Hippocampus Leads Ventral Striatum in Replay of Place-Reward Information methods
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Subjects
Four male Wistar rats (375-425 g; Harlan) were individually housed under a 12/12-h alternating light-dark cycle with light onset at 8:00 am. All experiments were conducted in the animal's inactive period. During training and recording periods, rats had access to water during a 2-h period following the experimental session, whereas food was available ad libitum. Rats were chronically implanted with a microdrive containing five individually movable tetrodes directed to the dorsal hippocampal CA1 area (4.0 mm posterior and 2.5 mm lateral to bregma) and seven to the VS (1.8 mm anterior and 1.4 mm lateral to bregma). Reference electrodes were placed in the corpus callosum dorsal to the HC, and near the hippocampal fissure. A skull screw inserted in the caudal part of the parietal skull bone served as ground.
Histology
Recordings of hippocampal CA1 neurons were made from 103 locations between 2.6 mm and 4.8 mm posterior and between 1.2 mm to 2.8 mm lateral to bregma compared to an atlas of the rat brain. Ventral striatal tetrodes were situated between approximately 2.2 and 1.2 mm anterior to bregma and between 1.6 and 3.0 mm laterally. From a total of 140 recording sites, 58% was estimated to be situated in the core region and 42% in the shell region of the VS. Although most sessions were likely to contain recordings from both the core and shell region, six sessions were identified to contain core-only recordings. No gross differences were observed in the number, firing rate, or appearance of behavioral correlates that were estimated to be recorded from the core and the shell region. Moreover, cross-regional reactivation was observed for the core-only sessions, with EV and REV values similar to tho...
Resting State and Sleep Phase Identification
Pre- and postbehavioral rest episodes included all periods of at least 20 s in which the rat was in the flower pot and remained motionless; i.e., episodes of movement were excluded from analysis. Within these periods of rest, episodes of SWS were characterized by the presence of large irregular activity and the occurrence of sharp wave-ripple complexes in the LFP of the CA1 pyramidal layer,. Ripples were detected each time the squared amplitude of the filtered LFP trace (100-300 Hz) crossed a threshold of 3.5 standard deviations (SD) for at least 25 ms. Because incidentally short periods of quiet wakefulness may have been included in SWS episodes, as these two phases share principal LFP characteristics, this state is referred to as quiet wakefulness-slow-wave sleep (QW-SWS). REM sleep periods were indicated by an elevated ratio (>0.4) of spectral density in the theta ban...
Quantification of Reactivation
The assessment of covariation in firing rates and reactivation within an experimental session with the EV method was previously described,,,. The temporal correlation between the firing patterns of two neurons was expressed in a Pearson's correlation coefficient that was computed for all concurrently recorded cell pairs using binned spike trains (50-ms bin size) of each rest/active episode. For assessment of cross-structural reactivation, pairs always consisted of one hippocampal and one ventral striatal cell; i.e., intra-area pairs were not taken into account. Separate analyses were conducted to examine intra-area reactivation; see and. All Pearson correlation coefficients of a particular episode (i.e., prebehavioral rest, track running, and postbehavioral rest) were assembled into a single matrix, and the similarity between the matrices was determined by computing a correlation...
Theta-Modulated Firing
Modulation of a cell's firing pattern to the theta oscillation was determined by first filtering LFP traces recorded from the hippocampal fissure and the VS using a Chebyshev type-1 bandpass filter between 6 and 10 Hz. Binned spikes (10°/bin) were then plotted relative to the theta peaks of two successive theta periods. The spike distribution was considered nonuniform when the Rayleigh score was <1 × 10 -5. The phase angle of the spikes was determined by computing the Hilbert transform of the filtered theta signal. Firing of a unit was considered as being modulated by the theta rhythm when shuffling of the spikes abolished the nonuniformity of the spike firing distribution as assessed with the Rayleigh score.
Identification of Place Fields
To characterize spatially selective firing fields, instantaneous firing rates were computed for bins of 50 ms. The spatial position of the rat's head was determined by creating a one-dimensional representation of the track and using a resolution of 2.3 cm. Mutual information was computed between the binned spike trains and the position, and corrected for finite sampling size,. A cell was considered to express a place field if its firing rate during track running was at least 0.3 Hz and if it carried at least 0.25 bits/spike of spatial information.
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Evidence quotes (6)
Four male Wistar rats (375-425 g; Harlan) were individually housed under a 12/12-h alternating light-dark cycle with light onset at 8:00 am. All experiments were conducted in the animal's inactive period. During training and recording periods, rats had access to water during a 2-h period following the experimental session, whereas food was available ad libitum. Rats were chronically implanted with a microdrive containing five individually movable tetrodes directed to the dorsal hippocampal CA1 area (4.0 mm posterior and 2.5 mm lateral to bregma) and seven to the VS (1.8 mm anterior and 1.4 mm lateral to bregma). Reference electrodes were placed in the corpus callosum dorsal to the HC, and near the hippocampal fissure. A skull screw inserted in the caudal part of the parietal skull bone served as ground.
Recordings of hippocampal CA1 neurons were made from 103 locations between 2.6 mm and 4.8 mm posterior and between 1.2 mm to 2.8 mm lateral to bregma compared to an atlas of the rat brain. Ventral striatal tetrodes were situated between approximately 2.2 and 1.2 mm anterior to bregma and between 1.6 and 3.0 mm laterally. From a total of 140 recording sites, 58% was estimated to be situated in the core region and 42% in the shell region of the VS. Although most sessions were likely to contain recordings from both the core and shell region, six sessions were identified to contain core-only recordings. No gross differences were observed in the number, firing rate, or appearance of behavioral correlates that were estimated to be recorded from the core and the shell region. Moreover, cross-regional reactivation was observed for the core-only sessions, with EV and REV values similar to those observed for other sessions. Therefore, core and shell recordings were pooled.
Pre- and postbehavioral rest episodes included all periods of at least 20 s in which the rat was in the flower pot and remained motionless; i.e., episodes of movement were excluded from analysis. Within these periods of rest, episodes of SWS were characterized by the presence of large irregular activity and the occurrence of sharp wave-ripple complexes in the LFP of the CA1 pyramidal layer,. Ripples were detected each time the squared amplitude of the filtered LFP trace (100-300 Hz) crossed a threshold of 3.5 standard deviations (SD) for at least 25 ms. Because incidentally short periods of quiet wakefulness may have been included in SWS episodes, as these two phases share principal LFP characteristics, this state is referred to as quiet wakefulness-slow-wave sleep (QW-SWS). REM sleep periods were indicated by an elevated ratio (>0.4) of spectral density in the theta band (6-10 Hz) to the overall power of the LFP trace recorded near the hippocampal fissure. Their borders were refined upon visual inspection of the trace.
The assessment of covariation in firing rates and reactivation within an experimental session with the EV method was previously described,,,. The temporal correlation between the firing patterns of two neurons was expressed in a Pearson's correlation coefficient that was computed for all concurrently recorded cell pairs using binned spike trains (50-ms bin size) of each rest/active episode. For assessment of cross-structural reactivation, pairs always consisted of one hippocampal and one ventral striatal cell; i.e., intra-area pairs were not taken into account. Separate analyses were conducted to examine intra-area reactivation; see and. All Pearson correlation coefficients of a particular episode (i.e., prebehavioral rest, track running, and postbehavioral rest) were assembled into a single matrix, and the similarity between the matrices was determined by computing a correlation coefficient for each of the three possible combinations of rest/active episodes. These matrix-based correlation values were used to assess which proportion of the variance in the postbehavioral correlation pattern can be explained by the pattern established during track running while controlling fo...
Modulation of a cell's firing pattern to the theta oscillation was determined by first filtering LFP traces recorded from the hippocampal fissure and the VS using a Chebyshev type-1 bandpass filter between 6 and 10 Hz. Binned spikes (10°/bin) were then plotted relative to the theta peaks of two successive theta periods. The spike distribution was considered nonuniform when the Rayleigh score was <1 × 10 -5. The phase angle of the spikes was determined by computing the Hilbert transform of the filtered theta signal. Firing of a unit was considered as being modulated by the theta rhythm when shuffling of the spikes abolished the nonuniformity of the spike firing distribution as assessed with the Rayleigh score.
To characterize spatially selective firing fields, instantaneous firing rates were computed for bins of 50 ms. The spatial position of the rat's head was determined by creating a one-dimensional representation of the track and using a resolution of 2.3 cm. Mutual information was computed between the binned spike trains and the position, and corrected for finite sampling size,. A cell was considered to express a place field if its firing rate during track running was at least 0.3 Hz and if it carried at least 0.25 bits/spike of spatial information.
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