Cortical neural responses to previous trial outcome during learning of a directional choice task

Abstract

The outcomes that result from previous behavior affect future choices in several ways, but the neural mechanisms underlying these effects remain to be determined. Previous studies have shown that the lateral (AGl) and medial (AGm) agranular areas of the rat frontal cortex are involved in the learning and selection of action. Here we describe the activity of single neurons in AGl and AGm as rats learned to perform a directional choice task. Our analysis shows that single-cell activity in AGl and AGm was modulated by the outcome of the previous trial. A larger proportion of neurons encoded the previous trial's outcome shortly after cue onset than during other time periods of a trial. Most of these neurons had greater activity after correct trials than after error trials, a difference that increased as behavioral performance improved. The number of neurons encoding the previous trial's outcome correlated positively with performance accuracy. In summary, we found that neurons in both AGl and AGm encode the outcome of the immediately preceding trial, information that might play a role in the successful selection of action based on past experience.

Keywords: firing rates; learning; previous trial outcome; primary motor and nonprimary motor areas.

Fig. 1.

Implant site and illustration of the behavioral task. A: implant site and hit map of the recorded units. A 16-channel (2×8) microwire array with electrode numbers labeled was implanted in the rat's left hemisphere centered at 3 mm AP, 2 mm ML from the bregma. The delineation of lateral (AGl) and medial (AGm) agranular was made according to the Rat Brain Atlas (Paxinos and Watson 2005). The hit map is a summary of all units from the 8 implanted rats. B: example spike waveforms and interstimulus interval histograms in 2 different sessions. C: behavioral interface panel facing the rat and task trial timelines. The rat would press the center paddle to start a trial and 1 of the 5 cue lights would be on immediately (as shown in the example, the 1st cue light of the left side was on for that trial). Both left and right response paddles would extend 2 s after cue onset. The rat would press response paddles to shift the position of the lighted cue light to the center for a sugar pellet reward, which was dispensed into the little tray shown by the arc along the center line of the face panel. The task was for the rat to press on the paddle of the same side as the cue light. As shown in the example, the correct response was a press on the left-side paddle, which moved the cue light to the right by one position, or the center position.

Fig. 2.

Examples of performance. A: daily performance accuracy of rat A. Three learning stages were defined based on daily accuracy: prelearning, learning, and postlearning, which are delineated by the vertical lines. B and C: response latency for failed and successful trials (B) and posterror and postsuccess trials (C) of rat A in each recording session.

Fig. 3.

Movement characteristics. A: example movement trajectories from cue onset to paddle press of rat J. The background is the front view of the interface panel facing the rat. The light and dark gray curves represent the trajectories of left and right trials, respectively. The circles represent movement onset and the squares represent end of movement, which correspond to the rat's head positions. B and C: x- and y-positions corresponding to movement trajectory in rat A along time. Error bars represent 1SD. D: start time, end time, and movement duration as a function of learning sessions of rat I. Movement start and end time was longer in the 1st 3 sessions of learning and stays more stable afterwards. E: histograms of start time, end time, and movement duration for all 6 rats (A, B, H, I, J, and K). Left: movement start time; middle, movement end time; right: movement duration.

Fig. 4.

Rat's movement was not dependent on the previous trial outcome. The x-coordinate is plotted as a function of time. Black lines and gray lines represent postsuccess and posterror trials, respectively. A: movement trajectories in an early session (#5) of learning of rat L, i.e., in the prelearning stage. B: movement trajectories in a later session (#24) of rat K in the learning stage.

Fig. 5.

Performance in 3 learning stages for 8 rats. The x axis represents the normalized session number, and the y axis represents posterror accuracy (R_es; unfilled circles) and postsuccess accuracy (R_ss; *). The 4th order polynomial regression lines for R_ss and R_es are provided separately for each of the learning stages. Only during the learning stage was the posterror accuracy R_es slightly higher than the postsuccess accuracy R_ss (paired t-test, P < 0.05).

Fig. 6.

Example AGl unit and its spike raster of rat D isolated from channel 7 on the 12th recording session (left) and example AGm neural spike raster for rat E isolated from channel 14 on the 16th recording session (right). The x-axis is the time course with event markers. Top: spike raster plots from individually recorded trials and the average firing rates. Middle: area under the curves (AUCs) to compare differences in neural responses between postsuccess and posterror trials for a left (green) or right (black) directional choice, respectively. Bottom: AUCs to compare differences in neural responses between left and right directional choices after a successful trial (blue) or an error trial (red), respectively. The respective chance level AUC values are shown in dashed lines in middle and bottom.

Fig. 7.

Neural population (n = 192) and their dynamic modulations according to the two task factors: directional choice of current trial (left press or right press) or previous trial outcome (success or error). A and B: dynamic representations of the percentages of neurons that showed significant modulation to the two task factors using two-way ANOVA. The peak modulation value for previous trial outcome is marked as “c” and “d” for the AGm and AGl area, respectively. C and D: scatter plots of P value pairs of each neuron. C: point “c” in A corresponds with the 8th time point (400–900 ms after cue onset) during the cue-on task period. 30.1% (n = 31) of the AGm neurons were encoding previous trial outcome, 22.3% (n = 23) were encoding directional choice, and 35.9% (n = 37) were encoding both. D: point “d” in B corresponds with the 8th time point (400–900 ms after cue onset) during the cue-on task period. 41.6% (n = 37) of the AGl neurons were encoding previous trial outcome, 24.7% (n = 22) were encoding directional choice, and 27.0% (n = 24) were encoding both.

Fig. 8.

Summary of previous trial modulation measure I₁ vector over the cue-on task period (0–2,000 ms) for all units (n = 192). A: component-wise absolute values of I₁ of each unit over time during the cue-on task period. Unit records were sorted in ascending order according to the absolute values of Ī₁. B: distribution of τ₁ using 100-ms time bin resolution. C: histogram of all units according to Ī₁.

Fig. 9.

The percentage of previous outcome selective AGm and AGl units as a function of daily performance accuracy R. Solid line represents the combined regression line for AGm and AGl. This analysis used 10 performance accuracy intervals, ranging from 40 to 85%. The percentage of previous outcome selective neurons in each interval was expressed as the number of previous trial outcome selective neurons divided by the total number of neurons in the interval.

Fig. 10.

AUC measurement of difference in neural responses between posterror trials and postsuccess trials as behavioral accuracy improved.