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1.  An fMRI investigation of expectation violation in magic tricks 
Magic tricks violate the expected causal relationships that form an implicit belief system about what is possible in the world around us. Observing a magic effect seemingly invalidates our implicit assumptions about what action causes which outcome. We aimed at identifying the neural correlates of such expectation violations by contrasting 24 video clips of magic tricks with 24 control clips in which the expected action-outcome relationship is upheld. Using fMRI, we measured the brain activity of 25 normal volunteers while they watched the clips in the scanner. Additionally, we measured the professional magician who had performed the magic tricks under the assumption that, in contrast to naïve observers, the magician himself would not perceive his own magic tricks as an expectation violation. As the main effect of magic – control clips in the normal sample, we found higher activity for magic in the head of the caudate nucleus (CN) bilaterally, the left inferior frontal gyrus and the left anterior insula. As expected, the magician’s brain activity substantially differed from these results, with mainly parietal areas (supramarginal gyrus bilaterally) activated, supporting our hypothesis that he did not experience any expectation violation. These findings are in accordance with previous research that has implicated the head of the CN in processing changes in the contingency between action and outcome, even in the absence of reward or feedback.
PMCID: PMC4316608
expectation violation; magic; fMRI; caudate nucleus; perceptual prediction error; movement observation; action
2.  It's a kind of magic—what self-reports can reveal about the phenomenology of insight problem solving 
Frontiers in Psychology  2014;5:1408.
Magic tricks usually remain a mystery to the observer. For the sake of science, we offered participants the opportunity to discover the magician's secret method by repeatedly presenting the same trick and asking them to find out how the trick worked. In the context of insightful problem solving, the present work investigated the emotions that participants experience upon solving a magic trick. We assumed that these emotions form the typical “Aha! experience” that accompanies insightful solutions to difficult problems. We aimed to show that Aha! experiences can be triggered by magic tricks and to systematically explore the phenomenology of the Aha! experience by breaking it down into five previously postulated dimensions. 34 video clips of different magic tricks were presented up to three times to 50 participants who had to find out how the trick was accomplished, and to indicate whether they had experienced an Aha! during the solving process. Participants then performed a comprehensive quantitative and qualitative assessment of their Aha! experiences which was repeated after 14 days to control for its reliability. 41% of all suggested solutions were accompanied by an Aha! experience. The quantitative assessment remained stable across time in all five dimensions. Happiness was rated as the most important dimension. This primacy of positive emotions was also reflected in participants' qualitative self-reports which contained more emotional than cognitive aspects. Implementing magic tricks as problem solving task, we could show that strong Aha! experiences can be triggered if a trick is solved. We could at least partially capture the phenomenology of Aha! by identifying one prevailing aspect (positive emotions), a new aspect (release of tension upon gaining insight into a magic trick) and one less important aspect (impasse).
PMCID: PMC4258999  PMID: 25538658
insight; problem solving; magic; Aha! experience; impasse
3.  Neuronal Adaptation Translates Stimulus Gaps into a Population Code 
PLoS ONE  2014;9(4):e95705.
Neurons in sensory pathways exhibit a vast multitude of adaptation behaviors, which are assumed to aid the encoding of temporal stimulus features and provide the basis for a population code in higher brain areas. Here we study the transition to a population code for auditory gap stimuli both in neurophysiological recordings and in a computational network model. Independent component analysis (ICA) of experimental data from the inferior colliculus of Mongolian gerbils reveals that the network encodes different gap sizes primarily with its population firing rate within 30 ms after the presentation of the gap, where longer gap size evokes higher network activity. We then developed a computational model to investigate possible mechanisms of how to generate the population code for gaps. Phenomenological (ICA) and functional (discrimination performance) analyses of our simulated networks show that the experimentally observed patterns may result from heterogeneous adaptation, where adaptation provides gap detection at the single neuron level and neuronal heterogeneity ensures discriminable population codes for the whole range of gap sizes in the input. Furthermore, our work suggests that network recurrence additionally enhances the network's ability to provide discriminable population patterns.
PMCID: PMC3997522  PMID: 24759970
4.  Nitric oxide signaling modulates synaptic inhibition in the superior paraolivary nucleus (SPN) via cGMP-dependent suppression of KCC2 
Glycinergic inhibition plays a central role in the auditory brainstem circuitries involved in sound localization and in the encoding of temporal action potential firing patterns. Modulation of this inhibition has the potential to fine-tune information processing in these networks. Here we show that nitric oxide (NO) signaling in the auditory brainstem (where activity-dependent generation of NO is documented) modulates the strength of inhibition by changing the chloride equilibrium potential. Recent evidence demonstrates that large inhibitory postsynaptic currents (IPSCs) in neurons of the superior paraolivary nucleus (SPN) are enhanced by a very low intracellular chloride concentration, generated by the neuronal potassium chloride co-transporter (KCC2) expressed in the postsynaptic neurons. Our data show that modulation by NO caused a 15 mV depolarizing shift of the IPSC reversal potential, reducing the strength of inhibition in SPN neurons, without changing the threshold for action potential firing. Regulating inhibitory strength, through cGMP-dependent changes in the efficacy of KCC2 in the target neuron provides a postsynaptic mechanism for rapidly controlling the inhibitory drive, without altering the timing or pattern of the afferent spike train. Therefore, this NO-mediated suppression of KCC2 can modulate inhibition in one target nucleus (SPN), without influencing inhibitory strength of other target nuclei (MSO, LSO) even though they are each receiving collaterals from the same afferent nucleus (a projection from the medial nucleus of the trapezoid body, MNTB).
PMCID: PMC4060731  PMID: 24987336
nitric oxide; KCC2; post-inhibitory rebound; gap-detection; auditory brainstem
5.  The natural history of sound localization in mammals – a story of neuronal inhibition 
Our concepts of sound localization in the vertebrate brain are widely based on the general assumption that both the ability to detect air-borne sounds and the neuronal processing are homologous in archosaurs (present day crocodiles and birds) and mammals. Yet studies repeatedly report conflicting results on the neuronal circuits and mechanisms, in particular the role of inhibition, as well as the coding strategies between avian and mammalian model systems. Here we argue that mammalian and avian phylogeny of spatial hearing is characterized by a convergent evolution of hearing air-borne sounds rather than by homology. In particular, the different evolutionary origins of tympanic ears and the different availability of binaural cues in early mammals and archosaurs imposed distinct constraints on the respective binaural processing mechanisms. The role of synaptic inhibition in generating binaural spatial sensitivity in mammals is highlighted, as it reveals a unifying principle of mammalian circuit design for encoding sound position. Together, we combine evolutionary, anatomical and physiological arguments for making a clear distinction between mammalian processing mechanisms and coding strategies and those of archosaurs. We emphasize that a consideration of the convergent nature of neuronal mechanisms will significantly increase the explanatory power of studies of spatial processing in both mammals and birds.
PMCID: PMC4181121  PMID: 25324726
MSO; LSO; evolution; glycine; GABA; archosaurs; birds; binaural hearing
6.  Metabolic Maturation of Auditory Neurones in the Superior Olivary Complex 
PLoS ONE  2013;8(6):e67351.
Neuronal activity is energetically costly, but despite its importance, energy production and consumption have been studied in only a few neurone types. Neuroenergetics is of special importance in auditory brainstem nuclei, where neurones exhibit various biophysical adaptations for extraordinary temporal precision and show particularly high firing rates. We have studied the development of energy metabolism in three principal nuclei of the superior olivary complex (SOC) involved in precise binaural processing in the Mongolian gerbil (Meriones unguiculatus). We used immunohistochemistry to quantify metabolic markers for energy consumption (Na+/K+-ATPase) and production (mitochondria, cytochrome c oxidase activity and glucose transporter 3 (GLUT3)). In addition, we calculated neuronal ATP consumption for different postnatal ages (P0–90) based upon published electrophysiological and morphological data. Our calculations relate neuronal processes to the regeneration of Na+ gradients perturbed by neuronal firing, and thus to ATP consumption by Na+/K+-ATPase. The developmental changes of calculated energy consumption closely resemble those of metabolic markers. Both increase before and after hearing onset occurring at P12–13 and reach a plateau thereafter. The increase in Na+/K+-ATPase and mitochondria precedes the rise in GLUT3 levels and is already substantial before hearing onset, whilst GLUT3 levels are scarcely detectable at this age. Based on these findings we assume that auditory inputs crucially contribute to metabolic maturation. In one nucleus, the medial nucleus of the trapezoid body (MNTB), the initial rise in marker levels and calculated ATP consumption occurs distinctly earlier than in the other nuclei investigated, and is almost completed by hearing onset. Our study shows that the mathematical model used is applicable to brainstem neurones. Energy consumption varies markedly between SOC nuclei with their different neuronal properties. Especially for the medial superior olive (MSO), we propose that temporally precise input integration is energetically more costly than the high firing frequencies typical for all SOC nuclei.
PMCID: PMC3694961  PMID: 23826275
7.  Sound Localization in Noise by Gerbils and Humans 
Detection and localization of a target sound in the presence of concurrent, spatially distributed masking sounds is one of the most challenging tasks for the mammalian auditory system. Previous studies demonstrated that the ability to localize signals is decreased by interfering noise. In order to directly compare the behavioral performance in a signal processing task in noise between gerbils and humans in the free sound field, we quantified their localization ability for a low-frequency signal in the presence of six masking noise sources surrounding the subject. Thresholds were measured both for masking noises that were correlated or uncorrelated across the masking sources. Overall, the gerbils required a higher signal/noise ratio to detect the low-frequency signal than the humans; that is, the behavioral performance of the gerbils was considerably worse than that of the humans. Moreover, switching from maskers that were uncorrelated across the masking sources to correlated maskers resulted in more masking in gerbils but in a release from masking in humans. These results would suggest that the gerbil may not be a good animal model for binaural processing. However, simulations of the localization thresholds in a numerical model of binaural processing in gerbils and humans reveal that both the inferior overall performance in gerbils and the opposite effect of masker correlation on the detection thresholds can be attributed to the smaller head size and the wider peripheral auditory filters in gerbils. Thus, the current data indicate that the binaural processor itself (i.e., the evaluation of signals coming from the two ears) is equally sensitive in gerbils and humans. However, the physical limitations imposed by the small head prevent the gerbil from performing equally well in the current paradigm.
PMCID: PMC3298617  PMID: 22245918
unmasking; BMLD; binaural hearing; signal detection; binaural modeling
8.  Frequency-Invariant Representation of Interaural Time Differences in Mammals 
PLoS Computational Biology  2011;7(3):e1002013.
Interaural time differences (ITDs) are the major cue for localizing low-frequency sounds. The activity of neuronal populations in the brainstem encodes ITDs with an exquisite temporal acuity of about . The response of single neurons, however, also changes with other stimulus properties like the spectral composition of sound. The influence of stimulus frequency is very different across neurons and thus it is unclear how ITDs are encoded independently of stimulus frequency by populations of neurons. Here we fitted a statistical model to single-cell rate responses of the dorsal nucleus of the lateral lemniscus. The model was used to evaluate the impact of single-cell response characteristics on the frequency-invariant mutual information between rate response and ITD. We found a rough correspondence between the measured cell characteristics and those predicted by computing mutual information. Furthermore, we studied two readout mechanisms, a linear classifier and a two-channel rate difference decoder. The latter turned out to be better suited to decode the population patterns obtained from the fitted model.
Author Summary
Neuronal codes are usually studied by estimating how much information the brain activity carries about the stimulus. On a single cell level, the relevant features of neuronal activity such as the firing rate or spike timing are readily available. On a population level, where many neurons together encode a stimulus property, finding the most appropriate activity features is less obvious, particularly because the neurons respond with a huge cell-to-cell variability. Here, using the example of the neuronal representation of interaural time differences, we show that the quality of the population code strongly depends on the assumption — or the model — of the population readout. We argue that invariances are useful constraints to identify “good” population codes. Based on these ideas, we suggest that the representation of interaural time differences serves a two-channel code in which the difference between the summed activities of the neurons in the two hemispheres exhibits an invariant and linear dependence on interaural time difference.
PMCID: PMC3060160  PMID: 21445227
9.  The Long Adventurous Journey of Rhombic Lip Cells in Jawed Vertebrates: A Comparative Developmental Analysis 
This review summarizes vertebrate rhombic lip and early cerebellar development covering classic approaches up to modern developmental genetics which identifies the relevant differential gene expression domains and their progeny. Most of this information is derived from amniotes. However, progress in anamniotes, particularly in the zebrafish, has recently been made. The current picture suggests that rhombic lip and cerebellar development in jawed vertebrates (gnathostomes) share many characteristics. Regarding cerebellar development, these include a ptf1a expressing ventral cerebellar proliferation (VCP) giving rise to Purkinje cells and other inhibitory cerebellar cell types, and an atoh1 expressing upper rhombic lip giving rise to an external granular layer (EGL, i.e., excitatory granule cells) and an early ventral migration into the anterior rhombencephalon (cholinergic nuclei). As for the lower rhombic lip (LRL), gnathostome commonalities likely include the formation of precerebellar nuclei (mossy fiber origins) and partially primary auditory nuclei (likely convergently evolved) from the atoh1 expressing dorsal zone. The fate of the ptf1a expressing ventral LRL zone which gives rise to (excitatory cells of) the inferior olive (climbing fiber origin) and (inhibitory cells of ) cochlear nuclei in amniotes, has not been determined in anamniotes. Special for the zebrafish in comparison to amniotes is the predominant origin of anamniote excitatory deep cerebellar nuclei homologs (i.e., eurydendroid cells) from ptf1a expressing VCP cells, the sequential activity of various atoh1 paralogs and the incomplete coverage of the subpial cerebellar plate with proliferative EGL cells. Nevertheless, the conclusion that a rhombic lip and its major derivatives evolved with gnathostome vertebrates only and are thus not an ancestral craniate character complex is supported by the absence of a cerebellum (and likely absence of its afferent and efferent nuclei) in jawless fishes
PMCID: PMC3085262  PMID: 21559349
atoh1; cerebellum; cochlear nuclei; precerebellar systems; ptf1a; wnt1; zebrafish; rhombic lip
10.  Dynamic Changes in Level Influence Spatial Coding in the Lateral Superior Olive 
Hearing research  2007;238(1-2):58-67.
It is well established that the responses of binaural auditory neurons can adapt and change dramatically depending on the nature of a preceding sound. Examples of how the effects of ensuing stimuli play a functional role in auditory processing include motion sensitivity and precedence-like effects. To date, these types of effects have been documented at the level of the midbrain and above. Little is known about sensitivity to ensuing stimuli below in the superior olivary nuclei where binaural response properties are first established. Here we report on single cell responses in the gerbil lateral superior olive, the initial site where sensitivity to interaural level differences is established. In contrast to our expectations we found a robust sensitivity to ensuing stimuli. The majority of the cells we tested (86%), showed substantial suppression and/or enhancement to a designated target stimulus, depending on the nature of a preceding stimulus. Hence, sensitivity to ensuing stimuli is already established at the first synaptic station of binaural processing.
PMCID: PMC2398711  PMID: 18162347
Binaural; Sound Localization; Interaural Level Difference
11.  Efficient Temporal Processing of Naturalistic Sounds 
PLoS ONE  2008;3(2):e1655.
In this study, we investigate the ability of the mammalian auditory pathway to adapt its strategy for temporal processing under natural stimulus conditions. We derive temporal receptive fields from the responses of neurons in the inferior colliculus to vocalization stimuli with and without additional ambient noise. We find that the onset of ambient noise evokes a change in receptive field dynamics that corresponds to a change from bandpass to lowpass temporal filtering. We show that these changes occur within a few hundred milliseconds of the onset of the noise and are evident across a range of overall stimulus intensities. Using a simple model, we illustrate how these changes in temporal processing exploit differences in the statistical properties of vocalizations and ambient noises to increase the information in the neural response in a manner consistent with the principles of efficient coding.
PMCID: PMC2249929  PMID: 18301738
12.  Glycinergic inhibition tunes coincidence detection in the auditory brainstem 
Nature Communications  2014;5:3790.
Neurons in the medial superior olive (MSO) detect microsecond differences in the arrival time of sounds between the ears (interaural time differences or ITDs), a crucial binaural cue for sound localization. Synaptic inhibition has been implicated in tuning ITD sensitivity, but the cellular mechanisms underlying its influence on coincidence detection are debated. Here we determine the impact of inhibition on coincidence detection in adult Mongolian gerbil MSO brain slices by testing precise temporal integration of measured synaptic responses using conductance-clamp. We find that inhibition dynamically shifts the peak timing of excitation, depending on its relative arrival time, which in turn modulates the timing of best coincidence detection. Inhibitory control of coincidence detection timing is consistent with the diversity of ITD functions observed in vivo and is robust under physiologically relevant conditions. Our results provide strong evidence that temporal interactions between excitation and inhibition on microsecond timescales are critical for binaural processing.
Coincidence detector neurons in the mammalian brainstem encode interaural time differences (ITDs) that are implicated in auditory processing. Myoga et al. study a previously developed neuronal model and find that inhibition is crucial for sound localization, but more dynamically than previously thought.
PMCID: PMC4024823  PMID: 24804642

Results 1-12 (12)