Localized lesion of caudal part of lobus parolfactorius caused impulsive choice in the domestic chick: evolutionarily conserved function of ventral striatum

Abstract

Effects of bilateral chemical lesions of the medial basal ganglia [lobus parolfactorius (LPO)] were examined in 7- to 14-d-old domestic chicks. Chicks were trained in a color discrimination task, in which the subject had to peck one of the two colored beads associated with rewards that differed in quantity (amount of food) and/or temporal proximity (delay of food delivery from peck). In experiment 1, food was given without delay, and chicks successfully learned to choose a colored bead that was associated with a larger reward than the other. In experiment 2, a colored bead (red) was associated with a large reward delivered after a delay (D = 1, 2, or 3 sec), whereas another (yellow) was associated with a small reward delivered immediately. In intact and sham-operated conditions, chicks with a longer D chose the red bead progressively fewer times. Selective lesions to the caudal LPO (but not the rostral LPO) caused impulsive choice, and the ablated chicks chose the yellow bead and gained a small-immediate reward regardless of D. However, when retrained in a null-delay condition (D = 0 sec), the lesioned chick chose the red bead again. Ability to associate novel colors with reward was also unimpaired. These results suggest that the LPO may be responsible for the anticipation of reward proximity and involved in a suppression of impulsiveness by which animals seek immediate gains. The present results also indicate a striking similarity in functional roles between the avian LPO and the nucleus accumbens/ventral striatum in mammals.

Fig. 1.

Procedure and results of experiment 1.A, Protocol of the choice task with different reward quantities. In training, three types of trials were given in pseudorandom sequences: trials with a pair of identical blue beads (−, no reward), trials with a pair of yellow (1 or 6 pellets) and blue (−, no reward) beads, and trials with a pair of red (6 or 1 pellets) and blue (−, no reward) beads. The side of presentation was randomized. Chicks thus learned to choose a rewarding color (red or yellow) in the red/blue and the yellow/blue trials and not to peck beads in the blue/blue trials. Chicks were then tested in four trial types that were arranged randomly, i.e., blue/blue (20 trials), yellow/blue (5 trials), red/blue (5 trials), and red/yellow (10 trials). The side of presentation was also randomized. B, Number of choices in test trials with red/blue pair and yellow/blue pair; data obtained from the 6-vs-1 chicks (open columns), the 6-vs-6 chicks (filled columns), and the 1-vs-6 chicks (shaded columns). The number of choices per five trials was averaged over chicks. All of the chicks chose red or yellow;n denotes number of chicks. C, Proportion (percentage) of chicks that chose red was plotted along the 10 test trials with red/yellow pairs. Data were obtained from the 6-vs-1 chicks (open symbols), the 6-vs-6 chicks (filled symbols), and the 1-vs-6 chicks (shaded symbols). D, The number of choices of red was counted in the red/yellow test trials, averaged over chicks, and compared among 6-vs-1, 6-vs-6, and 1-vs-6 chicks; post hoc multiple comparisons between pairs among these three groups revealed significant differences at p < 0.001 (asterisks). Error bars denote SEM.

Fig. 2.

Procedure of experiment 2. A, Protocol of the choice task with delayed reward. B, Schedule of training and tests. Ba, Chicks were trained according to the same protocol as in experiment 1 (Fig.1A) except that the yellow bead was associated with a reward of one pellet and a longer delay time (D = 0, 1, 2, or 3 sec) was introduced for the red bead. Afterward, four types of trials were given, and chicks were tested with a choice between red (6) and yellow (1) (preoperative test). Bb, After recovery from the operation, chicks were retrained and tested according to the same procedures (postoperative test). We examined whether the lesion changed the choice between red (large-late reward) and yellow (small-immediate reward). Bc, Chicks were further retrained and tested in the null-delay condition, whereD = 0 for both red and yellow. We examined the ability to choose the large reward by color cues. Bd, Finally, chicks were trained using a novel color pair, e.g., green associated with six pellets (6) and black with no reward (−) with D = 0 sec for both colors; the ability to associate novel colors with reward was thus examined. InBa–Bc, symbols indicate the colors of the beads: black = red bead,gray = yellow bead, white = blue bead, respectively. In Bd, black and green beads were used; see Materials and Methods for further explanation.

Fig. 3.

Histological reconstruction of ibotenic acid lesions in six groups of chicks. A, Lesioned areas are superimposed on frontal sections of the telencephalon; the coordinates (A9.2–A12.2) follow the stereotaxic atlas of Kuenzel and Masson (1988). Dark areas indicate overlaps among chicks. a–d indicate four groups of chicks with caudal LPO lesion (cLPO), ande and f indicate two group of chicks with rostral LPO lesion (rLPO). The cLPO lesions included the rostral part of the nucleus accumbens. Groups differed also in the delay time (D = 0, 1, 2, 3; see Fig.2A); n denotes the number of chicks in each group. Ac, Nucleus accumbens;E, ectostriatum; LPO, lobus parolfactorius; N, neostriatum; PP, paleostriatum primitivum. B, Representative photomicrographs of Nissl-stained caudal LPO in a sham (a) and a lesioned (b) chick; note the clear boundary between lesioned area and its surroundings (b, dashed line). Regions inrectangles marked by c andd are shown at a higher magnification inc and d, respectively.

Fig. 4.

Effects of LPO lesions on the choice between red (large-late reward) and yellow (small-immediate reward). The number of choices for the red bead per 10 trials in the tests was averaged over chicks in each group and plotted against the delay time (D). Error bars denote SEM, andn = number of chicks. A, In four groups of sham chicks (sham injection into cLPO; D= 0, 1, 2, or 3 sec, respectively), longer D resulted in progressively lower chance of choosing red (large-late reward) in both preoperative and postoperative tests. After retraining in the null-delay condition, however, chicks of all groups chose red (large reward), suggesting that the association between color cue and reward quantity was unimpaired. B, In four other groups of chicks (D = 0, 1, 2, or 3 sec, respectively), cLPO was lesioned as shown in Figure 2A. The choice in the postoperative test differed from the preoperative test in three groups of chicks with D ≥ 1 sec; chicks became impulsive and chose the small-immediate reward. After retraining in the null-delay condition, chicks chose the large reward, indicating that the lesion did not impair the chicks' ability to discriminate colors on the basis of the quantity of the associated reward.C, Two groups of rLPO-lesioned chicks (D = 1 and 2 sec) were trained and tested in the same procedure but remained unimpulsive. Null-delay retraining similarly caused a shift toward large reward. See Results for statistic comparisons.

Fig. 5.

No effects of LPO lesions on novel training.A, B, Total number of trials (A) and number of incorrect trials (B) during the novel training procedure (Fig.2Bd) were compared among three groups of chicks: sham, cLPO-, and rLPO-lesioned chicks. Training continued until chicks met the criteria of correct choice in six successive trials. The cLPO-lesioned chicks tended to have longer training times than others, although no statistically significant difference was found.C, The number of correct choices per 12 test trials was compared, and no significant differences were found among groups.D, The number of pecks required for chicks to ingest five pellets showed no significant differences among groups, suggesting that the pecking accuracy was unimpaired. Columns and error bars indicate mean ± SEM, respectively. One-way ANOVA was adopted after Bartlett's test, both at p < 0.05.