Abstract
A prerequisite for adaptive goal-directed behavior is that animals constantly evaluate action outcomes and relate them to both their antecedent behavior and to stimuli predictive of reward or non-reward. Here, we investigate whether single neurons in the avian nidopallium caudolaterale (NCL), a multimodal associative forebrain structure and a presumed analogue of mammalian prefrontal cortex, represent information useful for goal-directed behavior. We subjected pigeons to a go-nogo task, in which responding to one visual stimulus (S+) was partially reinforced, responding to another stimulus (S–) was punished, and responding to test stimuli from the same physical dimension (spatial frequency) was inconsequential. The birds responded most intensely to S+, and their response rates decreased monotonically as stimuli became progressively dissimilar to S+; thereby, response rates provided a behavioral index of reward expectancy. We found that many NCL neurons' responses were modulated in the stimulus discrimination phase, the outcome phase, or both. A substantial fraction of neurons increased firing for cues predicting non-reward or decreased firing for cues predicting reward. Interestingly, the same neurons also responded when reward was expected but not delivered, and could thus provide a negative reward prediction error or, alternatively, signal negative value. In addition, many cells showed motor-related response modulation. In summary, NCL neurons represent information about the reward value of specific stimuli, instrumental actions as well as action outcomes, and therefore provide signals useful for adaptive behavior in dynamically changing environments.
Highlights
Pigeons are classic model animals for the study of learning and choice, and psychological research employing pigeons as subjects forms the backbone of contemporary learning theory [1,2,3,4,5,6,7]
Converging evidence from neurochemical [13,14,15], anatomical [8,16], behavioral [10,17,18,19], and electrophysiological [20,21] studies point to functional equivalence of nidopallium caudolaterale (NCL) and mammalian prefrontal cortex that possibly results from a process of convergent evolution [9,22]
Water was available at all times; food was restricted to the period of daily testing on workdays, with additional free food available on weekends
Summary
Pigeons are classic model animals for the study of learning and choice, and psychological research employing pigeons as subjects forms the backbone of contemporary learning theory [1,2,3,4,5,6,7]. The wealth of available behavioral and neuroanatomical data renders the pigeon a highly suitable model system for behavioral neuroscientists too, few studies so far investigated single-neuron responses in pigeons during operant behavior. We examined the response properties of single neurons in the nidopallium caudolaterale (NCL) while the birds performed a perceptual decision task. The NCL is a multimodal associative forebrain area that receives input from secondary sensory areas of all modalities and projects to both limbic and sensorimotor striatum as well as premotor areas [8,9]. NCL lesions impair executive processes such as working memory and reversal learning [10,11] while leaving sensory discrimination and motor performance unaffected [12]. Converging evidence from neurochemical [13,14,15], anatomical [8,16], behavioral [10,17,18,19], and electrophysiological [20,21] studies point to functional equivalence of NCL and mammalian prefrontal cortex that possibly results from a process of convergent evolution [9,22]
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