Jonas Rose

Neural Correlates of Executive Control in the Avian Brain

Executive control, the ability to plan ones behaviour to achieve a goal, is a hallmark of frontal lobe function in humans and other primates. In the current study we report neural correlates of executive control in the avian nidopallium caudolaterale, a region analogous to the mammalian prefrontal cortex. Homing pigeons (Columba livia) performed a working memory task in which cues instructed them whether stimuli should be remembered or forgotten. When instructed to remember, many neurons showed sustained activation throughout the memory period. When instructed to forget, the sustained activation was abolished. Consistent with the neural data, the behavioural data showed that memory performance was high after instructions to remember, and dropped to chance after instructions to forget. Our findings indicate that neurons in the avian nidopallium caudolaterale participate in one of the core forms of executive control, the control of what should be remembered and what should be forgotten. This form of executive control is fundamental not only to working memory, but also to all cognition.

The Biopsychology-Toolbox: a free, open-source Matlab-toolbox for the control of behavioral experiments.

The Biopsychology-Toolbox is a free, open-source Matlab-toolbox for the control of behavioral experiments. The major aim of the project was to provide a set of basic tools that allow programming novices to control basic hardware used for behavioral experimentation without limiting the power and flexibility of the underlying programming language. The modular design of the toolbox allows portation of parts as well as entire paradigms between different types of hardware. In addition to the toolbox, this project offers a platform for the exchange of functions, hardware solutions and complete behavioral paradigms.

Dopamine modulation of learning and memory in the prefrontal cortex: insights from studies in primates, rodents, and birds

In this review, we provide a brief overview over the current knowledge about the role of dopamine transmission in the prefrontal cortex during learning and memory. We discuss work in humans, monkeys, rats, and birds in order to provide a basis for comparison across species that might help identify crucial features and constraints of the dopaminergic system in executive function. Computational models of dopamine function are introduced to provide a framework for such a comparison. We also provide a brief evolutionary perspective showing that the dopaminergic system is highly preserved across mammals. Even birds, following a largely independent evolution of higher cognitive abilities, have evolved a comparable dopaminergic system. Finally, we discuss the unique advantages and challenges of using different animal models for advancing our understanding of dopamine function in the healthy and diseased brain.

Disentangling the relationship between hemispheric asymmetry and cognitive performance

It is widely believed that advantages of hemispheric asymmetries originated in better cognitive processing, hence it is often implied that the relationship between hemispheric asymmetry and cognitive performance is linearly positive: the higher the degree of lateralization in a specific cognitive domain, the better the performance in a corresponding task. Yet, the empirical evidence for this notion is mixed and the statistical methods to analyze this relationship have been criticized. The present study therefore investigated the relationship between hemispheric asymmetries and cognitive performance in two behavioral tasks (a left-lateralized word-matching task and a right-lateralized face-decision task) in 230 participants (140 women, 90 men) by using two different approaches. Both methods correspondingly revealed that a relationship between hemispheric asymmetries and cognitive performance does exist. Contrary to a positive (linear) relationship however, the data could be best described by an inverted U-shaped curve. Although the optimal degree of lateralization seemed to be task-specific, a slight or moderate degree of hemispheric asymmetry achieved best cognitive performance in all tasks. Moreover, performances deteriorated towards extreme ends of lateralization (i.e., participants with either extreme left or right hemispheric biases). Taken together, the present study provides evidence against the notion that higher lateralization is related to enhanced cognitive performance.

The role of dopamine in maintenance and distractability of attention in the “prefrontal cortex” of pigeons

Selective attention is a crucial component of all sensory processing. Here we test the role of dopamine in attentional selection and in the maintenance of attention. Pigeons were trained on a moving-dot paradigm comparable to the shell game. In this paradigm, pigeons had to select a target among distractors and maintain attention to the target. Target and distractors consisted of white dots, moving at random on a touch-screen. In this task, the demand on attention was modulated by varying the number of distractors and the duration of motion. Both manipulations affected performance equally. In the next step, we investigated the contribution of dopamine to attention. Intracranial injections of D1-antagonist (Sch23390) before testing led to decrements in performance that equally affected trials with different attentional demand. This drop in performance cannot be attributed to altered motivation or motor performance. We conclude that dopamine has a critical role in attention. It is involved in the selection of targets for attention and in the stabilization of attention against interference. This is comparable to the role dopamine plays in working memory and argues for similar mechanisms underlying selective attention and working memory.

A method for the evaluation of intracranial tetrodotoxin injections

Tetrodotoxin is one of the most potent and oldest known neurotoxins. It acts by blocking the voltage-gated sodium channels in nerve cell membranes, leading to a transient silencing of neural activity. TTX is among the most widely used pharmacological agents for the temporary and selective blocking of neural structures. As such, an exact knowledge of the spatial and temporal diffusion gradient of TTX is important when planning pharmacological interventions. Here we report a method for the direct assessment of spatio-temporal TTX diffusion gradients using immunohistochemistry. TTX injections were performed in vivo via chronically implanted guiding cannulae, placed bilaterally in the dorsal entopallium of pigeons. To determine the temporal spread, animals were perfused at different time points after TTX injections. For visualization of the TTX affected area an immunohistochemical protocol was developed. The extension of staining was assessed 1h after injection when TTX was diffused over 3mm in all directions. TTX immunolabeling could be detected for up to 32 h; after 48 h no staining was found. Our findings provide a better understanding of the temporal decay and spread of intracranial TTX injections, thereby allowing a more reliable estimation of size and duration of TTX-effects.

Peck tracking: a method for localizing critical features within complex pictures for pigeons

The pigeon is a standard animal in comparative psychology and is frequently used to investigate visuocognitive functions. Nonetheless, the strategies that pigeons use to discriminate complex visual stimuli remain a difficult area of study. In search of a reliable method to identify features that control the discrimination behaviour, pecking location was tracked using touch screen technology in a people-absent/people-present discrimination task. The correct stimuli contained human figures anywhere on the picture, but the birds were not required to peck on that part. However, the stimuli were designed in a way that only the human figures contained distinguishing information. All pigeons focused their pecks on a subarea of the distinctive human figures, namely the heads. Removal of the heads significantly impaired performance, while removal of other distinctive parts did not. Thus, peck tracking reveals the location within a complex visual stimulus that controls discrimination behaviour, and might be a valuable tool to reveal the strategies pigeons apply in visual discrimination tasks.

Striatal dopamine D1 receptors are involved in the dissociation of learning based on reward-magnitude.

Here we investigate the contribution of striatal dopamine receptors (D1) to the influence of reward-magnitude on learning. Pigeons (Columba livia) were trained on a discrimination-task with two pairs of stimuli; correct discrimination resulted in a large reward in one pair of stimuli and in a small reward in the other pair. Acquisition of the discrimination-task was accompanied by intracranial injections to the medial striatum, either of a dopamine-antagonist (Sch23390) or of vehicle. In the control-condition the rate of learning was modulated by the magnitude of the reward; discrimination was learned faster if contingent rewards were large and learning was slower if contingent rewards were small. Following injections of D1 antagonist this effect vanished even though the ability to discriminate between the rewards was unaffected. Interestingly, the mean rate of learning was indistinguishable between the control and antagonist conditions. Consequently, it appears that not learning per se but the effect of reward-magnitude on learning is mediated through D1 receptors in the striatum. We argue that the injections of dopamine-antagonist cause a shift in strategy underlying learning. In the control-condition animals rely on positive feedback and thus learning is affected by the magnitude of the contingent reward; in the antagonist-condition, however, learning might rely on negative feedback and is thus insensitive to reward-magnitude.

Sustained activation and executive control in the avian prefrontal cortex

We review our studies examining neural correlates of directed forgetting and executive control in the avian prefrontal cortex. One of the fundamental forms of executive control is the ability to selectively filter information, retaining that which is critical for the current purposes and discarding that which is not. In our first experiment, we trained birds on a directed-forgetting version of a delayed matching-to-sample task. Following a sample stimulus, a bird heard either a remember tone indicating that a memory test would follow, or a forget tone indicating that no memory test would be given. We found that neural activity in the avian prefrontal cortex increased when the bird was told to remember, and decreased when the bird was told to forget. Behavioral probe tests confirmed that the animals were forgetting on forget trials. Although the sustained activation observed on remember trials and the absence of such activation on forget trials could be a code of remembering and forgetting the sample stimulus, it could also be a code of the possibility of obtaining a reward. To address this issue we conducted a second study in which we used three cues: remember, forget, and forget-reward. The forget-reward cue instructed the subject to forget the sample yet at the same time provided a free reward. Neural activity on forget-reward trials matched that on remember trials tentatively indicating that the sustained activation on remember trials might be a reward code rather than a sample stimulus code. Behavioral probe tests, however, failed to indicate that the animals were forgetting on forget-reward trials, and hence it still is possible that the sustained activation could be a code for memory of the sample stimulus.

Crows Rival Monkeys in Cognitive Capacity

The present study compares the ‘bandwidth of cognition’ between crows and primates. Working memory is the ability to maintain and manipulate information over short periods of time – a core component of cognition. The capacity of working memory is tightly limited, in humans correlated with individual intelligence and commonly used synonymously with cognitive capacity. Crows have remarkable cognitive skills and while birds and mammals share neural principles of working memory, its capacity has not been tested in crows. Here we report the performance of two carrion crows on a working memory paradigm adapted from a recent experiment in rhesus monkeys. Capacity of crows is remarkably similar to monkeys and estimated at about four items. In both species, the visual hemifields show largely independent capacity. These results show that crows, like primates evolved a high-capacity working memory that reflects the result of convergent evolution of higher cognitive abilities in both species.