wood shavings were used as bedding and dry pellets were provided as food. The animals were housed in a temperature controlled (68°F), but not a specific pathogen free, environment under 12:12-hours light:dark cycle where light cycle was from 7AM to 7PM. After surgery, the rats were housed individually, and highly absorbent paper (Techboard, Shepherd Specialty Papers) was used as bedding, and the animal’s health was assessed daily by the experimenters.

Details of surgery and recovery procedures have been previously described in detail 45, 46 . Eleven Long Evans rats (male, 3–8 months old, 250–400 g) were deeply anesthetized with isoflurane (1–1.5%). In two rats (f01_m and g01_m), two silicon probes were implanted (one in each hemisphere) and targeted CA1 region. In three rats (gor01, pin01 and vvp01), two probes (32- and/or 64-site silicon probes) were implanted in the left dorsal hippocampus, targeted to CA1 and CA3 separately, and advanced over sessions and days through overlying neocortical and hippocampal tissue. The probe positions were: rat pin01: CA3: a plane formed by probe shanks was at a 35° angle to coronal plane approximately along the septo-temporal axis, probe shanks were centered on 2.8 mm posterior and 2.6 mm lateral to bregma. CA1: a plane formed by probe shanks was at a 26.5° angle to vertical, at a 35° angle to coronal approximately along the septo-temporal axis, probe shanks were centered on 4.6 mm posterior and 2.4 mm lateral to bregma; rat vvp01: CA3: a plane formed by probe shanks was at a 26.5° angle to coronal plane, probe shanks were centered on 2.8 mm posterior and 2.6 mm lateral to bregma. CA1: a plane formed by probe shanks was at a 26.5° angle to vertical, parallel to sagittal plane, probe shanks were centered on 4.4 mm posterior and 2.3 mm lateral to bregma; rat gor01: CA3: a plane formed by probe shanks was at a 26.5° angle to coronal plane, probe shanks were centered on 3.1 mm posterior, and 3.0 mm lateral to bregma. CA1: a plane formed by probe shanks was at a 26.5° angle to vertical, at a 45° angle to coronal plane, probe shanks were centered on 4.9 mm posterior and 1.5 mm lateral to bregma. In four rats (ec013, ec014, ec016 and i01_m), 32- or 64-site silicon probe(s) were implanted in the right dorsal hippocampus and recorded from CA1, CA3 or dentate gyrus, and another 4-shank silicon probe was implanted in the right dorsocaudal medial entorhinal cortex. In one rat (ec012), one 4-shank silicon probe was implanted in the right dorsocaudal medial entorhinal cortex. In rat ec012, ec013, ec014, and ec016, the probe targeting the entorhinal cortex was positioned such that the different shanks recorded from different layers 21 (4.5 mm lateral from the midline; 0.1 mm anterior to the edge of the transverse sinus at a 20–25° angle in the sagittal plane with the tip pointing toward the anterior direction). In rat i01_m, the EC probe had 4 shanks and was positioned such that all shanks recorded from the same layer. For the hippocampus probe in rats ec013, ec014 and ec016, the shanks were aligned parallel to the septo-temporal axis of the hippocampus (45° parasagittal), positioned centrally at 3.5 mm posterior from bregma and 2.5 mm lateral from the midline. During recordings, CA1 electrodes could be recognized by characteristic ripples in the pyramidal layer, whereas uniform ripples were not detected on the DG or CA3 electrodes.

For all silicon probes used, each shank had eight recording sites (160 µm 2 each site, 1–3-MΩ impedance), and intershank distance was 200 µm. Recordings sites were staggered to provide a two-dimensional arrangement (20 µm vertical separation) 47, 48 . The individual silicon probes were attached to respective microdrives and moved independently and slowly to the target. Two stainless steel screws inserted above the cerebellum were used as indifferent (reference) and ground electrodes during recordings. At the end of the physiological recordings during the behavioural tasks, a small anodal DC current (2–5 µA, 10 s) was applied to recording sites 1 or 2 days before rats were deeply anesthetized and euthanized by perfusion with 10% formalin solution. The positions of the electrodes were confirmed histologically and reported previously in detail 21, 24 . Histological pictures of rat ec012, ec013, ec014 ec016 are reported in the original publications, using the same animal identifiers 21 . Histological analysis of rat pin01, vvp01 and gor01 was also reported previously using animal identifier rat1, 2 and 3 respectively 24 . Histological verification of rats f01_m, g01_m, i01_m and j01_m is not available, but the physiological characterization of the recording sites provide a reliable indication of their locations.

 Behavioural testing

After the animals recovered from surgery (1 to 2 weeks), physiological signals were recorded during eight different types of behaviours mostly during light cycles (see Table 1).

Behaviour descriptions.
Behaviour Behaviour subclass (Behaviour identifier) Description
elevated linear track linear Linear track, 250 cm × 7 cm.
elevated linear track linearOne Linear track (170 cm × 6.2 cm, with 22 cm × 22 cm end platforms) that was shortened to 79 or 125 cm in some trials 23, 24 (Usually shortened but sometimes also lengthened). The same linear track was used in linearOne and linearTwo but at different locations in the same recording room. The center of the track was at the same position for linearOne and linearTwo, but the track was at fixed at a 74° angles from each other, corresponding to the diagonals of the 480 × 640 pixel camera.
elevated linear track linearTwo Exactly the same as linearOne but the linear track was at different locations in the same recording room. See linearOne.
open field bigSquare 180 cm × 180 cm.
open field bigSquarePlus 180 cm × 180 cm square open field, divided by plus shaped walls put in the center of the field.
open field midSquare 120 cm × 120 cm.
open field Open 100 cm × 200 cm.
rewarded wheel- running task wheel Operant wheel running task, See Mizuseki et al., 2009 21 .
alternation task in T-maze Mwheel Alternation task in T-maze (100 cm × 120 cm) with wheel running delay. See Pastalkova et al., 2008 6 .
alternation task in T-maze Tmaze Alternation task in T-maze, the same as Mwheel but without delay period. There were 2.78 camera pixels/cm, which converts to 22.24 units/cm for the .whl files (8x compression of pixels).
elevated plus maze plus Plus maze. 100 cm × 100 cm.
zigzag maze Zigzag 100 cm × 200 cm zigzag maze. See Royer et al., 2010 49 .
wheel-running in home cage wheel_home Wheel running in home cage with free access to a wheel with no reinforcement.
sleep sleep Sleeping in home cage.

On an elevated linear track (250 cm × 7 cm), the animals were required to run back and forth to obtain water reward at both ends 21 . In three animals (gor01, pin01, and vvp01), a similar elevated track was used (170 cm × 6.2 cm, with 22 cm × 22 cm end platforms) that was shortened to 79 or 125 cm in some trials 23, 24 .

In the open field task, the rats chased randomly dispersed drops of water or pieces of Froot Loops (25 mg; Kellogg’s) on an elevated open platform 21 (180 cm × 180 cm, 120 cm × 120 cm or 100 cm × 200 cm).

In the rewarded wheel-running task, a wheel (diameter = 29 cm) was attached to a rectangular-shape box (39 cm × 39 cm × 39 cm). The rat was required to run in the wheel continuously for 10 seconds, after which time a piece of Froot Loop was dropped in the box as reinforcement 21 .

In the alternation task in the T-maze (100 cm × 120 cm) with wheel running delay, the animal was required to run on a wheel attached to the waiting area for 10 sec, after which time the animal had access to the central arm of the T-maze, at the end of which the animal chose to turn right or left. The animal was rewarded with water if the choice was opposite to the previous one 6 .

The elevated plus maze (100 cm × 100 cm) consisted of two open and two closed arms, and each arm had a water cup at the outer end of the corridor. Before the session started, all the four cups were filled with water (~20ul). Once the animal consumed water in all of the water cups, water was given in two water cups either in the closed or open arms depending on the last visited arm. If the animal consumed the water in the closed arm lastly, water was provided in water cups in the open arms (and vice versa) and this regime continued to encourage the rat to visit all arms with similar probability.

In the zigzag maze (100 cm × 200 cm) with 11 corridors, the animals learned to run back and forth between two water wells; 100 µl of water was delivered at each well 21, 22, 25, 49 .

In the wheel-running in home cage, a wheel (diameter = 29 cm) was attached to a rectangular-shape box (39 cm × 39 cm × 39 cm) which was used as a home cage during the experiment. Rats had free access to the wheel, and ran on the wheel with no reinforcement.

In the sleeping session, the rat slept in the home cage.

For recording of behaviour (1) to (6), animals were water-scheduled for 23 hours prior to the experiment. Otherwise, both dry food and water were provided ad libitum. For tracking the position of the animals, two small light-emitting diodes, mounted above the headstage, were recorded by a digital video camera (SONY) at 30 Hz resolution.

 Data collection and cell-type classification

Detailed information about the recording system and spike sorting has been previously described 21, 24, 45 . Briefly, signals were amplified (1,000×), bandpass-filtered (1 Hz–5 kHz) and acquired continuously at 20 kHz (DataMax system; RC Electronics) or 32,552 Hz (NeuraLynx, MT) at 16-bit resolution. After recording, the signals were down-sampled to 1,250 Hz (DataMax system) or 1,252 Hz (NeuraLynx system) for the local field potential (LFP) analysis. In electrophysiological recordings, positive polarity is from zero toward positive values. To maximize the detection of very slowly discharging (‘silent’) neurons 50 , clustering was performed on concatenated files of several behavioural and sleep sessions recorded at the same electrode position on the same recording day 22, 25– 27 . We made extensive use of publicly available analytical and display programs, which were developed in our laboratory (KlustaKwik 51 available at http://sourceforge.net/projects/klustakwik/, Neuroscope 52 available at http://neuroscope.sourceforge.net/, Klusters 52 available at http://klusters.sourceforge.net/, NDmanager 52 available at http://ndmanager.sourceforge.net/). The latest available version at the time was used in each case. Spike sorting was performed automatically, using KlustaKwik 51 , followed by manual adjustment of the clusters, with the help of autocorrelogram, cross-correlogram and spike wave-shape similarity matrix (Klusters software package 52 ). Because none of the existing spike sorting algorithms is completely automated, manual adjustment is necessary 51 . This inevitably leads to some operator-dependent variability 51 ; therefore, provided clusters are not always identical to those used in our previous publications. Hippocampal principal cells and interneurons were separated based on their burstiness, waveforms and short-term monosynaptic interactions 6, 17, 21, 24, 45 . Classification of principal neurons and interneurons of entorhinal cortical neurons was based on waveforms and short-term monosynaptic interactions, and described previously in detail 21 . A total of 3,113 (CA1), 882 (CA3), 66 (DG), 491 (EC2), 568 (EC3) and 551 (EC5) principal neurons and 420 (CA1), 198 (CA3), 52 (DG), 85 (EC2), 215 (EC3) and 91 (EC5) interneurons were identified and included in this data set (see Table 2– Table 4).

Number of cells recorded.

Top row: animal identifier. Left column: brain region. Brain region EC4 indicates either entorhinal cortex layer 3 or 5 (could not be determined which); region EC? indicates in entorhinal cortex, but without layer assignment.

Brain region ec012 ec013 ec014 ec016 f01_m g01_m gor01 i01_m j01_m pin01 vvp01 total
EC2 311 180 112 603
EC3 201 362 177 116 856
EC4 276 57 333
EC5 110 416 68 154 748
EC? 82 82
Total EC 311 1365 425 439 82 2622
CA1 1185 1136 661 99 145 50 309 23 116 3724
CA3 223 646 153 45 56 1123
DG 41 94 135
Unknown 39 3 90 132
Total 311 2853 1561 1840 99 145 203 394 90 68 172 7736
Number of principal cells.

Top row: animal identifier. Left column: brain region.

Brain region ec012 ec013 ec014 ec016 f01_m g01_m gor01 i01_m j01_m pin01 vvp01 total
EC2 248 146 97 491
EC3 140 239 101 88 568
EC4 214 46 260
EC5 89 300 34 128 551
EC? 51 51
Total EC 229 1001 281 359 51 1921
CA1 887 995 577 79 131 42 289 19 94 3113
CA3 217 443 138 41 43 882
DG 18 48 66
Unknown 37 1 80 118
Total 229 2160 1276 1427 79 131 180 341 80 60 137 6100
Number of interneurons.

Top row: animal identifier. Left column: brain region.

Brain region ec012 ec013 ec014 ec016 f01_m g01_m gor01 i01_m j01_m pin01 vvp01 total
EC2 45 27 13 85
EC3 37 89 66 23 215
EC4 31 8 39
EC5 16 36 20 19 91
EC? 24 24
Total EC 53 201 113 63 24 454
CA1 205 90 46 19 13 8 14 3 22 420
CA3 4 174 14 2 4 198
DG 16 36 52
Unknown 1 1 6 8
Total 53 427 203 319 19 13 22 39 6 5 26 1132

To quantify the quality of spike sorting, for each neuron, we calculated an isolation distance 54 , an interspike interval index “R 2/10” 55 and a fraction of interspike intervals less than 2 msec 56 using the concatenated files described above. This information is provided in metadata tables included with the data set so that the user can identify sessions containing the desired cells based on these isolation quality measurements. An initial quality control filtering was done in selecting cells to include in the data set. Specifically, there were 7943 cells that were detected, but of those, only 7736 were included in the data set. 207 were not included because they were judged to have insufficient quality.

Our classification of principal neurons and interneurons is supported by short-term spike cross-correlogram and is consistent with previous reports 57– 59 . However, mis-classification of pyramidal cells and interneurons is inevitable to some extent by our methods. For example, certain types of interneurons with wider wave shapes (e.g., subgroups of somatostatin positive interneurons) might have been falsely classified as pyramidal cells by our method 60 . Examining the bursting properties of the putative pyramidal cells may help identifying these neurons. The cell-type classification method should be verified and refined by optogenetical tools in the future 60– 65 .

The tip of the probe either moved spontaneously relative to the brain or was moved by the experimenter between recording days to record from potentially different sets of neurons. However, we cannot exclude the possibility that some neurons recorded on different days were identical, because spikes recorded on each day were clustered separately, though in some instances neurons were recorded over multiple days. When we moved the electrodes, we waited for at least an hour before recording in order to stabilize the position of electrodes.

 Data description

The data are available 53 at CRCNS.org ( http://dx.doi.org/10.6080/K09G5JRZ). Details of the data collection, processing and storage of data into files are included with the data set, including scripts useful for processing the data 53 . Here, we briefly summarize the data description.

The number of cells recorded from each animal and brain region is shown in Table 2.

Most of the recorded cells were classified as principal neurons or interneurons. The number of cells classified as principal and interneuron are shown in Table 3 and Table 4.

The 8 types of behaviours (see Behavioural Testing section) were further subdivided into 14 behaviour subclasses based on minor differences (e.g. size of maze) and used as behaviour identifiers in the dataset ( Table 1).

The data were obtained during 442 recording sessions. During each session the animal performed one of the 14 behaviour subclasses. The number of recording sessions and behaviour subclasses used with each animal is shown in Table 5. The description of each behaviour subclass is given in Table 1.

Number of recording sessions.

Top row: animal identifier. Left column: behaviour subclass.

Behaviour subclass ec012 ec013 ec014 ec016 f01_m g01_m gor01 i01_m j01_m pin01 vvp01 total
bigSquare 24 45 4 13 1 4 91
bigSquarePlus 2 2
linear 18 90 2 9 119
linearOne 3 5 8
linearTwo 3 5 8
midSquare 4 8 2 14
Mwheel 28 16 8 14 8 7 8 89
Open 3 3
plus 11 11
sleep 19 10 1 30
Tmaze 2 3 1 6
wheel 40 8 9 1 58
wheel_home 2 2
ZigZag 1 1
Total 70 208 50 59 8 7 9 9 4 3 15 442

The 442 sessions with neural responses included in the data set have a total duration of 204.5 hours. They are a subset of 1,538 recording sessions that were used for the spike sorting and have a total duration of 547 hours. Most of the sessions for which neural responses are not included in the data set have behaviour “sleep”.

 Data file organization

The data files for each recording session are stored in separate compressed tar archive files (i.e. with extension “tar.gz”). These files are organized into top-level directories, each of which contains data for sessions recorded on the same day using the same animal and electrode placement combination. Data from all sessions recorded from the same animal on the same day were merged for spike sorting. All merged sessions are stored in the same top-level directory in the data set at CRCNS.org. Therefore, the cell identification numbers assigned by the spike sorting are common to all sessions within a top-level directory, and are not specific to individual sessions. Details of the file organization are provided in the document “CRCNS.org hc3 data description” which is included with the data set.

 Metadata organization

The metadata describing the data is stored in six tables that are included with the data set. Table cell has information about each spike sorted cell. Table session has information about the 442 experimental sessions that have data files included in the data set. Table session_a has information about all sessions (1,538) that were used to do spike sorting. Table spike_count has the number of spikes recorded from each cell in each of the 1,538 sessions. Table epos contains information about the position of the electrodes. And table file has information about the “.tar.gz” and video files that are included the data set.

These tables are provided in CSV (comma-separated values) format, Excel format, and as tables in an SQLite database. SQLite ( http://www.sqlite.org/) is a free, open source, SQL data base engine available for all common operating systems. Tables cell, session, session_a, epos and file are related to each other through the common field “topdir” which has the name of top-level directories described above. Table spike_count is related to tables cell, session, and session_a by the id field in those tables. The table fields are given in Listing 1 (except for session_a which is similar to session). Document “crcns-hc3-data-description” has examples showing how the SQLite command interface can be used with these tables to generate summary statistics from the metadata and to identify data files of interest (for example, find sessions with a maximum number of simultaneously recorded cells from a particular brain region that have a desired isolation characteristics) prior to downloading the data. Sessions of interest can also be identified using file “crcns-hc3-cell-counts.zip” which has tables giving the number of cells recorded from each region in each session (for both all cells and well isolated units) and also the sessions with the largest number of recorded cells from each region (for both all cells and well isolated).

Listing 1: Fields in metadata tables. Fields for each table are documented in the comments.

create table cell id integer, -- Id used to match original row number in MatLab PyrIntMap.Map matrix topdir string, -- top level directory containing data animal string, -- name of animal ele integer, -- electrode number clu integer, -- ID # in cluster files region string, -- brain region nexciting integer, -- number of cells this cell monosynaptically excited ninhibiting integer, -- number of cells this cell monosynaptically inhibited exciting integer, -- physiologically identified exciting cells based on CCG analysis inhibiting integer, -- physiologically identified inhibiting cells based on CCG analysis -- (Detailed method in Mizuseki Sirota Pastalkova and Buzsaki., 2009 Neuron paper.) excited integer, -- based on cross-correlogram analysis, the cell is monosynaptically excited by other cells inhibited integer, -- based on cross-correlogram analysis, the cell is monosynaptically inhibited by other cells fireRate real, -- meanISI=mean(bootstrp(100,'mean',ISI)); fireRate = SampleRate/MeanISI; ISI is interspike intervals. totalFireRate real, -- num of spikes divided by total recording length for a period during which the neuron was stably recorded. cellType string -- 'p'=pyramidal, 'i'=interneuron, 'n'=not assigned as pyramidal or interneuron eDist float, -- "isolation distance" (see Harris, Hirase, Leinekugel, Henze and Buzsaki, Neuron, 2001 54 ) RefracRatio float, -- This is an interspike interval index "R2/10" (in Fee, Mitra and Kleinfeld, Journal of -- Neuroscience Methods, 1996 55 ). R2/10 = (fraction of ISI < 2ms)/(fraction of ISI < 10 ms)*9.15/1.15 (our shortest -- interval between spikes allowed by our spike sorting method is 0.85 ms, (10-0.85)/(2-0.85) = 9.15/1.15) RefracViol float -- Fraction of interspike intervals less than 2 msec. ); create table session ( -- this is actually an SQL view on session_a, see crcns-hc3-data-description id integer, -- matches row in original MatLab Beh matrix topdir string, -- directory in data set containing data (tar.gz) files session string, -- individual session name (corresponds to name of tar.gz file having data) behavior string, -- one of: Mwheel, Open, Tmaze, Zigzag, bigSquare, bigSquarePlus, -- linear, linearOne, linearTwo, midSquare, plus, sleep, wheel, wheel_home familiarity integer, -- number of times animal has done task, 1=animal did task for first time, -- 2=second time, 3=third time, 10=10 or more duration real -- recording length in seconds ); create table file ( -- information about files in hc3 dataset topdir string, -- directory in data set containing data (tar.gz) files session string, -- individual session name (corresponds to name of tar.gz file having data) size integer, -- number of bytes in tar.gz file video_type string, -- 'mpg', 'm1v' or '-' (for no video file) video_size integer -- size of video file, or 0 if no video file ); create table epos ( -- has electrode positions for each top level directory -- Note, some regions do not match that in cell table. -- Those that differ have following meanings: -- DGCA3: not sure if the electrode is DG or CA3. -- Ctx: somewhere in the cortex (above the hippocampus) -- CA: somewhere in the hippocampus (do not know if it is CA1, CA3 or DG) topdir string, -- directory in data set containing data (tar.gz) file animal string, -- animal name e1 string, -- region for electrode 1 e2 string, -- region for electrode 2 -- ... (e3 through e15 fields not shown) e16 string -- region for electrode 16 ); create table spike_count ( -- contains number of spikes each cell has in each session (if cell could have fired). cellId integer, -- id in cell table (row in original MatLab PyrIntMap.Map) sessId integer, -- id in session table (row in original MatLab Beh table) nSpikes integer -- number of spikes for cell in the session );

Data availability

The data referenced by this article are under copyright with the following copyright statement: Copyright: � 2014 Mizuseki K et al.

CRCNS: Multiple single unit recordings from different rat hippocampal and entorhinal regions while the animals were performing multiple behavioral tasks, http://dx.doi.org/10.6080/K09G5JRZ 53

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 Acknowledgements

We thank Gautam Agarwal, Fritz Sommer, Kenneth Harris and members of the Buzsaki lab for support and discussions.

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Competing interests: No competing interests were disclosed.

 29 7 2014 Copyright: © 2014 Isomura Y 2014 This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. recommendation approve

I have no concerns on this paper. This is an excellent work that will be useful for many other researchers. I appreciate it.

Reviewer Expertise:

NA

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

 10.5256/f1000research.4171.r4603 Reviewer response for version 1 Knierim James 1 Referee Zanvyl Krieger Mind/Brain Institute and Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA

Competing interests: No competing interests were disclosed.

 7 5 2014 Copyright: © 2014 Knierim J 2014 This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. recommendation approve

This data set will be a valuable resource for investigators who wish to test hypotheses about hippocampal function and interaction with entorhinal cortex at the level of single unit and LFP physiology. I have not investigated the data base carefully to ensure its utility, as I assume the authors have done so. My comments are limited to a few questions about their F1000Research article describing the data base.

'Animal surgery' - second paragraph:

Do the authors mean "in the coronal plane?" It is not clear whether the tetrodes were angled medially or laterally in that plane, or whether the authors mean that the tetrodes were angled anteriorly or posteriorly to the coronal plane. Please clarify here and in other locations in the text how the tetrodes were angled.

'Animal surgery' - final paragraph:

Does the data base contain histological figures? If not, are they easily identifiable and accessible from published reports? It would be very useful to ensure that the precise location of tetrodes could be made available to investigators.

Table 1, ' elevated linear track':

Shouldn't the fixed angles be 74 degrees (i.e. +/- 37 degrees)?

' Behavioural testing'  item (5):

Were the rats motivated to run the corridors in any particular order?  Was there any working memory component to the trials?

Reviewer Expertise:

NA

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

 10.5256/f1000research.4171.r4604 Reviewer response for version 1 Maurer Andrew P. 1 Referee Division of Neural Systems Memory and Aging, University of Arizona, Tucson, AZ, USA

Competing interests: No competing interests were disclosed.

 6 5 2014 Copyright: © 2014 Maurer AP 2014 This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. recommendation approve

Mizuseki and colleagues provide a description of 442 datasets (more than 200 hours) of hippocampal  in vivo recordings. These datasets provide cell classification as well as the raw data, in case users wish to return to the high-sample traces and re-cluster the data on their own. The results of different analyses from the database have been published, although all analysis possibilities have not been exhausted. While this is an atypical review to write (as any suggestions on improvement to the database seem to be akin to looking a gift horse in the mouth), I am hoping the authors can discuss the ramifications of providing such an extensive database. While any database has limitations (e.g. sometimes determining the EEG units is a bit of an exercise with these data in the present format), it is perhaps more advantageous and constructive to discuss what the community can do to make the most use of it. As the authors state  “Community-driven data sharing may offer cross-validation of findings, refinement of interpretations and facilitate discoveries” and the challenges are now directed to those who are interested in participating in future analyses. In hopes that this will set-forth a new era of data-sharing, I hope that the authors can discuss their open database in a manner that parallels Giorgio Ascoli’s discussion on sharing neural reconstruction files (Ascoli, 2006). It should be noted that I do not expect the authors to have comprehensive answers to each of my comments below, but it might be beneficial if they would provide some initial thoughts to seed further discussion. Some points that the authors may wish to discuss include:

One barrier to sharing data is “the fear of being scooped” (Ascoli, 2006). For example, scientific progress will be dramatically increased through parallel (and hopefully, collaborative) data analysis. Are the authors concerned about being “scooped”? What about a group of researchers unknowingly using the database to conduct an analysis that is also a student’s PhD project? This hypothetical student may still be acquiring the expertise to keep pace with more seasoned researchers.

“An often unspoken resistance to the sharing… data is born out of concern for criticisms and mistakes” (Ascoli, 2006). This is an unprecedented event that Mizuseki and colleagues have set forth, by providing a comprehensive catalog of data in an unabashed manner. The first point I want to touch upon is the level of raw exposure in releasing data. I have never met a neuroscientist who believes that anyone else could’ve conducted their analyses better than themselves (save a modest few), but to find those who believe that the authors “didn’t look for the right thing” could make up a small battalion. Mizuseki and colleagues invite critics to their doorstep. Perhaps this is more similar to posing nude as a model for artist. By placing data online, it comes with judgment and the potential to be proved wrong. What do the authors believe the convention is if others follow in their footsteps? For example, if group A shares their database after publishing their results, group B downloads and analyzes their data in new light and finds the opposite results, what is the appropriate manner in handling the situation? The self-correction aspect of science is also accelerated when data is openly-shared. It remains to be seen how situations like this should/will be handled. 

There is also a chance for the data to be used in order to stifle or impede publication when the result is dubious. That is, should it be considered “fair-play” for a reviewer to use the same database and conduct a similar analysis with results that contradict a submitted manuscript’s results? A tactic such as this only seems appropriate in “open-review formats”.

“A final barrier to sharing digital reconstructions relates to the reluctance to lose or give a competitive edge” (Ascoli, 2006). The release of this immense database will surely be the stronghold of many new assistant professors who are still in the initial stages of setting up a physiology laboratory. Moreover, I can see these data being used in laboratories that are heavily analysis driven and limited in their own capacity for high-density  in vivo recordings. This increase in the number of people analyzing data invites competitors for the authors as well as their neutral peers. Sheer logic dictates that the authors are not afraid of competition (otherwise, why share the data? Please note that I am a cynic and have been taught by many reviewers that “scientific altruism” is as abundant as snarks and unicorns). Why should researchers not be afraid of others using this database to compete?  Is it believed that these data will be used for collaboration? What can be done to emphasize collaboration across laboratories when using the database? How is authorship handled when multiple groups use these data? If I spend my time analyzing these data, only to have it published under a “group project name” (similar to Sir William Timothy Gowers’ Polymath project), do I put it on my CV?

The paper explicitly states that large downloads are prohibited. Does this mean that I should not download all the data? Is it OK to use these data for a class project? If so, is it more appropriate for the professor to disseminate it to the students or should the students make their own CRCNS account? Finally, more of an afterthought but along similar lines: should there be a collaborative processing code library that should be developed and maintained in parallel with the use of these data (similar to GitHub or SourceForge)? 

  

I absolutely do not expect the authors to have complete answers to these questions nor should they carry the sole responsibility of determining the general conventions of what constitutes use versus misuse, but I do think that it is worth hearing their general thoughts. As this is the largest and most comprehensive database of  in vivo hippocampal and entorhinal physiology to become available to the general scientific community, there will be an immense ramification. Scientific replication/external validation is an immediate and positive application of this database. As I have cited Timothy Gowers above, I think it would be best to leave off with his opinion of open data-sharing and collaboration: “It feels as though this process is to normal research as driving is to pushing a car.” ( http://gowers.wordpress.com/2009/02/01/questions-of-procedure/).

As a field we have the opportunity to compete or collaborate. I hope that these data facilitate cross-laboratory collaboration where two groups are reticent to share their own data. For those that are interested in embracing the collaborative spirit, the CRCNS website also has a “marketplace” section where ideas and potential collaborations can be discussed. Finally, I applaud the authors for this unprecedented act of scientific altruism. I hope this will be a platform that accelerates our understanding of the entorhinal-hippocampal circuitry through collaboration.

Reviewer Expertise:

NA

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

 10.5256/f1000research.4171.r4607 Reviewer response for version 1 Sakata Shuzo 1 Referee Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow, UK

Competing interests: No competing interests were disclosed.

 6 5 2014 Copyright: © 2014 Sakata S 2014 This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. recommendation approve

This is an important report for the neuroscience community regarding huge data sets recorded from the dorsal hippocampus and dorsomedial entorhinal cortex of behaving rats. Because the authors have already published a number of papers with the data sets, I have no doubt that this paper and their shared data will contribute to the further advancement of this field.  

This manuscript is clearly written in details. This article can be improved by clarifying the following minor points in the section Data collection and cell-type classification:

1. Cluster quality

It is not clear whether the quality of single units was assessed objectively, for example, by measuring isolation distance.

2. Cell-type classification

Because now researchers including the authors can classify cell-types optogenetically, it would be better to comment on potential pitfalls of the classification procedure used here. For example, it is difficult to exclude the possibility that some of “principal” neurons can be interneurons.

Reviewer Expertise:

NA

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

 10.5256/f1000research.4171.r4602 Reviewer response for version 1 Isomura Yoshikazu 1 Referee Brain Science Institute, Tamagawa University, Tokyo, Japan

Competing interests: No competing interests were disclosed.

 6 5 2014 Copyright: © 2014 Isomura Y 2014 This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. recommendation approve

In this work, Mizuseki et al. provide valuable information on their large-scale data sets of multi-neuronal and local field potential (LFP) recordings from the hippocampus (dentate gyrus, CA3, and CA1) as well as the enthorhinal cortex across the layers (layers 2, 3, 4, 5 etc.) of behaving rats. These data sets have originally been used for a number of their excellent studies for past ten years. Here, they fully summarized the experimental conditions and results in individual recording sessions very clearly for any users to plan to analyze the data.  It will be a really useful treasure map for all hippocampus researchers.

I have one minor comment. While they showed the number of isolated neurons in each brain area of each animal (Table 2 to Table 4), it is not clear yet how many neurons, at most, were recorded simultaneously.  Some people will probably want to analyze spike activity in a population of many neurons. The data would be more available for the higher-order spike analysis if the authors added additional information on the best (or first choice) data set with a sufficient number of well-isolated neurons in the same brain area.

Reviewer Expertise:

NA

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.