Task-dependent encoding of space and events by striatal neurons is dependent on neural subtype

Abstract

The dorsal striatum plays a critical role in procedural learning and memory. Current models of basal ganglia assume that striatal neurons and circuitry are critical for the execution of overlearned, habitual sequences of action. However, less is known about how the striatum encodes task information that guides the performance of actions in procedural tasks. To explore the striatal encoding of task information, we compared the behavioral correlates of striatal neurons tested in two tasks: a multiple T-maze task in which reward delivery was entirely predictable based on spatial cues (the Multiple-T task), and a task in which rats ran on a rectangular track, but food delivery depended on the distance traveled on the track and was not dependent solely on spatial location (the Take-5 task). Striatal cells recorded on these tasks were divisible into three cell types: phasic-firing neurons (PFNs), tonically firing neurons (TFNs), and high-firing neurons (HFNs) and similar proportions of each cell type were found in each task. However, the behavioral correlates of each cell type were differentially sensitive to the type of task rats were performing. PFNs were responsive to specific task-parameters on each task. TFNs showed reliable burst-and-pause responses following food delivery and other events that were consistent with tonically active neurons (TANs) on the Take-5 (non-spatial) task but not on the Multiple-T (spatial) task. HFNs showed spatial oscillations on the Multiple-T (spatial) task but not the Take-5 (non-spatial) task. Reconstruction of the rats' position on the maze was highly accurate when using striatal ensembles recorded on the Multiple-T (spatial) task, but not when using ensembles recorded on the Take-5 (non-spatial) task. In contrast, reconstruction of time following food delivery was successful in both tasks. The results indicated a strong task dependency of the quality of the spatial, but not the reward-related, striatal representations on these tasks. These results suggest that striatal spatial representations depend on the degree to which spatial task-parameters can be unambiguously associated with goals.

Figure 1

Schematic of the Multiple-T (top) and Take-5 (bottom) tasks.

Figure 2

Sampling behavior on the Take 5 task. A: Average sampling traces from food ports on the Take 5 task in the 6 seconds following arrival at the food delivery locations. When no reward was delivered (Unrewarded), rats did not sample the food ports, while on normal trials (Tone+/Food+), rats began sampling the food ports approximately 1 second after arrival in the vicinity of the appropriate food delivery location. On probe trials, sampling behavior was similar to normal trials when either the tone (Tone−/Food+) or food delivery (Tone+/Food−) was omitted. Critically, rats also were likely to sample the food port when both sensory cues were omitted (Tone−/Food−), though sampling behavior on these probe trials was more variable. All sampling plots are to the same scale. B: Comparison of each trial type (averaged across the 6 second window shown in A). Robust sampling was seen for normal trials (Tone+/Food+) and probe trials in which at least one sensory cue was presented (Tone−/Food+ and Tone+/Food− probe trials). Weaker sampling was seen for probe trials in which both sensory cues were omitted (Tone−/Food−), but rat still sampled the food ports more than for Unrewarded arrivals. Error bars represent mean and 95% confidence intervals calculated across all Take 5 sessions.

Figure 3

Recording locations verified histologically. Shown separately are final tetrode locations from ten animals implanted with hyperdrives over the dorsal striatum. Final tetrode positions are marked by x’s, and all tetrode locations have been mapped to the nearest of the three coronal sections shown. Tetrodes were observed in a region extending approximately −0.5 to 1.5 mm anterior/posterior relative to bregma. Diagrams adapted from (Paxinos and Watson 1998). The final recording marks for one Take-5 rat included some ventral striatal locations. Removing this rat from our analyses does not qualitatively change our results. We have included this rat in the analyses because most of the cells recorded from this rat were recorded early (i.e. in the more dorsal zone).

Figure 4

Classification of striatal firing patterns. A: Measuring PropISIs > 2 seconds and postspike suppresion, striatal spike trains separate into three discernable categories: phasic firing neurons (PFNs), tonic firing neurons (TFNs), and high firing neurons (HFNs). B: The average waveforms of each category differ, with PFNs being preferentially biphasic, HFNs preferentially triphasic, and TFNs preferentially inverted. Scalebar shows 1 ms. C: The autocorrelation function, showing the strong post-spike suppression of TFNs. D: Sample spike trains from each category, showing the bouts and silence of PFNs, the variability with high-firing times of HFNs, and the steady firing of TFNs. Scalebar shows 1 second.

Figure 5

PFN responses. A, B: example cells from the Multiple-T task. (A: a neuron turned to the spatial/sequence component of the task; B: a neuron tuned to the reward component of the task). C–E: Example cells from the Take-5 task. (C: a reward-related neuron. D: a neuron tuned to the spatial/sequence component of the task. Note that this neuron shows tuning both to spatial location as well as the sequential component.) Note: the apparent spatial/sequence tuning of the neurons in A&C is due to the firing of these neurons following reward-delivery. These neurons did not continue to fire at high rates while the rats sat at these locations, and the neuron in C from the Take-5 task did not fire in a given spatial location if the rat ran past a pellet dispenser that was not rewarded. E: two tuning curves showing tuning to both space, sequence, and the cross-product (space × sequence). In the bottom panel, the response of each neuron is shown to three conditions (top) the spatial journey to each feeder (1–4), (middle) the sequence around the five feeder journeys (1–5), and (bottom) the cross product. In the cross-product, each column shows spatial location (1–4, repeated) and each row shows a sequence (12341, 23412, etc.). Each PFN showed tuning to both spatial location and sequence.

Figure 6

TFN responses. A: TFN with short latency excitations following the presentation of the food-predictive tone on the Take 5 task. The left plot shows the average waveform, interspike-interval histogram and autocorrelation, while the right plot shows the raster-plot and firing rate histogram in a ± 1 second window surrounding cue/food delivery onset. B: Population responses of TFNs to reward-predictive cues. Average population responses of TFNs aligned to either food-delivery on the Multiple-T task (left) and a tone predicting food delivery in the Take-5 task (right). Panels in which there was a significant population response in the 500 ms following event onset are marked with asterisks.

Figure 7

HFN responses. A–C: Example HFN from the Multiple-T task. A: Average waveform. B: Spatial firing rate map. Color panel indicates firing rate as a function of position, with blue representing low firing rates and red representing high firing rates. C: Rastergrams. Top: linearized spatial rastergram. Note the spatial consistency of the oscillation (the rat ran at different speeds on each lap). These oscillations were not well-aligned temporally across all trials when arranged relative to when the rat arrived at the first food delivery site (Middle) or to when the rat started the trial (by leaving the second food delivery site, Bottom). There was a 3 Hz frequency in the temporal autocorrelation, but which was reset spatially on each lap. D: Population statistics. A significant increase at 3 Hz power was seen on Multiple-T but not the Take-5.

Figure 8

Ensemble reconstruction. A: Spatial reconstruction accuracy as a function of ensemble size of PFNs. Only on the Multiple-T, was there a significant increase in accuracy with increasing ensemble size. B: Reward-delivery reconstruction accuracy as a function of ensemble size. Striatal ensembles showed reliable representations of reward-delivery on both tasks.