Introduction
The hippocampus and entorhinal cortex are essential structures for memory and spatial navigation1–8. Position-tuned cells (‘place cells’) are present in CA1, CA3 and dentate gyrus regions1,9. Grid cells, head direction cells, and border cells have been described in the dorsomedial entorhinal cortex, and are critical ingredients of navigation systems5,7,8,10–13. The temporal coordination across the entorhinal cortex and hippocampus is secured by various oscillations, especially theta, gamma and sharp wave ripples14–21.
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 papers6,21–27.
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 dataset6,21–41. 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.
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 Speciality 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 detail42,43. 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: at a 35 degree angle to coronal plane, centered on 2.8 mm posterior and 2.6 mm lateral to bregma. CA1: 26.5 degree angle to vertical, at a 35 degree angle to coronal, centered on 4.6 mm posterior and 2.4 mm lateral to bregma; rat vvp01: CA3: at a 26.5 degree angle to coronal plane, centered on 2.8 mm posterior and 2.6 mm lateral to bregma. CA1: 26.5 degree angle to vertical, parallel to sagittal plane, centered on 4.4 mm posterior and 2.3 mm lateral to bregma; rat gor01: CA3: at a 26.5 degree angle to coronal plane, centered on 3.1 mm posterior, and 3.0 mm lateral to bregma. CA1: 26.5 degree angle to vertical, at a 45 degree angle to coronal plane, 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 layers21 (4.5 mm lateral from the midline; 0.1 mm anterior to the edge of the transverse sinus at a 20–25 degree 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 degrees parasagittal), positioned centrally at 3.5 mm posterior from bregma and 2.5 mm lateral from the midline.
For all silicon probes used, each shank had eight recording sites (160 µm2 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)44,45. 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 detail21,24.
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).
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 trials23,24 (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 36.9 degree 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., 200921. |
alternation task in T-maze | Mwheel | Alternation task in T-maze (100 cm × 120 cm) with wheel running delay. See Pastalkova et al., 20086 |
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., 201046. |
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. |
(1) On an elevated linear track (250 cm × 7 cm), the animals were required to run back and forth to obtain water reward at both ends21. 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 trials23,24.
(2) 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 platform21 (180 cm × 180 cm, 120 cm × 120 cm or 100 cm × 200 cm).
(3) 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 reinforcement21.
(4) 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 one6.
(5) In the elevated plus maze (100 cm × 100 cm), the rats were motivated to run to the ends of four corridors, where water was given every 30 s.
(6) 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 well21,22,25,46.
(7) 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.
(8) 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 described21,24,42. 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’) neurons47, clustering was performed on concatenated files of several behavioural and sleep sessions recorded at the same electrode position on the same recording day22,25–27. We made extensive use of publicly available analytical and display programs, which were developed in our laboratory (KlustaKwik48 available at http://sourceforge.net/projects/klustakwik/, Neuroscope49 available at http://neuroscope.sourceforge.net/, Klusters49 available at http://klusters.sourceforge.net/, NDmanager49 available at http://ndmanager.sourceforge.net/). The latest available version at the time was used in each case. Spike sorting was performed automatically, using KlustaKwik48, followed by manual adjustment of the clusters, with the help of autocorrelogram, cross-correlogram and spike wave-shape similarity matrix (Klusters software package49). Because none of the existing spike sorting algorithms is completely automated, manual adjustment is necessary48. This inevitably leads to some operator-dependent variability48; 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 interactions6,17,21,24,42. Classification of principal neurons and interneurons of entorhinal cortical neurons was based on waveforms and short-term monosynaptic interactions, and described previously in detail21. 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).
Table 2. 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 |
Table 3. 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 |
Table 4. 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 |
Table 5. 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 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 available50 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 data50. 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.
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 four tables that are included with the data set. Table cell has information about each spike sorted cell. Table session has information about each experimental session. Table epos contains information about the position of the electrodes. And table file has information about the “.tar.gz” and other files that are in 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. These tables are related to each other through a field (named “topdir”), which has the name of top-level directories described above and is common to all four tables. The fields in each of these tables are listed in Listing 1. As described in file “CRCNS.org hc3 data description” the SQLite command interface can be used with these tables to generate summary statistics from the metadata and to locate data files that satisfy particular search criteria (for example, find data for cells of a specific type from a particular brain region and experimental behaviour).
Listing 1: Create table statements for tables: cell, session, file and epos. Fields for each of these tables 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
cellType string -- 'p'=pyramidal, 'i'=interneuron, 'n'=not assigned as pyramidal or
interneuron
);
create table session (
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 string, -- region for electrode 3
e4 string, -- region for electrode 4
-- ... (e5 through e14 fields not shown)
e15 string, -- region for electrode 15
e16 string -- region for electrode 16
);
Data availability
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
Terms of data usage: Data on this site is made available only for scientific purposes. Redistribution of the data is not permitted. Any publications derived from the data must cite the data contributors and CRCNS.org as being the source of the data and the original paper(s) that generated the data. Unnecessary downloading of large data files is not permitted. (To minimize demands on the server, only data expected to be useful for your scientific purposes should be downloaded).
Privacy notice: Occasionally the researchers who contribute data wish to know who has downloaded their data. Upon request we will provide this information to the data contributors. So, if you download data, there is a possibility that your name and email address will be provided to the data contributor. We request that the data contributors only use the information for legitimate scientific purposes (such as determining the frequency of downloads, or contacting users to providing updated information about the data or to explore possible collaborations).
Author contributions
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.
Grant information
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), NIH 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.
Acknowledgements
We thank Gautam Agarwal, Kenneth Harris and members of the Buzsaki lab for support and discussions.
References
- 1.
O’Keefe J, Nadel L:
The Hippocampus as a Cognitive Map (Oxford: Oxford University Press). 1978. Reference Source
- 2.
Squire LR:
Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans.
Psychol Rev.
1992; 99(2): 195–231. PubMed Abstract
| Publisher Full Text
- 3.
Eichenbaum H, Dudchenko P, Wood E, et al.:
The hippocampus, memory, and place cells: is it spatial memory or a memory space?
Neuron.
1999; 23(2): 209–226. PubMed Abstract
| Publisher Full Text
- 4.
Buzsaki G:
Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory.
Hippocampus.
2005; 15(7): 827–840. PubMed Abstract
| Publisher Full Text
- 5.
McNaughton BL, Battaglia FP, Jensen O, et al.:
Path integration and the neural basis of the ‘cognitive map’.
Nat Rev Neurosci.
2006; 7(8): 663–678. PubMed Abstract
| Publisher Full Text
- 6.
Pastalkova E, Itskov V, Amarasingham A, et al.:
Internally generated cell assembly sequences in the rat hippocampus.
Science.
2008; 321(5894): 1322–1327. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 7.
Buzsaki G, Moser EI:
Memory, navigation and theta rhythm in the hippocampal-entorhinal system.
Nat Neurosci.
2013; 16(2): 130–138. PubMed Abstract
| Publisher Full Text
- 8.
Moser EI, Moser MB:
Grid cells and neural coding in high-end cortices.
Neuron.
2013; 80(3): 765–774. PubMed Abstract
| Publisher Full Text
- 9.
O‘Keefe J, Dostrovsky J:
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat.
Brain Res.
1971; 34(1): 171–175. PubMed Abstract
| Publisher Full Text
- 10.
Hafting T, Fyhn M, Molden S, et al.:
Microstructure of a spatial map in the entorhinal cortex.
Nature.
2005; 436(7052): 801–806. PubMed Abstract
| Publisher Full Text
- 11.
Sargolini F, Fyhn M, Hafting T, et al.:
Conjunctive representation of position, direction, and velocity in entorhinal cortex.
Science.
2006; 312(5774): 758–762. PubMed Abstract
| Publisher Full Text
- 12.
Solstad T, Boccara CN, Kropff E, et al.:
Representation of geometric borders in the entorhinal cortex.
Science.
2008; 322(5909): 1865–1868. PubMed Abstract
| Publisher Full Text
- 13.
Savelli F, Yoganarasimha D, Knierim JJ:
Influence of boundary removal on the spatial representations of the medial entorhinal cortex.
Hippocampus.
2008; 18(12): 1270–1282. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 14.
Buzsaki G, Horvath Z, Urioste R, et al.:
High-frequency network oscillation in the hippocampus.
Science.
1992; 256(5059): 1025–1027. PubMed Abstract
| Publisher Full Text
- 15.
O‘Keefe J, Recce ML:
Phase relationship between hippocampal place units and the EEG theta rhythm.
Hippocampus.
1993; 3(3): 317–330. PubMed Abstract
| Publisher Full Text
- 16.
Bragin A, Jando G, Nadasdy Z, et al.:
Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat.
J Neurosci.
1995; 15(1 Pt 1): 47–60. PubMed Abstract
- 17.
Skaggs WE, McNaughton BL, Wilson MA, et al.:
Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences.
Hippocampus.
1996; 6(2): 149–172. PubMed Abstract
| Publisher Full Text
- 18.
Buzsaki G:
Theta oscillations in the hippocampus.
Neuron.
2002; 33(3): 325–340. PubMed Abstract
| Publisher Full Text
- 19.
Buzsaki G:
Rhythms of the Brain (New York: Oxford University Press). 2006. Reference Source
- 20.
Buzsaki G, Wang XJ:
Mechanisms of gamma oscillations.
Annu Rev Neurosci.
2012; 35: 203–225. PubMed Abstract
| Publisher Full Text
- 21.
Mizuseki K, Sirota A, Pastalkova E, et al.:
Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop.
Neuron.
2009; 64(2): 267–280. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 22.
Mizuseki K, Diba K, Pastalkova E, et al.:
Hippocampal CA1 pyramidal cells form functionally distinct sublayers.
Nat Neurosci.
2011; 14(9): 1174–1181. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 23.
Diba K, Buzsaki G:
Forward and reverse hippocampal place-cell sequences during ripples.
Nat Neurosci.
2007; 10(10): 1241–1242. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 24.
Diba K, Buzsaki G:
Hippocampal network dynamics constrain the time lag between pyramidal cells across modified environments.
J Neurosci.
2008; 28(50): 13448–13456. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 25.
Mizuseki K, Royer S, Diba K, et al.:
Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons.
Hippocampus.
2012; 22(8): 1659–1680. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 26.
Mizuseki K, Buzsaki G:
Preconfigured, skewed distribution of firing rates in the hippocampus and entorhinal cortex.
Cell Rep.
2013; 4(5): 1010–1021. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 27.
Mizuseki K, Buzsaki G:
Theta oscillations decrease spike synchrony in the hippocampus and entorhinal cortex.
Philos Trans R Soc Lond B Biol Sci.
2014; 369(1635): 20120530. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 28.
Belluscio MA, Mizuseki K, Schmidt R, et al.:
Cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus.
J Neurosci.
2012; 32(2): 423–435. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 29.
Geisler C, Diba K, Pastalkova E, et al.:
Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus.
Proc Natl Acad Sci U S A.
2010; 107(17): 7957–7962. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 30.
Grosmark AD, Mizuseki K, Pastalkova E, et al.:
REM sleep reorganizes hippocampal excitability.
Neuron.
2012; 75(6): 1001–1007. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 31.
Isomura Y, Sirota A, Ozen S, et al.:
Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations.
Neuron.
2006; 52(5): 871–882. PubMed Abstract
| Publisher Full Text
- 32.
Itskov V, Pastalkova E, Mizuseki K, et al.:
Theta-mediated dynamics of spatial information in hippocampus.
J Neurosci.
2008; 28(23): 5959–5964. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 33.
Itskov V, Curto C, Pastalkova E, et al.:
Cell assembly sequences arising from spike threshold adaptation keep track of time in the hippocampus.
J Neurosci.
2011; 31(8): 2828–2834. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 34.
Kempter R, Leibold C, Buzsaki G, et al.:
Quantifying circular-linear associations: hippocampal phase precession.
J Neurosci Methods.
2012; 207(1): 113–124. PubMed Abstract
| Publisher Full Text
- 35.
Schmidt R, Diba K, Leibold C, et al.:
Single-trial phase precession in the hippocampus.
J Neurosci.
2009; 29(42): 13232–13241. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 36.
Sullivan D, Csicsvari J, Mizuseki K, et al.:
Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity.
J Neurosci.
2011; 31(23): 8605–8616. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 37.
Sullivan D, Mizuseki K, Sorgi A, et al.:
Comparison of sleep spindles and theta oscillations in the hippocampus.
J Neurosci.
2014; 34(2): 662–674. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 38.
Schomburg EW, Anastassiou CA, Buzsaki G, et al.:
The spiking component of oscillatory extracellular potentials in the rat hippocampus.
J Neurosci.
2012; 32(34): 11798–11811. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 39.
Taxidis J, Mizuseki K, Mason R, et al.:
Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model.
Front Comput Neurosci.
2013; 7: 3. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 40.
Stevenson IH, London BM, Oby ER, et al.:
Functional connectivity and tuning curves in populations of simultaneously recorded neurons.
PLoS Comput Biol.
2012; 8(11): e1002775. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 41.
Buzsaki G, Mizuseki K:
The log-dynamic brain: how skewed distributions affect network operations.
Nat Rev Neurosci.
2014; 15(4): 264–78. PubMed Abstract
| Publisher Full Text
- 42.
Csicsvari J, Hirase H, Czurko A, et al.:
Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat.
J Neurosci.
1999; 19(1): 274–287. PubMed Abstract
- 43.
Vandecasteele M, Royer MS, Belluscio S, et al.:
Large-scale recording of neurons by movable silicon probes in behaving rodents.
J Vis Exp.
2012; (61): e3568. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 44.
Csicsvari J, Henze DA, Jamieson B, et al.:
Massively parallel recording of unit and local field potentials with silicon-based electrodes.
J Neurophysiol.
2003; 90(2): 1314–1323. PubMed Abstract
| Publisher Full Text
- 45.
Fujisawa S, Amarasingham A, Harrison MT, et al.:
Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex.
Nat Neurosci.
2008; 11(7): 823–833. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 46.
Royer S, Sirota A, Patel J, et al.:
Distinct representations and theta dynamics in dorsal and ventral hippocampus.
J Neurosci.
2010; 30(5): 1777–1787. PubMed Abstract
| Publisher Full Text
| Free Full Text
- 47.
Thompson LT, Best PJ:
Place cells and silent cells in the hippocampus of freely-behaving rats.
J Neurosci.
1989; 9(7): 2382–2390. PubMed Abstract
- 48.
Harris KD, Henze DA, Csicsvari J, et al.:
Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements.
J Neurophysiol.
2000; 84(1): 401–414. PubMed Abstract
- 49.
Hazan L, Zugaro M, Buzsaki G:
Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization.
J Neurosci Methods.
2006; 155(2): 207–216. PubMed Abstract
| Publisher Full Text
- 50.
Mizuseki K, Sirota A, Pastalkova E, et al.:
Multiple single unit recordings from different rat hippocampal and entorhinal regions while the animals were performing multiple behavioral tasks. CRCNS org. 2013. http://dx.doi.org/10.6080/K09G5JRZ. Data Source
Comments on this article Comments (0)