Shin Yanagihara

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.

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.

Expression of transcription factor ZENK (zif/268) in telencephalon of quail chicks after induced seizure and passive avoidance training.

Abstract Functional significance of an immediate early gene ZENK (zif/268) was examined in telencephalic regions (homologues of neocortex and basal ganglia) of newly-hatched quail chicks; hyperstriatum accessorium (HA), hyperstriatum ventrale (HV), neostriatum (N) and lobus parolfactorius (LPO). Chicks were trained by a green bead soaked either in a strong aversant (methylanthranilate, MeA), in a weak aversant (MeA diluted by ethanol, 1/3MeA), or in water. Chicks were then tested at 45–50 min post-training, and immediately processed for ZENK immunostaining. Neither the training condition (MeA, 1/3MeA, or water) nor the responses at test (recall or amnesia) significantly contributed to the immunopositive cell densities in all of these regions. On the other hand, single intraperitoneal injection of metrazole (CNS convulsant) induced a transient epileptiform seizure, and caused significantly enhanced ZENK expression in HV and LPO but not in HA and N. However, the metrazol-induced seizure did not interfere with the following passive avoidance training, and chicks successfully learned to avoid the aversive bead when tested at 24 hr subsequently. Among three groups of chicks (metrazol-treated, saline control, and untreated chicks), no significant differences were found in their responses at test (recall, generalized avoidance, or amnesia). These results suggest that enhanced ZENK expression may represent lasting neural activities, but may not be involved specifically in the passive avoidance memory formation.

Predisposed visual memory of shapes in quail chicks.

Abstract Newly hatched chicks will spontaneously peck at conspicuous objects in their field of view, and soon learn to distinguish between edible food particles and unpleasant tasting objects. To examine whether the selective pecking is based on the ability to memorize shapes, we analyzed pecking behavior of 1- to 2-days-old quail chicks (Coturnix japonica) by using ball- and triangle-shaped beads both painted in green. Repeated presentation of dry bead (either ball or triangle) resulted in a progressively fewer number of pecks (habituation). When chicks were tested by triangle after repeated presentation of ball, chicks showed a significant increase in the number of pecks at the triangle (dishabituation). On the other hand, when tested by ball after a series of triangle presentations, pecking frequency did not increase (no dishabituation). Chicks thus distinguished the triangle as a novel object after being habituated to ball, but did not respond to the ball after triangle. A similar asymmetry was found in one-trial passive avoidance task. Chicks were pre-trained by water-coated (neutral) triangle and then trained by methylanthranilate-coated (aversive) ball. In this case, most chicks learned to avoid the ball, and half of these successful learners pecked at the triangle; they distinguished triangle from ball. When chicks were pre-trained by neutral ball and trained by aversive triangle, on the other hand, most chicks did not distinguish the ball from triangle, and showed a generalized avoidance for both beads. Chicks may be innately predisposed to memorize a limited category of shapes such as ball, and associate them with selective avoidance.

Distinct mechanisms for expression of Fos-like immunoreactivity and synaptic potentiation in telencephalic hyperstriatum of the quail chick

In the intermediate and medial hyperstriatum ventrale (IMHV), a telencephalic region essentially involved in the initial processes of early learning tasks in poultry chicks, induction of an immediate early gene c-fos correlates significantly with the degree of learning (K.V. Anokhin, R. Mileusnic, I.Y. Shamakina, S.P.R. Rose, Effects of early experience on c-fos gene expression in the chick forebrain, Brain Res. 544 (1991) 101-107; B.J. McCabe, G. Horn, Learning-related changes in Fos-like immunoreactivity in the chick forebrain after imprinting, Proc. Natl. Acad. Sci. USA 91 (1994) 11417-11421). In slices of IMHV in vitro, on the other hand, tetanic stimulation at a low frequency induces a potentiation of synaptic responses (P.M. Bradley, B.D. Burns, A.C. Webb, Potentiation of synaptic responses in slices from the chick forebrain, Proc. R. Soc. Lond. B. 243 (1991) 19-24; T. Matsushima, K. Aoki, Potentiation and depotentiation of DNQX-sensitive fast excitatory synaptic transmission in telencephalon of the quail chick, Neurosci. Lett. 185 (1995) 179-182). In this study, we have examined a possible causal link between these two forms of activity-dependent processes, c-fos expression and synaptic potentiation. C-fos was visualized immunohistochemically using antibody raised against the Fos-protein, and potentiation was evaluated on the basis of field potential responses to local electrical stimulation. Tetanic stimulation (5 Hz x 300 pulses) was required for potentiation, but not for c-fos expression. Conversely, a negative correlation appeared between them, and slices with relatively high density of Fos-like immunoreactive cells around the stimulation site failed to show potentiation. Furthermore, drugs similarly effective in blocking potentiation (such as AP5 (NMDA receptor antagonist) and bicuculline (GABA(A) receptor antagonist)) had different effects on the c-fos induction. While AP5 had minor, if any, effects on c-fos expression, bicuculline enhanced it selectively around the site of stimulation. Our results suggest that these two processes are basically distinct, and could represent different aspects in the formation of memory traces in IMHV.

Phasic basal ganglia activity associated with high-gamma oscillation during sleep in a songbird

The basal ganglia is thought to be critical for motor control and learning in mammals. In specific basal ganglia regions, gamma frequency oscillations occur during various behavioral states, including sleeping periods. Given the critical role of sleep in regulating vocal plasticity of songbirds, we examined the presence of such oscillations in the basal ganglia. In the song system nucleus Area X, epochs of high-gamma frequency (80-160 Hz) oscillation of local field potential during sleep were associated with phasic increases of neural activity. While birds were awake, activity of the same neurons increased specifically when birds were singing. Furthermore, during sleep there was a clear tendency for phase locking of spikes to these oscillations. Such patterned activity in the sleeping songbird basal ganglia could play a role in off-line processing of song system motor networks.