"Prefrontal" neuronal foundations of visual asymmetries in pigeons

This study was conducted in order to reveal the possibly lateralized processes in the avian nidopallium caudolaterale (NCL), a functional analogue to the mammalian prefrontal cortex, during a color discrimination task. Pigeons are known to be visually lateralized with a superiority of the left hemisphere/right eye for visual feature discriminations. While animals were working on a color discrimination task, we recorded single visuomotor neurons in left and right NCL. As expected, pigeons learned faster and responded more quickly when seeing the stimuli with their right eyes. Our electrophysiological recordings discovered several neuronal properties of NCL neurons that possibly contributed to this behavioral asymmetry. We found that the speed of stimulus encoding was identical between left and right NCL but action generation was different. Here, most left hemispheric NCL neurons reached their peak activities shortly before response execution. In contrast, the majority of right hemispheric neurons lagged behind and came too late to control the response. Thus, the left NCL dominated the animals' behavior not by a higher efficacy of encoding, but by being faster in monopolizing the operant response. A further asymmetry concerned the hemisphere-specific integration of input from the contra- and ipsilateral eye. The left NCL was able to integrate and process visual input from the ipsilateral eye to a higher degree and thus achieved a more bilateral representation of two visual fields. We combine these novel findings with those from previous publications to come up with a working hypothesis that could explain how hemispheric asymmetries for visual feature discrimination in birds are realized by a sequential buildup of lateralized neuronal response properties in the avian forebrain

How foraging works

Food uncertainty has the effect of invigorating food-related responses. Psychologists have noted that mammals and birds respond more to a conditioned stimulus that unreliably predicts food delivery, and ecologists have shown that animals (especially small passerines) consume and/or hoard more food and can get fatter when access to that resource is unpredictable. Are these phenomena related? We think they are. Psychologists have proposed several mechanistic interpretations, while ecologists have suggested a functional interpretation: The effect of unpredictability on fat reserves and hoarding behavior is an evolutionary strategy acting against the risk of starvation when food is in short supply. Both perspectives are complementary, and we argue that the psychology of incentive motivational processes can shed some light on the causal mechanisms leading animals to seek and consume more food under uncertainty in the wild. Our theoretical approach is in agreement with neuroscientific data relating to the role of dopamine, a neurotransmitter strongly involved in incentive motivation, and its plausibility has received some explanatory and predictive value with respect to Pavlovian phenomena. Overall, we argue that the occasional and unavoidable absence of food rewards has motivational effects (called incentive hope) that facilitate foraging effort. We show that this hypothesis is computationally tenable, leading foragers in an unpredictable environment to consume more food items and to have higher long-term energy storage than foragers in a predictable environment

Stimulus-response-outcome coding in the pigeon nidopallium caudolaterale

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

Light-dependent development of the tectorotundal projection in pigeons

Left–right differences in the structural and functional organization of the brain are widespread in the animal kingdom and develop in close gene–environment interactions. The visual system of birds like chicks and pigeons exemplifies how sensory experience shapes lateralized visual processing. Owing to an asymmetrical posture of the embryo in the egg, the right eye/ left brain side is more strongly light-stimulated what triggers asymmetrical differentiation processes leading to a left-hemispheric dominance for visuomotor control. In pigeons ($\textit {Columba livia}$), a critical neuroanatomical element is the asymmetrically organized tectofugal pathway. Here, more fibres cross from the right tectum to the left rotundus than vice versa. In the current study, we tested whether the emergence of this projection asymmetry depends on embryonic light stimulation by tracing tectorotundal neurons in pigeons with and without lateralized embryonic light experience. The quantitative tracing pattern confirmed higher bilateral innervation of the left rotundus in light-exposed and thus, asymmetrically light-stimulated pigeons. This was the same in light-deprived pigeons. Here, however, also the right rotundus received an equally strong bilateral input. This suggests that embryonic light stimulation does not increase bilateral tectal innervation of the stronger stimulated left but rather decreases such an input pattern to the right brain side. Combined with a morphometric analysis, our data indicate that embryonic photic stimulation specifically affects differentiation of the contralateral cell population. Differential modification of ipsi- and contralateral tectorotundal connections could have important impact on the regulation of intra- and interhemispheric information transfer and ultimately on hemispheric dominance pattern during visual processing

Meta-control in pigeons (Columba livia)\textit {(Columba livia)} and the role of the commissura anterior

Meta-control describes an interhemispheric response conflict that results from the perception of stimuli that elicit a different reaction in each hemisphere. The dominant hemisphere for the perceived stimulus class often wins this competition. There is evidence from pigeons that meta-control results from interhemispheric response conflicts that prolong reaction time when the animal is confronted with conflicting information. However, recent evidence in pigeons also makes it likely that the dominant hemisphere can slow down the subdominant hemisphere, such that meta-control could instead result from the interhemispheric speed differences. Since both explanations make different predictions for the effect of commissurotomy, we tested pigeons in a meta-control task both before and after transection of the commissura anterior. This fiber pathway is the largest pallial commissura of the avian brain. The results revealed a transient phase in which meta-control possibly resulted from interhemispheric response conflicts. In subsequent sessions and after commissurotomy, however, the results suggest interhemispheric speed differences as a basis for meta-control. Furthermore, they reveal that meta-control is modified by interhemispheric transmission via the commissura anterior, although it does not seem to depend on it

Noradrenergic stimulation modulates activation of extinction-related brain regions and enhances contextual extinction learning without affecting renewal

Renewal in extinction learning describes the recovery of an extinguished response if the extinction context differs from the context present during acquisition and recall. Attention may have a role in contextual modulation of behavior and contribute to the renewal effect, while noradrenaline (NA) is involved in attentional processing. In this functional magnetic resonance imaging (fMRI) study we investigated the role of the noradrenergic system for behavioral and brain activation correlates of contextual extinction and renewal, with a particular focus upon hippocampus and ventromedial prefrontal cortex (PFC), which have crucial roles in processing of renewal. Healthy human volunteers received a single dose of the NA reuptake inhibitor atomoxetine prior to extinction learning. During extinction of previously acquired cue-outcome associations, cues were presented in a novel context (ABA) or in the acquisition context (AAA). In recall, all cues were again presented in the acquisition context. Atomoxetine participants (ATO) showed significantly faster extinction compared to placebo (PLAC). However, atomoxetine did not affect renewal. Hippocampal activation was higher in ATO during extinction and recall, as was ventromedial PFC activation, except for ABA recall. Moreover, ATO showed stronger recruitment of insula, anterior cingulate, and dorsolateral/orbitofrontal PFC. Across groups, cingulate, hippocampus and vmPFC activity during ABA extinction correlated with recall performance, suggesting high relevance of these regions for processing the renewal effect. In summary, the noradrenergic system appears to be involved in the modification of established associations during extinction learning and thus has a role in behavioral flexibility. The assignment of an association to a context and the subsequent decision on an adequate response, however, presumably operate largely independently of noradrenergic mechanisms

Lateralization of auditory processing of Silbo Gomero

Left-hemispheric language dominance is a well-known characteristic of the human language system. However, it has been shown that leftward language lateralization decreases dramatically when people communicate using whistles. Whistled languages present a transformation of a spoken language into whistles, facilitating communication over great distances. In order to investigate the laterality of Silbo Gomero, a form of whistled Spanish, we used a vocal and a whistled dichotic listening task in a sample of 75 healthy Spanish speakers. Both individuals that were able to whistle and to understand Silbo Gomero and a non-whistling control group showed a clear right-ear advantage for vocal dichotic listening. For whistled dichotic listening, the control group did not show any hemispheric asymmetries. In contrast, the whistlers' group showed a right-ear advantage for whistled stimuli. This right-ear advantage was, however, smaller compared to the right-ear advantage found for vocal dichotic listening. In line with a previous study on language lateralization of whistled Turkish, these findings suggest that whistled language processing is associated with a decrease in left and a relative increase in right hemispheric processing. This shows that bihemispheric processing of whistled language stimuli occurs independent of language

Plasticity in D1-like receptor expression is associated with different components of cognitive processes

Dopamine D1-like receptors consist of D1 (D1A) and D5 (D1B) receptors and play a key role in working memory. However, their possibly differential contribution to working memory is unclear. We combined a working memory training protocol with a stepwise increase of cognitive subcomponents and real-time RT-PCR analysis of dopamine receptor expression in pigeons to identify molecular changes that accompany training of isolated cognitive subfunctions. In birds, the D1-like receptor family is extended and consists of the D1A, D1B, and D1D receptors. Our data show that D1B receptor plasticity follows a training that includes active mental maintenance of information, whereas D1A and D1D receptor plasticity in addition accompanies learning of stimulus-response associations. Plasticity of D1-like receptors plays no role for processes like response selection and stimulus discrimination. None of the tasks altered D2 receptor expression. Our study shows that different cognitive components of working memory training have distinguishable effects on D1-like receptor expression

Empathy moderates the effect of repetitive transcranial magnetic stimulation of the right dorsolateral prefrontal cortex on costly punishment

Humans incur considerable costs to punish unfairness directed towards themselves or others. Recent studies using repetitive transcranial magnetic stimulation (rTMS) suggest that the right dorsolateral prefrontal cortex (DLPFC) is causally involved in such strategic decisions. Presently, two partly divergent hypotheses are discussed, suggesting either that the right DLPFC is necessary to control selfish motives by implementing culturally transmitted social norms, or is involved in suppressing emotion-driven prepotent responses to perceived unfairness. Accordingly, we studied the role of the DLPFC in costly (i.e. third party) punishment by applying rTMS to the left and right DLPFC before playing a Dictator Game with the option to punish observed unfair behavior (DG-P). In addition, sham stimulation took place. Individual differences in empathy were assessed with the German version of the Interpersonal Reactivity Index. Costly punishment increased (non-significantly) upon disruption of the right – but not the left – DLPFC as compared to sham stimulation. However, empathy emerged as a highly significant moderator variable of the effect of rTMS over the right, but not left, DLPFC, suggesting that the right DLPFC is involved in controlling prepotent emotional responses to observed unfairness, depending on individual differences in empathy

Brain activation in motor sequence learning is related to the level of native cortical excitability

Cortical excitability may be subject to changes through training and learning. Motor training can increase cortical excitability in motor cortex, and facilitation of motor cortical excitability has been shown to be positively correlated with improvements in performance in simple motor tasks. Thus cortical excitability may tentatively be considered as a marker of learning and use-dependent plasticity. Previous studies focused on changes in cortical excitability brought about by learning processes, however, the relation between native levels of cortical excitability on the one hand and brain activation and behavioral parameters on the other is as yet unknown. In the present study we investigated the role of differential native motor cortical excitability for learning a motor sequencing task with regard to post-training changes in excitability, behavioral performance and involvement of brain regions. Our motor task required our participants to reproduce and improvise over a pre-learned motor sequence. Over both task conditions, participants with low cortical excitability (CElo) showed significantly higher BOLD activation in task-relevant brain regions than participants with high cortical excitability (CEhi). In contrast, CElo and CEhi groups did not exhibit differences in percentage of correct responses and improvisation level. Moreover, cortical excitability did not change significantly after learning and training in either group, with the exception of a significant decrease in facilitatory excitability in the CEhi group. The present data suggest that the native, unmanipulated level of cortical excitability is related to brain activation intensity, but not to performance quality. The higher BOLD mean signal intensity during the motor task might reflect a compensatory mechanism in CElo participants