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

doi:10.1016/j.bbr.2005.10.002

Behavioural Brain Research

Volume 168, Issue 1, 15 March 2006, Pages 1-12

https://doi.org/10.1016/j.bbr.2005.10.002 Get rights and content

Abstract

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 bead's 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 flag's 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.

Introduction

Similar to the neostriatum and the nucleus accumbens of mammals [28], [36], the ventral striatum of the avian basal ganglia contains neural correlates of anticipated food rewards. Recording from freely-behaving chicks performing a color-discrimination task with a delayed food reward revealed a population of neurons that fired selectively to color cues associated with the reward, irrespective of the required operant [42]. Further analysis revealed specific correlates of the temporal proximity and the quantity of the reward [18]. Accordingly, localized lesions of the ventral striatum caused impulsive choice, and the lesioned chicks showed a stronger preference for immediate and small food rewards over delayed and large alternatives [17]. A similar result has been seen in rats with lesions to the core region of the nucleus accumbens [4], suggesting that these correlates could play a pivotal role in decision-making and that this role is highly conserved among amniotes.

Although the tasks employed in these studies are sensitive in elucidating the rules underlying choice (for a review see [25]), they may not represent the situations that the subject animals might face in natural environments. First, because natural food resources are unevenly distributed, animals actively search for food, rather than waiting in front of an empty feeder for a delayed delivery of food reward. Second, although local cues may signal the presence of food (such as colored leaves signaling hidden nuts), animals evaluate the distance to a potential food by direct visual inspection rather than anticipate it by the associated cues. It is critically important to examine whether the chicks in task conditions could make choices in the way that is predicted from foraging theory [6], [37].

The ventral striatum is not the sole region involved in reward anticipation in the avian brain. Arcopallium might also be involved in choices based on anticipated food rewards, because the intermediate arcopallium (AI) contains a population of neurons that fire selectively to cue colors associated with delayed food [1]. Actually, bilateral lesions of AI reduced the choice of large reward, when a high work-cost accompanied the consummatory act of food consumption [24]. However, so far, it has not yet been examined if similar lesions of the arcopallium could reduce choice, when a considerable amount of work-cost should be invested in approaching food reward.

In the present study, we therefore examined the effects of lesions on the performance of two different tasks. In the first task, cue colors were associated with the distance to a feeder, rather than the delay of reward delivery. In the second task, the feeders could be directly inspected at the time of choice and cue colors were associated with the quantity of the food. Comparing the chicks’ choices and their behavioral executions in these two tasks revealed striking differences, suggesting that the ventral striatum (but not the acropallium) is involved in the choice-making that is based on the anticipated proximity of food rewards.

Section snippets

Subjects

These experiments were conducted according to the guidelines of the Committee for Animal Experimentation at the Graduate School of Bioagricultural Science, Nagoya University; the guidelines are based on national regulations for animal welfare in Japan. A total of 49 unsexed domestic chicks (Gallus domesticus, Cobb strain) were used. Fertilized eggs obtained from a local supplier (3-M Co., Aichi, Japan) were incubated in the laboratory, and hatchlings were communally housed in a dark moisturized

Results

Of 27 chicks used in task 1, two chicks were discarded after step 1 and four chicks were discarded following step 2. The remaining 21 chicks were trained in step 3, tested in step 4, successfully operated, trained in step 5, and finally tested in step 6. Of the 22 chicks used in task 2, eight chicks were discarded after step 2 and another three chicks were discarded following step 3. Of the remaining 11 chicks, four died during the surgery. The following results are thus based on data obtained

Task dependence of the lesion effects

In the binary choice between two rewarding alternatives (i.e., a small and close food reward versus a large and distant food reward), excitotoxic lesion of the ventral striatum resulted in an enhanced impulsiveness in task 1, but not in task 2. In task 1, chicks associated colored cue beads with the distance to the feeders, whereas the quantity of the food did not vary in each trial but was fixed for each of the two runways. Chicks were required to peck a bead, so that the corresponding door

Acknowledgements

This study was supported by grants from the Japan Society for the Promotion of Science (JSPS) to E.I. (grant-in-aid for young scientists, #14005357) and to T.M. (grant-in-aid for scientific research (B)(2), #15370033), as well as those from the Japanese Ministry of Education, Culture, Sports, Science and Technology to T.M. (grant-in-aid for exploratory research, #1665702, grant-in-aid for priority areas—integrative brain research, #17021018). Financial support from the bilateral

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A deficient serotonergic system is associated with psychopathological behaviors in various species, among which, feather pecking (FP) in chickens. Deficiency in the serotonergic system can predispose birds to develop FP, while the serotonergic system is affected in birds that feather peck. Serotonin (5-HT) can further influence dopamine (DA) activity. Lines with high FP tendency generally have low central 5-HT and DA turnovers at a young age, but high turnovers at an adult age in brain areas involved in somato-motor regulation and goal-directed behavior. Agonizing 5-HT1A and 5-HT1B receptors increases FP, while antagonizing D2 receptor reduces FP. Genetic associations exist between FP, 5-HT1A and 5-HT1B receptor functioning and metabolism of 5-HT and DA. Birds with deficient functioning of the somatodendritic 5-HT1A autoreceptor and 5-HT metabolism appear predisposed to develop FP. Birds which feather peck often eat feathers, have low whole-blood 5-HT, different gut-microbiota composition and immune competence compared to non-peckers. FP and feather eating likely affect the interaction between gut microbiota, immune system and serotonergic system, but this needs further investigation.
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Previous studies have shown that domestic chicks, Gallus gallus domesticus, trained in a competitive foraging condition would subsequently develop a high degree of impulsiveness in an intertemporal choice paradigm. Competition inevitably causes variance in the amount of food that the foragers gain. However, it is not known whether the food variance is causally linked with the impulsiveness. In experiment 1, we compared four groups of chicks trained in combinations of two social conditions (pseudocompetition or isolated) and two food conditions (variable or constant food). The food variance was introduced by varying the number of grains in each trial according to a binomial distribution. The subject chick was separated from the competitors by a transparent wall, and no actual interference occurred. Chicks were subsequently tested in binary choices between a small reward after a short delay (SS) and a large reward after a long delay (LL) in an isolated and constant food condition. If chicks had been trained under the pseudocompetition and variable food, they chose LL significantly less frequently than the other three groups. The effect disappeared when the LL delay was omitted, suggesting that chicks accurately memorized the food amount. The food variance is thus a necessary condition for the stronger temporal discounting. Otherwise, the observed effect could be ascribed to a paradoxical risk proneness associated with the variable option. In experiment 2, we compared four groups of chicks in which food amount varied either in SS or LL, or both. The subsequent binary choice tests revealed that the chicks chose SS irrespective of whether SS or LL had varied. These results cannot be explained in terms of a greater risk-prone choice of the variable option. Coincidence of perceived competition and food variance, at least in one option, is sufficient for chicks to develop choice impulsiveness.
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Descending projections from the right arcopallium via the OM might be lateralized to social stimuli in the context of foraging behavior. However, bilateral excitotoxic lesions to the ventral arcopallium in chicks caused work cost aversion in terms of food pecking, but failed to impair behavioral execution [30,31]. Thus, the arcopallium is a strong candidate for social facilitation.
The frequency or intensity of behavior is often facilitated by the presence of others. This social facilitation has been reported in a variety of animals, including birds and humans. Based on Zajonc’s “drive theory,” we hypothesized that facilitation and drive have shared neural mechanisms, and that dopaminergic projections from the midbrain to striatum are involved. As the ascending dopaminergic projections include the mesolimbic and nigrostriatal pathways, we targeted our lesions at the medial striatum (MSt) and substantia nigra (SN). We found that a bilateral electrolytic lesion of the MSt suppressed baseline foraging effort, but social facilitation was intact. Conversely, an electrolytic lesion targeted at the unilateral SN (on the right side) partially suppressed social facilitation, while baseline foraging effort remained unaffected. However, selective depletion of catecholaminergic (thyrosine hydroxylase immunoreactive) terminals by micro-infusion of 6-hydroxydopamine (6-OHDA) to bilateral MSt had no significant effects on foraging behavior, whereas it impaired formation of the association memory reinforced by water reward. Neurochemical assay by high-perfromance liquid chromatography also revealed a significant decrease in the dopamine and noradrenaline contents in MSt after 6-OHDA micro-infusion compared with intact control chicks. Thus, we conclude that the neural substrate of social facilitation can be dissociated from that responsible for reward-based foraging effort, and that ascending dopaminergic pathways do not appear to contribute to social facilitation. Based on our detailed analysis of the lesion areas, we discuss fiber tracts or neural components of the midbrain tegmental area that may be responsible for social facilitation.
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Decisions are guided not just by expectations of the benefits that will ensue but also by expectations about costs. The foraging choices of animals, both in the laboratory and in the wild, are influenced by how energetically demanding, or effortful, a choice is. The making of such choices depends crucially on the anterior cingulate cortex and an interconnected set of brain regions including the striatum. Neurons in the anterior cingulate cortex are unusual in that they integrate information about several features of a choice including both rewards and effort costs. While brain regions such as the ventromedial prefrontal cortex represent the most pertinent features of decisions in a flexible manner, the anterior cingulate cortex’s representation of choices manifests in a reference frame appropriate for foraging – deciding whether to engage with a potential choice or whether the richness of the environment and expectations about effort suggest it is better to forage elsewhere.

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¹: Both authors equally contributed to the present study.

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

Abstract

Introduction

Section snippets

Subjects

Results

Task dependence of the lesion effects

Acknowledgements

J Chem Neuroanat

Neurosci Biobehavior Rev

Theor Popul Biol

Behav Brain Res

Brain Res

Trends Neurosci

Cog Brain Res

Behav Brain Res

Brain Res Bull

Trends Neurosci

Trends Neurosci

Behav Brain Res

Trends Cog Sci

Brain Res

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

Eur J Neurosci

Avian brains and a new understanding of vertebrate brain evolution

Nature Rev Neurosci

Impulsive choice induced in rats by lesions of the nucleus accumbens core

Science

Termination pattern of medial hyperstriatum ventrale efferents in the archistriatum of the domestic chick

J Comp Neurol

Efferent connections of the domestic chick archistriatum: a Phaseolus lectin anterograde tracing study

J Comp Neurol

Psychomotor stimulant addiction: a neural systems perspective

J Neurosci

Pathways of the past: the imprint of memory

Nature Rev Neurosci

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