Ei Ichi Izawa

The Mind Through Chick Eyes : Memory, Cognition and Anticipation

Abstract To understand the animal mind, we have to reconstruct how animals recognize the external world through their own eyes. For the reconstruction to be realistic, explanations must be made both in their proximate causes (brain mechanisms) as well as ultimate causes (evolutionary backgrounds). Here, we review recent advances in the behavioral, psychological, and system-neuroscience studies accomplished using the domestic chick as subjects. Diverse behavioral paradigms are compared (such as filial imprinting, sexual imprinting, one-trial passive avoidance learning, and reinforcement operant conditioning) in their behavioral characterizations (development, sensory and motor aspects of functions, fitness gains) and relevant brain mechanisms. We will stress that common brain regions are shared by these distinct paradigms, particularly those in the ventral telencephalic structures such as AIv (in the archistriatum) and LPO (in the medial striatum). Neuronal ensembles in these regions could code the chicks anticipation for forthcoming events, particularly the quality/quantity and the temporal proximity of rewards. Without the internal representation of the anticipated proximity in LPO, behavioral tolerance will be lost, and the chick makes impulsive choice for a less optimized option. Functional roles of these regions proved compatible with their anatomical counterparts in the mammalian brain, thus suggesting that the neural systems linking between the memorized past and the anticipated future have remained highly conservative through the evolution of the amniotic vertebrates during the last 300 million years. With the conservative nature in mind, research efforts should be oriented toward a unifying theory, which could explain behavioral deviations from optimized foraging, such as “naïve curiosity,” “contra-freeloading,” “Concorde fallacy,” and “altruism.”

Reward-related neuronal activities in basal ganglia of domestic chicks

We aimed to reveal what is coded in the basal ganglia of domestic chicks. In the water-reinforced ‘go’ task, chicks learned to peck selectively at a colored bead in order to obtain a drop of water. Out of 38 units obtained, seven showed excitatory activities specifically during the reward period. In the food-reinforced go/no-go task, chicks learned to discriminate two colors to obtain mash food after a delay period. They also learned to ignore another color, which was not associated with a reward. Out of 27 units obtained, four showed excitatory activities during the cue period, specifically when a food reward was anticipated. LPO neurons may code qualities of the obtained rewards, and also chicks anticipation of the forthcoming rewards.

The role of basal ganglia in reinforcement learning and imprinting in domestic chicks

Effects of bilateral kainate lesions of telencephalic basal ganglia (lobus parolfactorius, LPO) were examined in domestic chicks. In the imprinting paradigm, where chicks learned to selectively approach a moving object without any explicitly associated reward, both the pre- and post-training lesions were without effects. On the other hand, in the water-reinforced pecking task, pre-training lesions of LPO severely impaired immediate reinforcement as well as formation of the association memory. However, post-training LPO lesions did not cause amnesia, and chicks selectively pecked at the reinforced color. The LPO could thus be involved specifically in the evaluation of present rewards and the instantaneous reinforcement of pecking, but not in the execution of selective behavior based on a memorized color cue.

Neural correlates of memorized associations and cued movements in archistriatum of the domestic chick

The archistriatum mediates a neural pathway from the medial part of intermediate hyperstriatum ventrale (in the dorsal pallium) to the lobus parolfactorius (in the medial striatum), thus is possibly involved in memory formation in the domestic chick. To elucidate the functional roles, we examined single neuron activities from archistriatum in unconstrained chicks during execution of a GO/NOGO task. In this task, a brief motor sound was given as initial cue, and immediately followed by presentation of a coloured bead. Chick was required to recall the memorized associations between the colour and reward, and pecked at the bead to gain food after a delay (GO trials) or stayed not pecking (NOGO trials). The ventral part of intermediate archistriatum proved to contain a group of neurons that selectively responded to the reward‐associated colours before the reward was actually presented, possibly coding the memorized associations. Another group of neurons fired during the reward period, thus could code aspects of the food reward. Yet another group of neurons started to fire immediately on the cue sound and prior to the cued movements nonselectively in both GO and NOGO trials, thus could be involved in the sensori‐motor link between the sound and the targeted body movements. It is concluded that even a subregion of archistriatum contains diverse neural codes for memorized associations and food rewards, and neural codes of movements cued by sounds, suggesting that archistriatum is a complex of different functional systems, possibly corresponding to striatum, limbic amygdala, and prefrontal cortex in mammals.

Lesions of the ventro-medial basal ganglia impair the reinforcement but not the recall of memorized color discrimination in domestic chicks

Effects of bilateral chemical lesions of the ventro-medial basal ganglia (lobus parolfactorius, LPO) were examined in 3-9-day-old domestic chicks. In experiment-1, chicks were trained to peck at a blue bead that was associated with drops of water as a reward. Addition of passive avoidance training using a bitter yellow bead resulted in highly selective pecking between blue and yellow. LPO lesion (given 3-5 h after training) did not impair the selectivity when chicks were tested 24 h afterwards, while the novel reinforcement using a red bead was severely impaired. In experiment-2, chicks were trained in a GO/NO-GO color discrimination task with food reward. Trained chicks received bilateral LPO lesions, and they were tested 48 h afterwards for the number of pecks and latency of the first peck in each trial. The LPO lesion did not impair the recall of memorized color discrimination in tests, while the chicks were severely deficient in post-operative novel training. These results confirm that: (1) bilateral LPO ablation does not interfere with selective pecking based on the memorized color cues; but (2) it impairs reinforcement in novel training. LPO is thus supposed to be involved in acquisition, rather than execution of memorized behaviors.

Localized lesions of ventral striatum, but not arcopallium, enhanced impulsiveness in choices based on anticipated spatial proximity of food rewards in domestic chicks

The effects of bilateral chemical lesions of the ventral striatum (nucleus accumbens and the surrounding areas in the medial striatum) and arcopallium (major descending area of the avian telencephalon) were examined in 1-2-weeks old domestic chicks. Using a Y-maze, we analyzed the lesion effects on the choices that subject chicks made in two tasks with identical economical consequences, i.e., a small-and-close food reward vs. a large-and-distant food reward. In task 1, red, yellow, and green beads were associated with a feeder placed at various distances from the chicks; chicks thus anticipated the spatial proximity of food by the beads color, whereas the quantity of the food was fixed. In task 2, red and yellow flags on the feeders were associated with various amount of food; the chicks thus anticipated the quantity of food by the flags color, whereas the proximity of the reward could be directly visually determined. In task 1, bilateral lesions of the ventral striatum (but not the arcopallium) enhanced the impulsiveness of the chicks choices, suggesting that choices based on the anticipated proximity were selectively changed. In task 2, similar lesions of the ventral striatum did not change choices. In both experiments, motor functions of the chicks remained unchanged, suggesting that the lesions did not affect the foraging efficiency, i.e., objective values of food. Neural correlates of anticipated food rewards in the ventral striatum (but not those in the arcopallium) could allow chicks to invest appropriate amount of work-cost in approaching distant food resources.

D1-receptor dependent synaptic potentiation in the basal ganglia of quail chicks

Properties of local synapses were analyzed in lobus parolfactorius (LPO; avian homologue of caudate-nucleus) of quail chicks by using slice preparations in vitro. Field-potential extracellular and whole-cell intracellular recordings revealed excitatory synaptic inputs converging from dorsal and ventral regions within LPO. With exogenous dopamine (100 μM) in the perfusate, synchronized conditioning stimulation induced biased changes in the dorsal and the ventral inputs; potentiation in the dorsal input and depression in the ventral input in average. On the other hand, de-synchronized conditioning failed to induce such biased changes, although the differences were not statistically significant. SCH-23390 (3 μM) blocked the dorsal potentiation, while AP-5 (100 μM) tended to block both of these changes. The plastic nature may underlie the memory formation in appetitive/aversive learning tasks.

Accurate Visual Memory of Colors in Controlling the Pecking Behavior of Quail Chicks

Abstract Animals are predisposed to memorize specific features of objects they encounter, and to link them with behavioral outputs in a selective manner. In this study, we examined whether chicks memorize objects by colors, and how they exploit the memorized color cues for selective pecking in 1- to 2-days-old quail chicks (Coturnix japonica). Ball-shaped beads painted in green (G), yellowish green (YG) and the intermediate color (YGG) were used. Repetitive presentation of a bead (interval: 4.5 min) resulted in gradually fewer pecks (habituation). Subsequent presentation of a different color caused proportionately more pecks (dishabituation); e.g., after habituation to the G bead, the YG bead caused a stronger dishabituation than the YGG bead did. The dishabituation appeared symmetric; e.g., the YG bead caused as strong dishabituation after the G-habituation, as was caused by the G bead after the YG-habituation. Number of pecks could thus reveal the memory-based color perception in chicks. Similar discrimination of beads by memorized color cues was found after one-trial passive avoidance training, where chicks learned to avoid a bitter-tasting object without any differential pre-training experiences. However, proportion of the chicks that discriminated between different colors became progressively smaller at test 15 min, 1 hr, and 24 hr post-training. On the other hand, proportion of chicks that distinguished beads by non-color cues remained unchanged. Chicks may primarily form an accurate memory of colors, but gradually change the link between the color memory and the pecking behavior.

Hippocampal lesion delays the acquisition of egocentric spatial memory in chicks

Effects of bilateral chemical lesion of the hippocampus was examined in 1- to 2-week-old domestic chicks. Chicks were trained and tested in an egocentric spatial task, in which subject chicks should memorize location of a rewarding object in reference to the subjects viewpoint. Two beads were simultaneously presented on a wall, and chicks pecked at one of them based on relative location (left–right or above–below) to gain a reward. Comparison of training curves revealed that the lesion significantly delayed, but did not impair, the acquisition. Recall of the spatial cue, as well as conditioning with color cues, was not impaired. Hippocampus could thus be involved in memory formation of spatial relationships between nearby objects.